Research

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Open AccessArticle

Toxic Cyanobacterial Bloom Triggers in Missisquoi Bay, Lake Champlain, as Determined by Next-Generation Sequencing and Quantitative PCR

by Nathalie Fortin, Valentina Munoz-Ramos, David Bird, Benoît Lévesque, Lyle G. Whyte and Charles W. Greer

Life 2015, 5(2), 1346-1380; https://doi.org/10.3390/life5021346 - 12 May 2015

Cited by 26 | Viewed by 8580

Abstract

Missisquoi Bay (MB) is a temperate eutrophic freshwater lake that frequently experiences toxic Microcystis-dominated cyanobacterial blooms. Non-point sources are responsible for the high concentrations of phosphorus and nitrogen in the bay. This study combined data from environmental parameters, E. coli counts, high-throughput [...] Read more.

Missisquoi Bay (MB) is a temperate eutrophic freshwater lake that frequently experiences toxic Microcystis-dominated cyanobacterial blooms. Non-point sources are responsible for the high concentrations of phosphorus and nitrogen in the bay. This study combined data from environmental parameters, E. coli counts, high-throughput sequencing of 16S rRNA gene amplicons, quantitative PCR (16S rRNA and mcyD genes) and toxin analyses to identify the main bloom-promoting factors. In 2009, nutrient concentrations correlated with E. coli counts, abundance of total cyanobacterial cells, Microcystis 16S rRNA and mcyD genes and intracellular microcystin. Total and dissolved phosphorus also correlated significantly with rainfall. The major cyanobacterial taxa were members of the orders Chroococcales and Nostocales. The genus Microcystis was the main mcyD-carrier and main microcystin producer. Our results suggested that increasing nutrient concentrations and total nitrogen:total phosphorus (TN:TP) ratios approaching 11:1, coupled with an increase in temperature, promoted Microcystis-dominated toxic blooms. Although the importance of nutrient ratios and absolute concentrations on cyanobacterial and Microcystis dynamics have been documented in other laboratories, an optimum TN:TP ratio for Microcystis dominance has not been previously observed in situ. This observation provides further support that nutrient ratios are an important determinant of species composition in natural phytoplankton assemblages. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Open AccessArticle

Amino Acid Transporters and Release of Hydrophobic Amino Acids in the Heterocyst-Forming Cyanobacterium Anabaena sp. Strain PCC 7120

by Rafael Pernil, Silvia Picossi, Antonia Herrero, Enrique Flores and Vicente Mariscal

Life 2015, 5(2), 1282-1300; https://doi.org/10.3390/life5021282 - 23 Apr 2015

Cited by 18 | Viewed by 7913

Abstract

Anabaena sp. strain PCC 7120 is a filamentous cyanobacterium that can use inorganic compounds such as nitrate or ammonium as nitrogen sources. In the absence of combined nitrogen, it can fix N₂ in differentiated cells called heterocysts. Anabaena also shows substantial activities [...] Read more.

Anabaena sp. strain PCC 7120 is a filamentous cyanobacterium that can use inorganic compounds such as nitrate or ammonium as nitrogen sources. In the absence of combined nitrogen, it can fix N₂ in differentiated cells called heterocysts. Anabaena also shows substantial activities of amino acid uptake, and three ABC-type transporters for amino acids have been previously characterized. Seven new loci encoding predicted amino acid transporters were identified in the Anabaena genomic sequence and inactivated. Two of them were involved in amino acid uptake. Locus alr2535-alr2541 encodes the elements of a hydrophobic amino acid ABC-type transporter that is mainly involved in the uptake of glycine. ORF all0342 encodes a putative transporter from the dicarboxylate/amino acid:cation symporter (DAACS) family whose inactivation resulted in an increased uptake of a broad range of amino acids. An assay to study amino acid release from Anabaena filaments to the external medium was set up. Net release of the alanine analogue α-aminoisobutyric acid (AIB) was observed when transport system N-I (a hydrophobic amino acid ABC-type transporter) was engaged in the uptake of a specific substrate. The rate of AIB release was directly proportional to the intracellular AIB concentration, suggesting leakage from the cells by diffusion. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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1075 KiB

Open AccessArticle

Modeling the Role of pH on Baltic Sea Cyanobacteria

by Jana Hinners, Richard Hofmeister and Inga Hense

Life 2015, 5(2), 1204-1217; https://doi.org/10.3390/life5021204 - 30 Mar 2015

Cited by 12 | Viewed by 6237

Abstract

We simulate pH-dependent growth of cyanobacteria with an ecosystem model for the central Baltic Sea. Four model components—a life cycle model of cyanobacteria, a biogeochemical model, a carbonate chemistry model and a water column model—are coupled via the framework for aquatic biogeochemical models. [...] Read more.

We simulate pH-dependent growth of cyanobacteria with an ecosystem model for the central Baltic Sea. Four model components—a life cycle model of cyanobacteria, a biogeochemical model, a carbonate chemistry model and a water column model—are coupled via the framework for aquatic biogeochemical models. The coupled model is forced by the output of a regional climate model, based on the A1B emission scenario. With this coupled model, we perform simulations for the period 1968–2098. Our simulation experiments suggest that in the future, cyanobacteria growth is hardly affected by the projected pH decrease. However, in the simulation phase prior to 1980, cyanobacteria growth and N₂-fixation are limited by the relatively high pH. The observed absence of cyanobacteria before the 1960s may thus be explained not only by lower eutrophication levels, but also by a higher alkalinity. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Open AccessArticle

Advances in Understanding Carboxysome Assembly in Prochlorococcus and Synechococcus Implicate CsoS2 as a Critical Component

by Fei Cai, Zhicheng Dou, Susan L. Bernstein, Ryan Leverenz, Eric B. Williams, Sabine Heinhorst, Jessup Shively, Gordon C. Cannon and Cheryl A. Kerfeld

Life 2015, 5(2), 1141-1171; https://doi.org/10.3390/life5021141 - 27 Mar 2015

Cited by 68 | Viewed by 13048

Abstract

The marine Synechococcus and Prochlorococcus are the numerically dominant cyanobacteria in the ocean and important in global carbon fixation. They have evolved a CO₂-concentrating-mechanism, of which the central component is the carboxysome, a self-assembling proteinaceous organelle. Two types of carboxysome, α [...] Read more.

The marine Synechococcus and Prochlorococcus are the numerically dominant cyanobacteria in the ocean and important in global carbon fixation. They have evolved a CO₂-concentrating-mechanism, of which the central component is the carboxysome, a self-assembling proteinaceous organelle. Two types of carboxysome, α and β, encapsulating form IA and form IB d-ribulose-1,5-bisphosphate carboxylase/oxygenase, respectively, differ in gene organization and associated proteins. In contrast to the β-carboxysome, the assembly process of the α-carboxysome is enigmatic. Moreover, an absolutely conserved α-carboxysome protein, CsoS2, is of unknown function and has proven recalcitrant to crystallization. Here, we present studies on the CsoS2 protein in three model organisms and show that CsoS2 is vital for α-carboxysome biogenesis. The primary structure of CsoS2 appears tripartite, composed of an N-terminal, middle (M)-, and C-terminal region. Repetitive motifs can be identified in the N- and M-regions. Multiple lines of evidence suggest CsoS2 is highly flexible, possibly an intrinsically disordered protein. Based on our results from bioinformatic, biophysical, genetic and biochemical approaches, including peptide array scanning for protein-protein interactions, we propose a model for CsoS2 function and its spatial location in the α-carboxysome. Analogies between the pathway for β-carboxysome biogenesis and our model for α-carboxysome assembly are discussed. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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976 KiB

Open AccessArticle

Integrated in silico Analyses of Regulatory and Metabolic Networks of Synechococcus sp. PCC 7002 Reveal Relationships between Gene Centrality and Essentiality

by Hyun-Seob Song, Ryan S. McClure, Hans C. Bernstein, Christopher C. Overall, Eric A. Hill and Alexander S. Beliaev

Life 2015, 5(2), 1127-1140; https://doi.org/10.3390/life5021127 - 27 Mar 2015

Cited by 17 | Viewed by 6410

Abstract

Cyanobacteria dynamically relay environmental inputs to intracellular adaptations through a coordinated adjustment of photosynthetic efficiency and carbon processing rates. The output of such adaptations is reflected through changes in transcriptional patterns and metabolic flux distributions that ultimately define growth strategy. To address interrelationships [...] Read more.

Cyanobacteria dynamically relay environmental inputs to intracellular adaptations through a coordinated adjustment of photosynthetic efficiency and carbon processing rates. The output of such adaptations is reflected through changes in transcriptional patterns and metabolic flux distributions that ultimately define growth strategy. To address interrelationships between metabolism and regulation, we performed integrative analyses of metabolic and gene co-expression networks in a model cyanobacterium, Synechococcus sp. PCC 7002. Centrality analyses using the gene co-expression network identified a set of key genes, which were defined here as “topologically important.” Parallel in silico gene knock-out simulations, using the genome-scale metabolic network, classified what we termed as “functionally important” genes, deletion of which affected growth or metabolism. A strong positive correlation was observed between topologically and functionally important genes. Functionally important genes exhibited variable levels of topological centrality; however, the majority of topologically central genes were found to be functionally essential for growth. Subsequent functional enrichment analysis revealed that both functionally and topologically important genes in Synechococcus sp. PCC 7002 are predominantly associated with translation and energy metabolism, two cellular processes critical for growth. This research demonstrates how synergistic network-level analyses can be used for reconciliation of metabolic and gene expression data to uncover fundamental biological principles. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Open AccessArticle

Enhancing Alkane Production in Cyanobacterial Lipid Droplets: A Model Platform for Industrially Relevant Compound Production

by Anantha Peramuna, Ray Morton and Michael L. Summers

Life 2015, 5(2), 1111-1126; https://doi.org/10.3390/life5021111 - 26 Mar 2015

Cited by 30 | Viewed by 7168

Abstract

Cyanobacterial lipid droplets (LDs) are packed with hydrophobic energy-dense compounds and have great potential for biotechnological expression and the compartmentalization of high value compounds. Nostoc punctiforme normally accumulates LDs containing neutral lipids, and small amounts of heptadecane, during the stationary phase of growth. [...] Read more.

Cyanobacterial lipid droplets (LDs) are packed with hydrophobic energy-dense compounds and have great potential for biotechnological expression and the compartmentalization of high value compounds. Nostoc punctiforme normally accumulates LDs containing neutral lipids, and small amounts of heptadecane, during the stationary phase of growth. In this study, we further enhanced heptadecane production in N. punctiforme by introducing extrachromosomal copies of aar/adc genes, and report the discovery of a putative novel lipase encoded by Npun_F5141, which further enhanced alkane production. Extra copies of all three genes in high light conditions resulted in a 16-fold higher accumulation of heptadecane compared to the wild type strain in the exponential phase. LD accumulation during exponential phase also increased massively to accommodate the heptadecane production. A large number of small, less fluorescent LDs were observed at the cell periphery in exponential growth phase, whereas fewer number of highly fluorescent, much larger LDs were localized towards the center of the cell in the stationary phase. These advances demonstrate that cyanobacterial LDs are an ideal model platform to make industrially relevant compounds, such as alkanes, during exponential growth, and provide insight into LD formation in cyanobacteria. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Open AccessArticle

Highly Iterated Palindromic Sequences (HIPs) and Their Relationship to DNA Methyltransferases

by Jeff Elhai

Life 2015, 5(1), 921-948; https://doi.org/10.3390/life5010921 - 17 Mar 2015

Cited by 15 | Viewed by 7315

Abstract

The sequence GCGATCGC (Highly Iterated Palindrome, HIP1) is commonly found in high frequency in cyanobacterial genomes. An important clue to its function may be the presence of two orphan DNA methyltransferases that recognize internal sequences GATC and CGATCG. An examination of genomes from [...] Read more.

The sequence GCGATCGC (Highly Iterated Palindrome, HIP1) is commonly found in high frequency in cyanobacterial genomes. An important clue to its function may be the presence of two orphan DNA methyltransferases that recognize internal sequences GATC and CGATCG. An examination of genomes from 97 cyanobacteria, both free-living and obligate symbionts, showed that there are exceptional cases in which HIP1 is at a low frequency or nearly absent. In some of these cases, it appears to have been replaced by a different GC-rich palindromic sequence, alternate HIPs. When HIP1 is at a high frequency, GATC- and CGATCG-specific methyltransferases are generally present in the genome. When an alternate HIP is at high frequency, a methyltransferase specific for that sequence is present. The pattern of 1-nt deviations from HIP1 sequences is biased towards the first and last nucleotides, i.e., those distinguish CGATCG from HIP1. Taken together, the results point to a role of DNA methylation in the creation or functioning of HIP sites. A model is presented that postulates the existence of a G^meC-dependent mismatch repair system whose activity creates and maintains HIP sequences. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Open AccessArticle

Nitrogen Starvation Acclimation in Synechococcus elongatus: Redox-Control and the Role of Nitrate Reduction as an Electron Sink

by Alexander Klotz, Edgar Reinhold, Sofía Doello and Karl Forchhammer

Life 2015, 5(1), 888-904; https://doi.org/10.3390/life5010888 - 13 Mar 2015

Cited by 30 | Viewed by 7769

Abstract

Nitrogen starvation acclimation in non-diazotrophic cyanobacteria is characterized by a process termed chlorosis, where the light harvesting pigments are degraded and the cells gradually tune down photosynthetic and metabolic activities. The chlorosis response is governed by a complex and poorly understood regulatory network, [...] Read more.

Nitrogen starvation acclimation in non-diazotrophic cyanobacteria is characterized by a process termed chlorosis, where the light harvesting pigments are degraded and the cells gradually tune down photosynthetic and metabolic activities. The chlorosis response is governed by a complex and poorly understood regulatory network, which converges at the expression of the nblA gene, the triggering factor for phycobiliprotein degradation. This study established a method that allows uncoupling metabolic and redox-signals involved in nitrogen-starvation acclimation. Inhibition of glutamine synthetase (GS) by a precise dosage of l-methionine-sulfoximine (MSX) mimics the metabolic situation of nitrogen starvation. Addition of nitrate to such MSX-inhibited cells eliminates the associated redox-stress by enabling electron flow towards nitrate/nitrite reduction and thereby, prevents the induction of nblA expression and the associated chlorosis response. This study demonstrates that nitrogen starvation is perceived not only through metabolic signals, but requires a redox signal indicating over-reduction of PSI-reduced electron acceptors. It further establishes a cryptic role of nitrate/nitrite reductases as electron sinks to balance conditions of over-reduction. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Open AccessArticle

A Comparative Study of Iron Uptake Rates and Mechanisms amongst Marine and Fresh Water Cyanobacteria: Prevalence of Reductive Iron Uptake

by Hagar Lis, Chana Kranzler, Nir Keren and Yeala Shaked

Life 2015, 5(1), 841-860; https://doi.org/10.3390/life5010841 - 11 Mar 2015

Cited by 55 | Viewed by 7832

Abstract

In this contribution, we address the question of iron bioavailability to cyanobacteria by measuring Fe uptake rates and probing for a reductive uptake pathway in diverse cyanobacterial species. We examined three Fe-substrates: dissolved inorganic iron (Fe') and the Fe-siderophores Ferrioxamine B (FOB) and [...] Read more.

In this contribution, we address the question of iron bioavailability to cyanobacteria by measuring Fe uptake rates and probing for a reductive uptake pathway in diverse cyanobacterial species. We examined three Fe-substrates: dissolved inorganic iron (Fe') and the Fe-siderophores Ferrioxamine B (FOB) and FeAerobactin (FeAB). In order to compare across substrates and strains, we extracted uptake rate constants (k_in = uptake rate/[Fe-substrate]). Fe' was the most bioavailable Fe form to cyanobacteria, with k_in values higher than those of other substrates. When accounting for surface area (SA), all strains acquired Fe' at similar rates, as their k_in/SA were similar. We also observed homogeneity in the uptake of FOB among strains, but with 10,000 times lower k_in/SA values than Fe'. Uniformity in k_in/SA suggests similarity in the mechanism of uptake and indeed, all strains were found to employ a reductive step in the uptake of Fe' and FOB. In contrast, different uptake pathways were found for FeAB along with variations in k_in/SA. Our data supports the existence of a common reductive Fe uptake pathway amongst cyanobacteria, functioning alone or in addition to siderophore-mediated uptake. Cyanobacteria combining both uptake strategies benefit from increased flexibility in accessing different Fe-substrates. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Open AccessArticle

CaCO₃ Precipitation in Multilayered Cyanobacterial Mats: Clues to Explain the Alternation of Micrite and Sparite Layers in Calcareous Stromatolites

by Józef Kaźmierczak, Tom Fenchel, Michael Kühl, Stephan Kempe, Barbara Kremer, Bożena Łącka and Krzysztof Małkowski

Life 2015, 5(1), 744-769; https://doi.org/10.3390/life5010744 - 09 Mar 2015

Cited by 54 | Viewed by 10941

Abstract

Marine cyanobacterial mats were cultured on coastal sediments (Nivå Bay, Øresund, Denmark) for over three years in a closed system. Carbonate particles formed in two different modes in the mat: (i) through precipitation of submicrometer-sized grains of Mg calcite within the mucilage near [...] Read more.

Marine cyanobacterial mats were cultured on coastal sediments (Nivå Bay, Øresund, Denmark) for over three years in a closed system. Carbonate particles formed in two different modes in the mat: (i) through precipitation of submicrometer-sized grains of Mg calcite within the mucilage near the base of living cyanobacterial layers, and (ii) through precipitation of a variety of mixed Mg calcite/aragonite morphs in layers of degraded cyanobacteria dominated by purple sulfur bacteria. The d¹³C values were about 2‰ heavier in carbonates from the living cyanobacterial zones as compared to those generated in the purple bacterial zones. Saturation indices calculated with respect to calcite, aragonite, and dolomite inside the mats showed extremely high values across the mat profile. Such high values were caused by high pH and high carbonate alkalinity generated within the mats in conjunction with increased concentrations of calcium and magnesium that were presumably stored in sheaths and extracellular polymer substances (EPS) of the living cyanobacteria and liberated during their post-mortem degradation. The generated CaCO₃ morphs were highly similar to morphs reported from heterotrophic bacterial cultures, and from bacterially decomposed cyanobacterial biomass emplaced in Ca-rich media. They are also similar to CaCO₃ morphs precipitated from purely inorganic solutions. No metabolically (enzymatically) controlled formation of particular CaCO3 morphs by heterotrophic bacteria was observed in the studied mats. The apparent alternation of in vivo and post-mortem generated calcareous layers in the studied cyanobacterial mats may explain the alternation of fine-grained (micritic) and coarse-grained (sparitic) laminae observed in modern and fossil calcareous cyanobacterial microbialites as the result of a probably similar multilayered mat organization. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Open AccessArticle

Mechanisms of High Temperature Resistance of Synechocystis sp. PCC 6803: An Impact of Histidine Kinase 34

by Jan Červený, Maria A. Sinetova, Tomáš Zavřel and Dmitry A. Los

Life 2015, 5(1), 676-699; https://doi.org/10.3390/life5010676 - 02 Mar 2015

Cited by 31 | Viewed by 9569

Abstract

Synechocystis sp. PCC 6803 is a widely used model cyanobacterium for studying responses and acclimation to different abiotic stresses. Changes in transcriptome, proteome, lipidome, and photosynthesis in response to short term heat stress are well studied in this organism, and histidine kinase 34 [...] Read more.

Synechocystis sp. PCC 6803 is a widely used model cyanobacterium for studying responses and acclimation to different abiotic stresses. Changes in transcriptome, proteome, lipidome, and photosynthesis in response to short term heat stress are well studied in this organism, and histidine kinase 34 (Hik34) is shown to play an important role in mediating such response. Corresponding data on long term responses, however, are fragmentary and vary depending on parameters of experiments and methods of data collection, and thus are hard to compare. In order to elucidate how the early stress responses help cells to sustain long-term heat stress, as well as the role of Hik34 in prolonged acclimation, we examined the resistance to long-term heat stress of wild-type and ΔHik34 mutant of Synechocystis. In this work, we were able to precisely control the long term experimental conditions by cultivating Synechocystis in automated photobioreactors, measuring selected physiological parameters within a time range of minutes. In addition, morphological and ultrastructural changes in cells were analyzed and western blotting of individual proteins was used to study the heat stress-affected protein expression. We have shown that the majority of wild type cell population was able to recover after 24 h of cultivation at 44 °C. In contrast, while ΔHik34 mutant cells were resistant to heat stress within its first hours, they could not recover after 24 h long high temperature treatment. We demonstrated that the early induction of HspA expression and maintenance of high amount of other HSPs throughout the heat incubation is critical for successful adaptation to long-term stress. In addition, it appears that histidine kinase Hik34 is an essential component for the long term high temperature resistance. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Open AccessArticle

Regulation of Genes Involved in Heterocyst Differentiation in the Cyanobacterium Anabaena sp. Strain PCC 7120 by a Group 2 Sigma Factor SigC

by Shigeki Ehira and Shogo Miyazaki

Life 2015, 5(1), 587-603; https://doi.org/10.3390/life5010587 - 16 Feb 2015

Cited by 17 | Viewed by 6599

Abstract

The filamentous cyanobacterium Anabaena sp. strain PCC 7120 differentiates specialized cells for nitrogen fixation called heterocysts upon limitation of combined nitrogen in the medium. During heterocyst differentiation, expression of approximately 500 genes is upregulated with spatiotemporal regulation. In the present study, we investigated [...] Read more.

The filamentous cyanobacterium Anabaena sp. strain PCC 7120 differentiates specialized cells for nitrogen fixation called heterocysts upon limitation of combined nitrogen in the medium. During heterocyst differentiation, expression of approximately 500 genes is upregulated with spatiotemporal regulation. In the present study, we investigated the functions of sigma factors of RNA polymerase in the regulation of heterocyst differentiation. The transcript levels of sigC, sigE, and sigG were increased during heterocyst differentiation, while expression of sigJ was downregulated. We carried out DNA microarray analysis to identify genes regulated by SigC, SigE, and SigG. It was indicated that SigC regulated the expression of genes involved in heterocyst differentiation and functions. Moreover, genes regulated by SigC partially overlapped with those regulated by SigE, and deficiency of SigC was likely to be compensated by SigE. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Open AccessCommunication

Modes of Fatty Acid Desaturation in Cyanobacteria: An Update

by Dmitry A. Los and Kirill S. Mironov

Life 2015, 5(1), 554-567; https://doi.org/10.3390/life5010554 - 16 Feb 2015

Cited by 63 | Viewed by 8124

Abstract

Fatty acid composition of individual species of cyanobacteria is conserved and it may be used as a phylogenetic marker. The previously proposed classification system was based solely on biochemical data. Today, new genomic data are available, which support a need to update a [...] Read more.

Fatty acid composition of individual species of cyanobacteria is conserved and it may be used as a phylogenetic marker. The previously proposed classification system was based solely on biochemical data. Today, new genomic data are available, which support a need to update a previously postulated FA-based classification of cyanobacteria. These changes are necessary in order to adjust and synchronize biochemical, physiological and genomic data, which may help to establish an adequate comprehensive taxonomic system for cyanobacteria in the future. Here, we propose an update to the classification system of cyanobacteria based on their fatty acid composition. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Open AccessArticle

Functional Characterization of the FNT Family Nitrite Transporter of Marine Picocyanobacteria

by Shin-ichi Maeda, Akio Murakami, Hisashi Ito, Ayumi Tanaka and Tatsuo Omata

Life 2015, 5(1), 432-446; https://doi.org/10.3390/life5010432 - 09 Feb 2015

Cited by 21 | Viewed by 6344

Abstract

Many of the cyanobacterial species found in marine and saline environments have a gene encoding a putative nitrite transporter of the formate/nitrite transporter (FNT) family. The presumed function of the gene (designated nitM) was confirmed by functional expression of the gene from [...] Read more.

Many of the cyanobacterial species found in marine and saline environments have a gene encoding a putative nitrite transporter of the formate/nitrite transporter (FNT) family. The presumed function of the gene (designated nitM) was confirmed by functional expression of the gene from the coastal marine species Synechococcus sp. strain PCC7002 in the nitrite-transport-less mutant (NA4) of the freshwater cyanobacterium Synechococcus elongatus strain PCC7942. The NitM-mediated nitrite uptake showed an apparent K_m (NO₂⁻) of about 8 μM and was not inhibited by nitrate, cyanate or formate. Of the nitM orthologs from the three oceanic cyanobacterial species, which are classified as α-cyanobacteria on the basis of the occurrence of Type 1a RuBisCO, the one from Synechococcus sp. strain CC9605 conferred nitrite uptake activity on NA4, but those from Synechococcus sp. strain CC9311 and Prochlorococcus marinus strain MIT9313 did not. A strongly conserved hydrophilic amino acid sequence was found at the C-termini of the deduced NitM sequences from α-cyanobacteria, with a notable exception of the Synechococcus sp. strain CC9605 NitM protein, which entirely lacked the C-terminal amino acids. The C-terminal sequence was not conserved in the NitM proteins from β-cyanobacteria carrying the Type 1b RuBisCO, including the one from Synechococcus sp. strain PCC7002. Expression of the truncated nitM genes from Synechococcus sp. strain CC9311 and Prochlorococcus marinus strain MIT9313, encoding the proteins lacking the conserved C-terminal region, conferred nitrite uptake activity on the NA4 mutant, indicating that the C-terminal region of α-cyanobacterial NitM proteins inhibits the activity of the transporter. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Open AccessArticle

The RUBISCO to Photosystem II Ratio Limits the Maximum Photosynthetic Rate in Picocyanobacteria

by Jackie K. Zorz, Jessica R. Allanach, Cole D. Murphy, Mitchell S. Roodvoets, Douglas A. Campbell and Amanda M. Cockshutt

Life 2015, 5(1), 403-417; https://doi.org/10.3390/life5010403 - 04 Feb 2015

Cited by 33 | Viewed by 6769

Abstract

Marine Synechococcus and Prochlorococcus are picocyanobacteria predominating in subtropical, oligotrophic marine environments, a niche predicted to expand with climate change. When grown under common low light conditions Synechococcus WH 8102 and Prochlorococcus MED 4 show similar Cytochrome b₆f and Photosystem I [...] Read more.

Marine Synechococcus and Prochlorococcus are picocyanobacteria predominating in subtropical, oligotrophic marine environments, a niche predicted to expand with climate change. When grown under common low light conditions Synechococcus WH 8102 and Prochlorococcus MED 4 show similar Cytochrome b₆f and Photosystem I contents normalized to Photosystem II content, while Prochlorococcus MIT 9313 has twice the Cytochrome b₆f content and four times the Photosystem I content of the other strains. Interestingly, the Prochlorococcus strains contain only one third to one half of the RUBISCO catalytic subunits compared to the marine Synechococcus strain. The maximum Photosystem II electron transport rates were similar for the two Prochlorococcus strains but higher for the marine Synechococcus strain. Photosystem II electron transport capacity is highly correlated to the molar ratio of RUBISCO active sites to Photosystem II but not to the ratio of cytochrome b₆f to Photosystem II, nor to the ratio of Photosystem I: Photosystem II. Thus, the catalytic capacity for the rate-limiting step of carbon fixation, the ultimate electron sink, appears to limit electron transport rates. The high abundance of Cytochrome b₆f and Photosystem I in MIT 9313, combined with the slower flow of electrons away from Photosystem II and the relatively low level of RUBISCO, are consistent with cyclic electron flow around Photosystem I in this strain. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Open AccessArticle

The Anabaena sp. PCC 7120 Exoproteome: Taking a Peek outside the Box

by Paulo Oliveira, Nuno M. Martins, Marina Santos, Narciso A. S. Couto, Phillip C. Wright and Paula Tamagnini

Life 2015, 5(1), 130-163; https://doi.org/10.3390/life5010130 - 08 Jan 2015

Cited by 36 | Viewed by 8890

Abstract

The interest in examining the subset of proteins present in the extracellular milieu, the exoproteome, has been growing due to novel insights highlighting their role on extracellular matrix organization and biofilm formation, but also on homeostasis and development. The cyanobacterial exoproteome is poorly [...] Read more.

The interest in examining the subset of proteins present in the extracellular milieu, the exoproteome, has been growing due to novel insights highlighting their role on extracellular matrix organization and biofilm formation, but also on homeostasis and development. The cyanobacterial exoproteome is poorly studied, and the role of cyanobacterial exoproteins on cell wall biogenesis, morphology and even physiology is largely unknown. Here, we present a comprehensive examination of the Anabaena sp. PCC 7120 exoproteome under various growth conditions. Altogether, 139 proteins belonging to 16 different functional categories have been identified. A large fraction (48%) of the identified proteins is classified as “hypothetical”, falls into the “other categories” set or presents no similarity to other proteins. The evidence presented here shows that Anabaena sp. PCC 7120 is capable of outer membrane vesicle formation and that these vesicles are likely to contribute to the exoproteome profile. Furthermore, the activity of selected exoproteins associated with oxidative stress has been assessed, suggesting their involvement in redox homeostasis mechanisms in the extracellular space. Finally, we discuss our results in light of other cyanobacterial exoproteome studies and focus on the potential of exploring cyanobacteria as cell factories to produce and secrete selected proteins. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Open AccessArticle

Does a Barcoding Gap Exist in Prokaryotes? Evidences from Species Delimitation in Cyanobacteria

by Ester M. Eckert, Diego Fontaneto, Manuela Coci and Cristiana Callieri

Life 2015, 5(1), 50-64; https://doi.org/10.3390/life5010050 - 31 Dec 2014

Cited by 16 | Viewed by 10450

Abstract

The amount of information that is available on 16S rRNA sequences for prokaryotes thanks to high-throughput sequencing could allow a better understanding of diversity. Nevertheless, the application of predetermined threshold in genetic distances to identify units of diversity (Operative Taxonomic Units, OTUs) may [...] Read more.

The amount of information that is available on 16S rRNA sequences for prokaryotes thanks to high-throughput sequencing could allow a better understanding of diversity. Nevertheless, the application of predetermined threshold in genetic distances to identify units of diversity (Operative Taxonomic Units, OTUs) may provide biased results. Here we tests for the existence of a barcoding gap in several groups of Cyanobacteria, defining units of diversity according to clear differences between within-species and among-species genetic distances in 16S rRNA. The application of a tool developed for animal DNA taxonomy, the Automatic Barcode Gap Detector (ABGD), revealed that a barcoding gap could actually be found in almost half of the datasets that we tested. The identification of units of diversity through this method provided results that were not compatible with those obtained with the identification of OTUs with threshold of similarity in genetic distances of 97% or 99%. The main message of our results is a call for caution in the estimate of diversity from 16S sequences only, given that different subjective choices in the method to delimit units could provide different results. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Open AccessArticle

Occurrence of Far-Red Light Photoacclimation (FaRLiP) in Diverse Cyanobacteria

by Fei Gan, Gaozhong Shen and Donald A. Bryant

Life 2015, 5(1), 4-24; https://doi.org/10.3390/life5010004 - 29 Dec 2014

Cited by 139 | Viewed by 14187

Abstract

Cyanobacteria have evolved a number of acclimation strategies to sense and respond to changing nutrient and light conditions. Leptolyngbya sp. JSC-1 was recently shown to photoacclimate to far-red light by extensively remodeling its photosystem (PS) I, PS II and phycobilisome complexes, thereby gaining [...] Read more.

Cyanobacteria have evolved a number of acclimation strategies to sense and respond to changing nutrient and light conditions. Leptolyngbya sp. JSC-1 was recently shown to photoacclimate to far-red light by extensively remodeling its photosystem (PS) I, PS II and phycobilisome complexes, thereby gaining the ability to grow in far-red light. A 21-gene photosynthetic gene cluster (rfpA/B/C, apcA2/B2/D2/E2/D3, psbA3/D3/C2/B2/ H2/A4, psaA2/B2/L2/I2/F2/J2) that is specifically expressed in far-red light encodes the core subunits of the three major photosynthetic complexes. The growth responses to far-red light were studied here for five additional cyanobacterial strains, each of which has a gene cluster similar to that in Leptolyngbya sp. JSC-1. After acclimation all five strains could grow continuously in far-red light. Under these growth conditions each strain synthesizes chlorophylls d, f and a after photoacclimation, and each strain produces modified forms of PS I, PS II (and phycobiliproteins) that absorb light between 700 and 800 nm. We conclude that these photosynthetic gene clusters are diagnostic of the capacity to photoacclimate to and grow in far-red light. Given the diversity of terrestrial environments from which these cyanobacteria were isolated, it is likely that FaRLiP plays an important role in optimizing photosynthesis in terrestrial environments. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Open AccessArticle

Distribution and Ecology of Cyanobacteria in the Rocky Littoral of an English Lake District Water Body, Devoke Water

by Allan Pentecost

Life 2014, 4(4), 1026-1037; https://doi.org/10.3390/life4041026 - 16 Dec 2014

Cited by 3 | Viewed by 5760

Abstract

Cyanobacteria were sampled along two vertical and two horizontal transects in the littoral of Devoke Water, English Lake District. Profiles of cyanobacterium diversity and abundance showed that both attained a maximum close to the water line, but declined rapidly 20–40 cm above it. [...] Read more.

Cyanobacteria were sampled along two vertical and two horizontal transects in the littoral of Devoke Water, English Lake District. Profiles of cyanobacterium diversity and abundance showed that both attained a maximum close to the water line, but declined rapidly 20–40 cm above it. The distribution of individual species with height together with species and site ordinations showed that several taxa occurred in well-defined zones. A narrow “black zone” in the supralittoral was colonised mainly by species of Calothrix, Dichothrix and Gloeocapsa with pigmented sheaths. There was no evidence of lateral variation of species around the lake, but the height of the black zone correlated positively with wind exposure. The flora of Devoke Water is that of a base-poor mountain lake with some elements of a lowland, more alkaline water-body. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Ecology and Physiology of the Pathogenic Cyanobacterium Roseofilum reptotaenium

by Laurie L. Richardson, Dina Stanić, Amanda May, Abigael Brownell, Miroslav Gantar and Shawn R. Campagna

Life 2014, 4(4), 968-987; https://doi.org/10.3390/life4040968 - 15 Dec 2014

Cited by 17 | Viewed by 10642

Abstract

Roseofilum reptotaenium is a gliding, filamentous, phycoerythrin-rich cyanobacterium that has been found only in the horizontally migrating, pathogenic microbial mat, black band disease (BBD) on Caribbean corals. R. reptotaenium dominates the BBD mat in terms of biomass and motility, and the filaments form [...] Read more.

Roseofilum reptotaenium is a gliding, filamentous, phycoerythrin-rich cyanobacterium that has been found only in the horizontally migrating, pathogenic microbial mat, black band disease (BBD) on Caribbean corals. R. reptotaenium dominates the BBD mat in terms of biomass and motility, and the filaments form the mat fabric. This cyanobacterium produces the cyanotoxin microcystin, predominately MC-LR, and can tolerate high levels of sulfide produced by sulfate reducing bacteria (SRB) that are also associated with BBD. Laboratory cultures of R. reptotaenium infect coral fragments, suggesting that the cyanobacterium is the primary pathogen of BBD, but since this species cannot grow axenically and Koch’s Postulates cannot be fulfilled, it cannot be proposed as a primary pathogen. However, R. reptotaenium does play several major pathogenic roles in this polymicrobial disease. Here, we provide an overview of the ecology of this coral pathogen and present new information on R. reptotaenium ecophysiology, including roles in the infection process, chemotactic and other motility responses, and the effect of pH on growth and motility. Additionally, we show, using metabolomics, that exposure of the BBD microbial community to the cyanotoxin MC-LR affects community metabolite profiles, in particular those associated with nucleic acid biosynthesis. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Consequences of Decreased Light Harvesting Capability on Photosystem II Function in Synechocystis sp. PCC 6803

by Aparna Nagarajan, Lawrence E. Page, Michelle Liberton and Himadri B. Pakrasi

Life 2014, 4(4), 903-914; https://doi.org/10.3390/life4040903 - 11 Dec 2014

Cited by 12 | Viewed by 7516

Abstract

Cyanobacteria use large pigment-protein complexes called phycobilisomes to harvest light energy primarily for photosystem II (PSII). We used a series of mutants with partial to complete reduction of phycobilisomes to examine the effects of antenna truncation on photosystem function in Synechocystis sp. PCC [...] Read more.

Cyanobacteria use large pigment-protein complexes called phycobilisomes to harvest light energy primarily for photosystem II (PSII). We used a series of mutants with partial to complete reduction of phycobilisomes to examine the effects of antenna truncation on photosystem function in Synechocystis sp. PCC 6803. The antenna mutants CB, CK, and PAL expressed increasing levels of functional PSII centers to compensate for the loss of phycobilisomes, with a concomitant decrease in photosystem I (PSI). This increased PSII titer led to progressively higher oxygen evolution rates on a per chlorophyll basis. The mutants also exhibited impaired S-state transition profiles for oxygen evolution. Additionally, P700⁺ re-reduction rates were impacted by antenna reduction. Thus, a decrease in antenna size resulted in overall physiological changes in light harvesting and delivery to PSII as well as changes in downstream electron transfer to PSI. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Cellular Dynamics Drives the Emergence of Supracellular Structure in the Cyanobacterium, Phormidium sp. KS

by Naoki Sato, Yutaro Katsumata, Kaoru Sato and Naoyuki Tajima

Life 2014, 4(4), 819-836; https://doi.org/10.3390/life4040819 - 28 Nov 2014

Cited by 12 | Viewed by 9246

Abstract

Motile filamentous cyanobacteria, such as Oscillatoria, Phormidium and Arthrospira, are ubiquitous in terrestrial and aquatic environments. As noted by Nägeli in 1860, many of them form complex three-dimensional or two-dimensional structures, such as biofilm, weed-like thalli, bundles of filaments and [...] Read more.

Motile filamentous cyanobacteria, such as Oscillatoria, Phormidium and Arthrospira, are ubiquitous in terrestrial and aquatic environments. As noted by Nägeli in 1860, many of them form complex three-dimensional or two-dimensional structures, such as biofilm, weed-like thalli, bundles of filaments and spirals, which we call supracellular structures. In all of these structures, individual filaments incessantly move back and forth. The structures are, therefore, macroscopic, dynamic structures that are continuously changing their microscopic arrangement of filaments. In the present study, we analyzed quantitatively the movement of individual filaments of Phormidium sp. KS grown on agar plates. Junctional pores, which have been proposed to drive cell movement by mucilage/slime secretion, were found to align on both sides of each septum. The velocity of movement was highest just after the reversal of direction and, then, attenuated exponentially to a final value before the next reversal of direction. This kinetics is compatible with the “slime gun” model. A higher agar concentration restricts the movement more severely and, thus, resulted in more spiral formation. The spiral is a robust form compatible with non-homogeneous movements of different parts of a long filament. We propose a model of spiral formation based on the microscopic movement of filaments. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Open AccessArticle

The Effects of Dark Incubation on Cellular Metabolism of the Wild Type Cyanobacterium Synechocystis sp. PCC 6803 and a Mutant Lacking the Transcriptional Regulator cyAbrB2

by Masamitsu Hanai, Yusuke Sato, Atsuko Miyagi, Maki Kawai-Yamada, Kyoko Tanaka, Yasuko Kaneko, Yoshitaka Nishiyama and Yukako Hihara

Life 2014, 4(4), 770-787; https://doi.org/10.3390/life4040770 - 21 Nov 2014

Cited by 18 | Viewed by 7156

Abstract

The cyAbrB2 transcriptional regulator is essential for active sugar catabolism in Synechocystis sp. PCC 6803 grown under light conditions. In the light-grown cyabrB2-disrupted mutant, glycogen granules and sugar phosphates corresponding to early steps in the glycolytic pathway accumulated to higher levels than [...] Read more.

The cyAbrB2 transcriptional regulator is essential for active sugar catabolism in Synechocystis sp. PCC 6803 grown under light conditions. In the light-grown cyabrB2-disrupted mutant, glycogen granules and sugar phosphates corresponding to early steps in the glycolytic pathway accumulated to higher levels than those in the wild-type (WT) strain, whereas the amounts of 3-phosphoglycerate, phosphoenolpyruvate and ribulose 1,5-bisphosphate were significantly lower. We further determined that accumulated glycogen granules in the mutant could be actively catabolized under dark conditions. Differences in metabolite levels between WT and the mutant became less substantial during dark incubation due to a general quantitative decrease in metabolite levels. Notable exceptions, however, were increases in 2-oxoglutarate, histidine, ornithine and citrulline in the WT but not in the mutant. The amounts of cyAbrBs were highly responsive to the availability of light both in transcript and protein levels. When grown under light-dark cycle conditions, diurnal oscillatory pattern of glycogen content of the mutant was lost after the second dark period. These observations indicate that cyAbrB2 is dispensable for activation of sugar catabolism under dark conditions but involved in the proper switching between day and night metabolisms. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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A Model of Filamentous Cyanobacteria Leading to Reticulate Pattern Formation

by Carlos Tamulonis and Jaap Kaandorp

Life 2014, 4(3), 433-456; https://doi.org/10.3390/life4030433 - 03 Sep 2014

Cited by 15 | Viewed by 7437

Abstract

The filamentous cyanobacterium, Pseudanabaena, has been shown to produce reticulate patterns that are thought to be the result of its gliding motility. Similar fossilized structures found in the geological record constitute some of the earliest signs of life on Earth. It is difficult [...] Read more.

The filamentous cyanobacterium, Pseudanabaena, has been shown to produce reticulate patterns that are thought to be the result of its gliding motility. Similar fossilized structures found in the geological record constitute some of the earliest signs of life on Earth. It is difficult to tie these fossils, which are billions of years old, directly to the specific microorganisms that built them. Identifying the physicochemical conditions and microorganism properties that lead microbial mats to form macroscopic structures can lead to a better understanding of the conditions on Earth at the dawn of life. In this article, a cell-based model is used to simulate the formation of reticulate patterns in cultures of Pseudanabaena. A minimal system of long and flexible trichomes capable of gliding motility is shown to be sufficient to produce stable patterns consisting of a network of streams. Varying model parameters indicate that systems with little to no cohesion, high trichome density and persistent movement are conducive to reticulate pattern formation, in conformance with experimental observations. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Review

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Role of Cyanobacterial Exopolysaccharides in Phototrophic Biofilms and in Complex Microbial Mats

by Federico Rossi and Roberto De Philippis

Life 2015, 5(2), 1218-1238; https://doi.org/10.3390/life5021218 - 01 Apr 2015

Cited by 280 | Viewed by 16430

Abstract

Exopolysaccharides (EPSs) are an important class of biopolymers with great ecological importance. In natural environments, they are a common feature of microbial biofilms, where they play key protective and structural roles. As the primary colonizers of constrained environments, such as desert soils and [...] Read more.

Exopolysaccharides (EPSs) are an important class of biopolymers with great ecological importance. In natural environments, they are a common feature of microbial biofilms, where they play key protective and structural roles. As the primary colonizers of constrained environments, such as desert soils and lithic and exposed substrates, cyanobacteria are the first contributors to the synthesis of the EPSs constituting the extracellular polymeric matrix that favors the formation of microbial associations with varying levels of complexity called biofilms. Cyanobacterial colonization represents the first step for the formation of biofilms with different levels of complexity. In all of the possible systems in which cyanobacteria are involved, the synthesis of EPSs contributes a structurally-stable and hydrated microenvironment, as well as chemical/physical protection against biotic and abiotic stress factors. Notwithstanding the important roles of cyanobacterial EPSs, many aspects related to their roles and the relative elicited biotic and abiotic factors have still to be clarified. The aim of this survey is to outline the state-of-the-art of the importance of the cyanobacterial EPS excretion, both for the producing cells and for the microbial associations in which cyanobacteria are a key component. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Open AccessReview

Evolutionary Aspects and Regulation of Tetrapyrrole Biosynthesis in Cyanobacteria under Aerobic and Anaerobic Environments

by Yuichi Fujita, Ryoma Tsujimoto and Rina Aoki

Life 2015, 5(2), 1172-1203; https://doi.org/10.3390/life5021172 - 30 Mar 2015

Cited by 27 | Viewed by 8867

Abstract

Chlorophyll a (Chl) is a light-absorbing tetrapyrrole pigment that is essential for photosynthesis. The molecule is produced from glutamate via a complex biosynthetic pathway comprised of at least 15 enzymatic steps. The first half of the Chl pathway is shared with heme biosynthesis, [...] Read more.

Chlorophyll a (Chl) is a light-absorbing tetrapyrrole pigment that is essential for photosynthesis. The molecule is produced from glutamate via a complex biosynthetic pathway comprised of at least 15 enzymatic steps. The first half of the Chl pathway is shared with heme biosynthesis, and the latter half, called the Mg-branch, is specific to Mg-containing Chl a. Bilin pigments, such as phycocyanobilin, are additionally produced from heme, so these light-harvesting pigments also share many common biosynthetic steps with Chl biosynthesis. Some of these common steps in the biosynthetic pathways of heme, Chl and bilins require molecular oxygen for catalysis, such as oxygen-dependent coproporphyrinogen III oxidase. Cyanobacteria thrive in diverse environments in terms of oxygen levels. To cope with Chl deficiency caused by low-oxygen conditions, cyanobacteria have developed elaborate mechanisms to maintain Chl production, even under microoxic environments. The use of enzymes specialized for low-oxygen conditions, such as oxygen-independent coproporphyrinogen III oxidase, constitutes part of a mechanism adapted to low-oxygen conditions. Another mechanism adaptive to hypoxic conditions is mediated by the transcriptional regulator ChlR that senses low oxygen and subsequently activates the transcription of genes encoding enzymes that work under low-oxygen tension. In diazotrophic cyanobacteria, this multilayered regulation also contributes in Chl biosynthesis by supporting energy production for nitrogen fixation that also requires low-oxygen conditions. We will also discuss the evolutionary implications of cyanobacterial tetrapyrrole biosynthesis and regulation, because low oxygen-type enzymes also appear to be evolutionarily older than oxygen-dependent enzymes. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Open AccessReview

How Close We Are to Achieving Commercially Viable Large-Scale Photobiological Hydrogen Production by Cyanobacteria: A Review of the Biological Aspects

by Hidehiro Sakurai, Hajime Masukawa, Masaharu Kitashima and Kazuhito Inoue

Life 2015, 5(1), 997-1018; https://doi.org/10.3390/life5010997 - 18 Mar 2015

Cited by 26 | Viewed by 9578 | Correction

Abstract

Photobiological production of H₂ by cyanobacteria is considered to be an ideal source of renewable energy because the inputs, water and sunlight, are abundant. The products of photobiological systems are H₂ and O₂; the H₂ can be used [...] Read more.

Photobiological production of H₂ by cyanobacteria is considered to be an ideal source of renewable energy because the inputs, water and sunlight, are abundant. The products of photobiological systems are H₂ and O₂; the H₂ can be used as the energy source of fuel cells, etc., which generate electricity at high efficiencies and minimal pollution, as the waste product is H₂O. Overall, production of commercially viable algal fuels in any form, including biomass and biodiesel, is challenging, and the very few systems that are operational have yet to be evaluated. In this paper we will: briefly review some of the necessary conditions for economical production, summarize the reports of photobiological H₂ production by cyanobacteria, present our schemes for future production, and discuss the necessity for further progress in the research needed to achieve commercially viable large-scale H₂ production. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Open AccessReview

Cyanobacterial Oxygenic Photosynthesis is Protected by Flavodiiron Proteins

by Yagut Allahverdiyeva, Janne Isojärvi, Pengpeng Zhang and Eva-Mari Aro

Life 2015, 5(1), 716-743; https://doi.org/10.3390/life5010716 - 09 Mar 2015

Cited by 118 | Viewed by 11076

Abstract

Flavodiiron proteins (FDPs, also called flavoproteins, Flvs) are modular enzymes widely present in Bacteria and Archaea. The evolution of cyanobacteria and oxygenic photosynthesis occurred in concert with the modulation of typical bacterial FDPs. Present cyanobacterial FDPs are composed of three domains, the β-lactamase-like, [...] Read more.

Flavodiiron proteins (FDPs, also called flavoproteins, Flvs) are modular enzymes widely present in Bacteria and Archaea. The evolution of cyanobacteria and oxygenic photosynthesis occurred in concert with the modulation of typical bacterial FDPs. Present cyanobacterial FDPs are composed of three domains, the β-lactamase-like, flavodoxin-like and flavin-reductase like domains. Cyanobacterial FDPs function as hetero- and homodimers and are involved in the regulation of photosynthetic electron transport. Whilst Flv2 and Flv4 proteins are limited to specific cyanobacterial species (β-cyanobacteria) and function in photoprotection of Photosystem II, Flv1 and Flv3 proteins, functioning in the “Mehler-like” reaction and safeguarding Photosystem I under fluctuating light conditions, occur in nearly all cyanobacteria and additionally in green algae, mosses and lycophytes. Filamentous cyanobacteria have additional FDPs in heterocyst cells, ensuring a microaerobic environment for the function of the nitrogenase enzyme under the light. Here, the evolution, occurrence and functional mechanisms of various FDPs in oxygenic photosynthetic organisms are discussed. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Open AccessReview

Appendages of the Cyanobacterial Cell

by Nils Schuergers and Annegret Wilde

Life 2015, 5(1), 700-715; https://doi.org/10.3390/life5010700 - 04 Mar 2015

Cited by 43 | Viewed by 8406

Abstract

Extracellular non-flagellar appendages, called pili or fimbriae, are widespread in gram-negative bacteria. They are involved in many different functions, including motility, adhesion, biofilm formation, and uptake of DNA. Sequencing data for a large number of cyanobacterial genomes revealed that most of them contain [...] Read more.

Extracellular non-flagellar appendages, called pili or fimbriae, are widespread in gram-negative bacteria. They are involved in many different functions, including motility, adhesion, biofilm formation, and uptake of DNA. Sequencing data for a large number of cyanobacterial genomes revealed that most of them contain genes for pili synthesis. However, only for a very few cyanobacteria structure and function of these appendages have been analyzed. Here, we review the structure and function of type IV pili in Synechocystis sp. PCC 6803 and analyze the distribution of type IV pili associated genes in other cyanobacteria. Further, we discuss the role of the RNA-chaperone Hfq in pilus function and the presence of genes for the chaperone-usher pathway of pilus assembly in cyanobacteria. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Long-Term Changes in Cyanobacteria Populations in Lake Kinneret (Sea of Galilee), Israel: An Eco-Physiological Outlook

by Ora Hadas, Aaron Kaplan and Assaf Sukenik

Life 2015, 5(1), 418-431; https://doi.org/10.3390/life5010418 - 05 Feb 2015

Cited by 23 | Viewed by 6330

Abstract

The long-term record of cyanobacteria abundance in Lake Kinneret (Sea of Galilee), Israel, demonstrates changes in cyanobacteria abundance and composition in the last five decades. New invasive species of the order Nostocales (Aphanizomenon ovalisporum and Cylindrospermopsis raciborskii) became part of the [...] Read more.

The long-term record of cyanobacteria abundance in Lake Kinneret (Sea of Galilee), Israel, demonstrates changes in cyanobacteria abundance and composition in the last five decades. New invasive species of the order Nostocales (Aphanizomenon ovalisporum and Cylindrospermopsis raciborskii) became part of the annual phytoplankton assemblage during summer-autumn. Concomitantly, bloom events of Microcystis sp. (Chroococcales) during winter-spring intensified. These changes in cyanobacteria pattern may be partly attributed to the management policy in Lake Kinneret’s vicinity and watershed aimed to reduce effluent discharge to the lake and partly to climate changes in the region; i.e., increased water column temperature, less wind and reduced precipitation. The gradual decrease in the concentration of total and dissolved phosphorus and total and dissolved nitrogen and an increase in alkalinity, pH and salinity, combined with the physiological features of cyanobacteria, probably contributed to the success of cyanobacteria. The data presented here indicate that the trend of the continuous decline of nutrients may not be sufficient to reduce and to control the abundance and proliferation of toxic and non-toxic cyanobacteria. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Regulation of CO₂ Concentrating Mechanism in Cyanobacteria

by Robert L. Burnap, Martin Hagemann and Aaron Kaplan

Life 2015, 5(1), 348-371; https://doi.org/10.3390/life5010348 - 28 Jan 2015

Cited by 141 | Viewed by 12423

Abstract

In this chapter, we mainly focus on the acclimation of cyanobacteria to the changing ambient CO₂ and discuss mechanisms of inorganic carbon (C_i) uptake, photorespiration, and the regulation among the metabolic fluxes involved in photoautotrophic, photomixotrophic and heterotrophic growth. The [...] Read more.

In this chapter, we mainly focus on the acclimation of cyanobacteria to the changing ambient CO₂ and discuss mechanisms of inorganic carbon (C_i) uptake, photorespiration, and the regulation among the metabolic fluxes involved in photoautotrophic, photomixotrophic and heterotrophic growth. The structural components for several of the transport and uptake mechanisms are described and the progress towards elucidating their regulation is discussed in the context of studies, which have documented metabolomic changes in response to changes in C_i availability. Genes for several of the transport and uptake mechanisms are regulated by transcriptional regulators that are in the LysR-transcriptional regulator family and are known to act in concert with small molecule effectors, which appear to be well-known metabolites. Signals that trigger changes in gene expression and enzyme activity correspond to specific “regulatory metabolites” whose concentrations depend on the ambient C_i availability. Finally, emerging evidence for an additional layer of regulatory complexity involving small non-coding RNAs is discussed. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Portrait of a Geothermal Spring, Hunter’s Hot Springs, Oregon

by Richard W. Castenholz

Life 2015, 5(1), 332-347; https://doi.org/10.3390/life5010332 - 27 Jan 2015

Cited by 16 | Viewed by 6887

Abstract

Although alkaline Hunter’s Hot Springs in southeastern Oregon has been studied extensively for over 40 years, most of these studies and the subsequent publications were before the advent of molecular methods. However, there are many field observations and laboratory experiments that reveal the [...] Read more.

Although alkaline Hunter’s Hot Springs in southeastern Oregon has been studied extensively for over 40 years, most of these studies and the subsequent publications were before the advent of molecular methods. However, there are many field observations and laboratory experiments that reveal the major aspects of the phototrophic species composition within various physical and chemical gradients of these springs. Relatively constant temperature boundaries demark the upper boundary of the unicellular cyanobacterium, Synechococcus at 73–74 °C (the world-wide upper limit for photosynthesis), and 68–70 °C the upper limit for Chloroflexus. The upper limit for the cover of the filamentous cyanobacterium, Geitlerinema (Oscillatoria) is at 54–55 °C, and the in situ lower limit at 47–48 °C for all three of these phototrophs due to the upper temperature limit for the grazing ostracod, Thermopsis. The in situ upper limit for the cyanobacteria Pleurocapsa and Calothrix is at ~47–48 °C, which are more grazer-resistant and grazer dependent. All of these demarcations are easily visible in the field. In addition, there is a biosulfide production in some sections of the springs that have a large impact on the microbiology. Most of the temperature and chemical limits have been explained by field and laboratory experiments. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Terpenoids and Their Biosynthesis in Cyanobacteria

by Bagmi Pattanaik and Pia Lindberg

Life 2015, 5(1), 269-293; https://doi.org/10.3390/life5010269 - 21 Jan 2015

Cited by 111 | Viewed by 22119

Abstract

Terpenoids, or isoprenoids, are a family of compounds with great structural diversity which are essential for all living organisms. In cyanobacteria, they are synthesized from the methylerythritol-phosphate (MEP) pathway, using glyceraldehyde 3-phosphate and pyruvate produced by photosynthesis as substrates. The products of the [...] Read more.

Terpenoids, or isoprenoids, are a family of compounds with great structural diversity which are essential for all living organisms. In cyanobacteria, they are synthesized from the methylerythritol-phosphate (MEP) pathway, using glyceraldehyde 3-phosphate and pyruvate produced by photosynthesis as substrates. The products of the MEP pathway are the isomeric five-carbon compounds isopentenyl diphosphate and dimethylallyl diphosphate, which in turn form the basic building blocks for formation of all terpenoids. Many terpenoid compounds have useful properties and are of interest in the fields of pharmaceuticals and nutrition, and even potentially as future biofuels. The MEP pathway, its function and regulation, and the subsequent formation of terpenoids have not been fully elucidated in cyanobacteria, despite its relevance for biotechnological applications. In this review, we summarize the present knowledge about cyanobacterial terpenoid biosynthesis, both regarding the native metabolism and regarding metabolic engineering of cyanobacteria for heterologous production of non-native terpenoids. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Biosynthesis and Function of Extracellular Glycans in Cyanobacteria

by Jan-Christoph Kehr and Elke Dittmann

Life 2015, 5(1), 164-180; https://doi.org/10.3390/life5010164 - 12 Jan 2015

Cited by 83 | Viewed by 9714

Abstract

The cell surface of cyanobacteria is covered with glycans that confer versatility and adaptability to a multitude of environmental factors. The complex carbohydrates act as barriers against different types of stress and play a role in intra- as well as inter-species interactions. In [...] Read more.

The cell surface of cyanobacteria is covered with glycans that confer versatility and adaptability to a multitude of environmental factors. The complex carbohydrates act as barriers against different types of stress and play a role in intra- as well as inter-species interactions. In this review, we summarize the current knowledge of the chemical composition, biosynthesis and biological function of exo- and lipo-polysaccharides from cyanobacteria and give an overview of sugar-binding lectins characterized from cyanobacteria. We discuss similarities with well-studied enterobacterial systems and highlight the unique features of cyanobacteria. We pay special attention to colony formation and EPS biosynthesis in the bloom-forming cyanobacterium, Microcystis aeruginosa. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Sucrose in Cyanobacteria: From a Salt-Response Molecule to Play a Key Role in Nitrogen Fixation

by María A. Kolman, Carolina N. Nishi, Macarena Perez-Cenci and Graciela L. Salerno

Life 2015, 5(1), 102-126; https://doi.org/10.3390/life5010102 - 06 Jan 2015

Cited by 43 | Viewed by 10908

Abstract

In the biosphere, sucrose is mainly synthesized in oxygenic photosynthetic organisms, such as cyanobacteria, green algae and land plants, as part of the carbon dioxide assimilation pathway. Even though its central position in the functional biology of plants is well documented, much less [...] Read more.

In the biosphere, sucrose is mainly synthesized in oxygenic photosynthetic organisms, such as cyanobacteria, green algae and land plants, as part of the carbon dioxide assimilation pathway. Even though its central position in the functional biology of plants is well documented, much less is known about the role of sucrose in cyanobacteria. In those prokaryotes, sucrose accumulation has been associated with salt acclimation, and considered as a compatible solute in low-salt tolerant strains. In the last years, functional characterizations of sucrose metabolizing enzymes, metabolic control analysis, cellular localization of gene expressions, and reverse genetic experiments have revealed that sucrose metabolism is crucial in the diazotrophic growth of heterocystic strains, and besides, that it can be connected to glycogen synthesis. This article briefly summarizes the current state of knowledge of sucrose physiological functions in modern cyanobacteria and how they might have evolved taking into account the phylogenetic analyses of sucrose enzymes. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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1029 KiB

Open AccessReview

Salt Acclimation of Cyanobacteria and Their Application in Biotechnology

by Nadin Pade and Martin Hagemann

Life 2015, 5(1), 25-49; https://doi.org/10.3390/life5010025 - 29 Dec 2014

Cited by 115 | Viewed by 10067

Abstract

The long evolutionary history and photo-autotrophic lifestyle of cyanobacteria has allowed them to colonize almost all photic habitats on Earth, including environments with high or fluctuating salinity. Their basal salt acclimation strategy includes two principal reactions, the active export of ions and the [...] Read more.

The long evolutionary history and photo-autotrophic lifestyle of cyanobacteria has allowed them to colonize almost all photic habitats on Earth, including environments with high or fluctuating salinity. Their basal salt acclimation strategy includes two principal reactions, the active export of ions and the accumulation of compatible solutes. Cyanobacterial salt acclimation has been characterized in much detail using selected model cyanobacteria, but their salt sensing and regulatory mechanisms are less well understood. Here, we briefly review recent advances in the identification of salt acclimation processes and the essential genes/proteins involved in acclimation to high salt. This knowledge is of increasing importance because the necessary mass cultivation of cyanobacteria for future use in biotechnology will be performed in sea water. In addition, cyanobacterial salt resistance genes also can be applied to improve the salt tolerance of salt sensitive organisms, such as crop plants. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Mitigating Harmful Cyanobacterial Blooms in a Human- and Climatically-Impacted World

by Hans W. Paerl

Life 2014, 4(4), 988-1012; https://doi.org/10.3390/life4040988 - 15 Dec 2014

Cited by 199 | Viewed by 17520

Abstract

Bloom-forming harmful cyanobacteria (CyanoHABs) are harmful from environmental, ecological and human health perspectives by outcompeting beneficial phytoplankton, creating low oxygen conditions (hypoxia, anoxia), and by producing cyanotoxins. Cyanobacterial genera exhibit optimal growth rates and bloom potentials at relatively high water temperatures; hence, global [...] Read more.

Bloom-forming harmful cyanobacteria (CyanoHABs) are harmful from environmental, ecological and human health perspectives by outcompeting beneficial phytoplankton, creating low oxygen conditions (hypoxia, anoxia), and by producing cyanotoxins. Cyanobacterial genera exhibit optimal growth rates and bloom potentials at relatively high water temperatures; hence, global warming plays a key role in their expansion and persistence. CyanoHABs are regulated by synergistic effects of nutrient (nitrogen:N and phosphorus:P) supplies, light, temperature, vertical stratification, water residence times, and biotic interactions. In most instances, nutrient control strategies should focus on reducing both N and P inputs. Strategies based on physical, chemical (nutrient) and biological manipulations can be effective in reducing CyanoHABs; however, these strategies are largely confined to relatively small systems, and some are prone to ecological and environmental drawbacks, including enhancing release of cyanotoxins, disruption of planktonic and benthic communities and fisheries habitat. All strategies should consider and be adaptive to climatic variability and change in order to be effective for long-term control of CyanoHABs. Rising temperatures and greater hydrologic variability will increase growth rates and alter critical nutrient thresholds for CyanoHAB development; thus, nutrient reductions for bloom control may need to be more aggressively pursued in response to climatic changes globally. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Regulation of Three Nitrogenase Gene Clusters in the Cyanobacterium Anabaena variabilis ATCC 29413

by Teresa Thiel and Brenda S. Pratte

Life 2014, 4(4), 944-967; https://doi.org/10.3390/life4040944 - 11 Dec 2014

Cited by 41 | Viewed by 11290

Abstract

The filamentous cyanobacterium Anabaena variabilis ATCC 29413 fixes nitrogen under aerobic conditions in specialized cells called heterocysts that form in response to an environmental deficiency in combined nitrogen. Nitrogen fixation is mediated by the enzyme nitrogenase, which is very sensitive to oxygen. Heterocysts [...] Read more.

The filamentous cyanobacterium Anabaena variabilis ATCC 29413 fixes nitrogen under aerobic conditions in specialized cells called heterocysts that form in response to an environmental deficiency in combined nitrogen. Nitrogen fixation is mediated by the enzyme nitrogenase, which is very sensitive to oxygen. Heterocysts are microxic cells that allow nitrogenase to function in a filament comprised primarily of vegetative cells that produce oxygen by photosynthesis. A. variabilis is unique among well-characterized cyanobacteria in that it has three nitrogenase gene clusters that encode different nitrogenases, which function under different environmental conditions. The nif1 genes encode a Mo-nitrogenase that functions only in heterocysts, even in filaments grown anaerobically. The nif2 genes encode a different Mo-nitrogenase that functions in vegetative cells, but only in filaments grown under anoxic conditions. An alternative V-nitrogenase is encoded by vnf genes that are expressed only in heterocysts in an environment that is deficient in Mo. Thus, these three nitrogenases are expressed differentially in response to environmental conditions. The entire nif1 gene cluster, comprising at least 15 genes, is primarily under the control of the promoter for the first gene, nifB1. Transcriptional control of many of the downstream nif1 genes occurs by a combination of weak promoters within the coding regions of some downstream genes and by RNA processing, which is associated with increased transcript stability. The vnf genes show a similar pattern of transcriptional and post-transcriptional control of expression suggesting that the complex pattern of regulation of the nif1 cluster is conserved in other cyanobacterial nitrogenase gene clusters. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Metals in Cyanobacteria: Analysis of the Copper, Nickel, Cobalt and Arsenic Homeostasis Mechanisms

by María José Huertas, Luis López-Maury, Joaquín Giner-Lamia, Ana María Sánchez-Riego and Francisco Javier Florencio

Life 2014, 4(4), 865-886; https://doi.org/10.3390/life4040865 - 09 Dec 2014

Cited by 122 | Viewed by 12750

Abstract

Traces of metal are required for fundamental biochemical processes, such as photosynthesis and respiration. Cyanobacteria metal homeostasis acquires an important role because the photosynthetic machinery imposes a high demand for metals, making them a limiting factor for cyanobacteria, especially in the open oceans. [...] Read more.

Traces of metal are required for fundamental biochemical processes, such as photosynthesis and respiration. Cyanobacteria metal homeostasis acquires an important role because the photosynthetic machinery imposes a high demand for metals, making them a limiting factor for cyanobacteria, especially in the open oceans. On the other hand, in the last two centuries, the metal concentrations in marine environments and lake sediments have increased as a result of several industrial activities. In all cases, cells have to tightly regulate uptake to maintain their intracellular concentrations below toxic levels. Mechanisms to obtain metal under limiting conditions and to protect cells from an excess of metals are present in cyanobacteria. Understanding metal homeostasis in cyanobacteria and the proteins involved will help to evaluate the use of these microorganisms in metal bioremediation. Furthermore, it will also help to understand how metal availability impacts primary production in the oceans. In this review, we will focus on copper, nickel, cobalt and arsenic (a toxic metalloid) metabolism, which has been mainly analyzed in model cyanobacterium Synechocystis sp. PCC 6803. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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1170 KiB

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Survival Strategies in the Aquatic and Terrestrial World: The Impact of Second Messengers on Cyanobacterial Processes

by Marco Agostoni and Beronda L. Montgomery

Life 2014, 4(4), 745-769; https://doi.org/10.3390/life4040745 - 18 Nov 2014

Cited by 25 | Viewed by 11183

Abstract

Second messengers are intracellular substances regulated by specific external stimuli globally known as first messengers. Cells rely on second messengers to generate rapid responses to environmental changes and the importance of their roles is becoming increasingly realized in cellular signaling research. Cyanobacteria are [...] Read more.

Second messengers are intracellular substances regulated by specific external stimuli globally known as first messengers. Cells rely on second messengers to generate rapid responses to environmental changes and the importance of their roles is becoming increasingly realized in cellular signaling research. Cyanobacteria are photooxygenic bacteria that inhabit most of Earth’s environments. The ability of cyanobacteria to survive in ecologically diverse habitats is due to their capacity to adapt and respond to environmental changes. This article reviews known second messenger-controlled physiological processes in cyanobacteria. Second messengers used in these systems include the element calcium (Ca²⁺), nucleotide-based guanosine tetraphosphate or pentaphosphate (ppGpp or pppGpp, represented as (p)ppGpp), cyclic adenosine 3’,5’-monophosphate (cAMP), cyclic dimeric GMP (c-di-GMP), cyclic guanosine 3’,5’-monophosphate (cGMP), and cyclic dimeric AMP (c-di-AMP), and the gaseous nitric oxide (NO). The discussion focuses on processes central to cyanobacteria, such as nitrogen fixation, light perception, photosynthesis-related processes, and gliding motility. In addition, we address future research trajectories needed to better understand the signaling networks and cross talk in the signaling pathways of these molecules in cyanobacteria. Second messengers have significant potential to be adapted as technological tools and we highlight possible novel and practical applications based on our understanding of these molecules and the signaling networks that they control. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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1860 KiB

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Function and Regulation of Ferredoxins in the Cyanobacterium, Synechocystis PCC6803: Recent Advances

by Corinne Cassier-Chauvat and Franck Chauvat

Life 2014, 4(4), 666-680; https://doi.org/10.3390/life4040666 - 07 Nov 2014

Cited by 82 | Viewed by 9490

Abstract

Ferredoxins (Fed), occurring in most organisms, are small proteins that use their iron-sulfur cluster to distribute electrons to various metabolic pathways, likely including hydrogen production. Here, we summarize the current knowledge on ferredoxins in cyanobacteria, the prokaryotes regarded as important producers of the [...] Read more.

Ferredoxins (Fed), occurring in most organisms, are small proteins that use their iron-sulfur cluster to distribute electrons to various metabolic pathways, likely including hydrogen production. Here, we summarize the current knowledge on ferredoxins in cyanobacteria, the prokaryotes regarded as important producers of the oxygenic atmosphere and biomass for the food chain, as well as promising cell factories for biofuel production. Most studies of ferredoxins were performed in the model strain, Synechocystis PCC6803, which possesses nine highly-conserved ferredoxins encoded by monocistronic or operonic genes, some of which are localized in conserved genome regions. Fed1, encoded by a light-inducible gene, is a highly abundant protein essential to photosynthesis. Fed2-Fed9, encoded by genes differently regulated by trophic conditions, are low-abundant proteins that play prominent roles in the tolerance to environmental stresses. Concerning the selectivity/redundancy of ferredoxin, we report that Fed1, Fed7 and Fed9 belong to ferredoxin-glutaredoxin-thioredoxin crosstalk pathways operating in the protection against oxidative and metal stresses. Furthermore, Fed7 specifically interacts with a DnaJ-like protein, an interaction that has been conserved in photosynthetic eukaryotes in the form of a composite protein comprising DnaJ- and Fed7-like domains. Fed9 specifically interacts with the Flv3 flavodiiron protein acting in the photoreduction of O₂ to H₂O. Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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Open AccessCorrection

Correction: Sakurai, H.; et al. How Close We Are to Achieving Commercially Viable Large-Scale Photobiological Hydrogen Production by Cyanobacteria: A Review of the Biological Aspects. Life 2015, 5, 997–1018

by Hidehiro Sakurai, Hajime Masukawa, Masaharu Kitashima and Kazuhito Inoue

Life 2018, 8(4), 48; https://doi.org/10.3390/life8040048 - 19 Oct 2018

Viewed by 2534

Abstract

In the published article “How close we are to achieving commercially viable large-scale photobiological hydrogen production by cyanobacteria:[...] Full article

(This article belongs to the Special Issue Cyanobacteria: Ecology, Physiology and Genetics)

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