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Advances in the Biology of Phototrophic Bacteria
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Advances in the Biology of Phototrophic Bacteria

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Environmental Microbiology".

Deadline for manuscript submissions: closed (31 March 2021) | Viewed by 55029

Printed Edition Available!
A printed edition of this Special Issue is available here.

Special Issue Editor

Prof. Dr. Johannes F. Imhoff

E-Mail Website
Guest Editor
Marine Mikrobiologie, Helmholtz Centre for Ocean Research GEOMAR, Düsternbrooker Weg 20, D-24105 Kiel, Germany
Interests: marine microbial diversity; marine biotechnology; marine natural products; phylogeny and taxonomy of anoxygenic phototrophic bacteria; photosynthetic bacteria from extreme environments
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Phototrophic bacteria represent a remarkable group of microorganisms which has significantly shaped the earth environment over millennia. During early ages and in the absence of oxygen in the atmosphere, photosynthetic capabilities have developed in several prokaryotic phyla, including Chlorobi, Heliobacteria, Chloroflexi, Chloracidobacteria, and Proteobacteria. With the onset of oxygenic photosynthesis and the release of oxygen into the atmosphere, the conditions for life changed dramatically, and many phototrophic bacteria were pushed back to anoxic environmental niches. On the other hand, oxygen helped to initiate adaptation of some phototrophic bacteria, making them well adapted to live in the anoxic environment to various levels of oxygen. Finally, this has led to dependence on oxygen for a number of anoxygenic photosynthetic bacteria. As a consequence, phototrophic bacteria are found in all kinds of photic environments, including those with extreme conditions for life as hot vents, saturated brines, acid peat bogs, dry rock surfaces or even solid ice. They proliferate under very low as well as under extremely high rates of illumination, in the strict absence of oxygen, and also under the full pressure of atmospheric oxygen.

In this Special Issue of Microorganisms, you are invited to send contributions (original articles as well as reviews) concerning the biology and biodiversity of phototrophic bacteria, in particular using genomic and metagenomic approaches to study microbial communities. Information that will improve our understanding of the evolution of photosynthesis and phototrophic bacteria, of their adaptation to the wide spectrum of environmental conditions, and of their genetic and functional diversity is especially welcome.

Prof. Dr. Johannes F. Imhoff
Guest Editor

Manuscript Submission Information

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Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Microorganisms is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2700 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • Bacterial photosynthesis
  • Phototrophic bacteria
  • Anoxygenic photosynthesis
  • Anaerobic/aerobic phototrophic way of life
  • Phylogeny
  • Evolution
  • Genetic/functional biodiversity
  • Environmental gradients
  • Thermophilic
  • Halophilic

Published Papers (14 papers)

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Editorial

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5 pages, 209 KiB  
Editorial
Editorial for the Special Issue: Advances in the Biology of Phototrophic Bacteria
by Johannes F. Imhoff
Microorganisms 2021, 9(10), 2119; https://doi.org/10.3390/microorganisms9102119 - 08 Oct 2021
Cited by 2 | Viewed by 1933
Abstract
Phototrophic bacteria represent a very ancient phylogenetic and highly diverse metabolic type of bacteria that diverged early into several major phylogenetic lineages with quite different properties [...] Full article
(This article belongs to the Special Issue Advances in the Biology of Phototrophic Bacteria)

Research

Jump to: Editorial

19 pages, 2953 KiB  
Article
Discovery of Siderophore and Metallophore Production in the Aerobic Anoxygenic Phototrophs
by Steven B. Kuzyk, Elizabeth Hughes and Vladimir Yurkov
Microorganisms 2021, 9(5), 959; https://doi.org/10.3390/microorganisms9050959 - 29 Apr 2021
Cited by 11 | Viewed by 3494
Abstract
Aerobic anoxygenic phototrophs have been isolated from a rich variety of environments including marine ecosystems, freshwater and meromictic lakes, hypersaline springs, and biological soil crusts, all in the hopes of understanding their ecological niche. Over 100 isolates were chosen for this study, representing [...] Read more.
Aerobic anoxygenic phototrophs have been isolated from a rich variety of environments including marine ecosystems, freshwater and meromictic lakes, hypersaline springs, and biological soil crusts, all in the hopes of understanding their ecological niche. Over 100 isolates were chosen for this study, representing 44 species from 27 genera. Interactions with Fe3+ and other metal(loid) cations such as Mg2+, V3+, Mn2+, Co2+, Ni2+, Cu2+, Zn2+, Se4+ and Te2+ were tested using a chromeazurol S assay to detect siderophore or metallophore production, respectively. Representatives from 20 species in 14 genera of α-Proteobacteria, or 30% of strains, produced highly diffusible siderophores that could bind one or more metal(loid)s, with activity strength as follows: Fe > Zn > V > Te > Cu > Mn > Mg > Se > Ni > Co. In addition, γ-proteobacterial Chromocurvus halotolerans, strain EG19 excreted a brown compound into growth medium, which was purified and confirmed to act as a siderophore. It had an approximate size of ~341 Da and drew similarities to the siderophore rhodotorulic acid, a member of the hydroxamate group, previously found only among yeasts. This study is the first to discover siderophore production to be widespread among the aerobic anoxygenic phototrophs, which may be another key method of metal(loid) chelation and potential detoxification within their environments. Full article
(This article belongs to the Special Issue Advances in the Biology of Phototrophic Bacteria)
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13 pages, 2972 KiB  
Article
Characterization of the Aerobic Anoxygenic Phototrophic Bacterium Sphingomonas sp. AAP5
by Karel Kopejtka, Yonghui Zeng, David Kaftan, Vadim Selyanin, Zdenko Gardian, Jürgen Tomasch, Ruben Sommaruga and Michal Koblížek
Microorganisms 2021, 9(4), 768; https://doi.org/10.3390/microorganisms9040768 - 06 Apr 2021
Cited by 11 | Viewed by 3849
Abstract
An aerobic, yellow-pigmented, bacteriochlorophyll a-producing strain, designated AAP5 (=DSM 111157=CCUG 74776), was isolated from the alpine lake Gossenköllesee located in the Tyrolean Alps, Austria. Here, we report its description and polyphasic characterization. Phylogenetic analysis of the 16S rRNA gene showed that strain [...] Read more.
An aerobic, yellow-pigmented, bacteriochlorophyll a-producing strain, designated AAP5 (=DSM 111157=CCUG 74776), was isolated from the alpine lake Gossenköllesee located in the Tyrolean Alps, Austria. Here, we report its description and polyphasic characterization. Phylogenetic analysis of the 16S rRNA gene showed that strain AAP5 belongs to the bacterial genus Sphingomonas and has the highest pairwise 16S rRNA gene sequence similarity with Sphingomonas glacialis (98.3%), Sphingomonas psychrolutea (96.8%), and Sphingomonas melonis (96.5%). Its genomic DNA G + C content is 65.9%. Further, in silico DNA-DNA hybridization and calculation of the average nucleotide identity speaks for the close phylogenetic relationship of AAP5 and Sphingomonas glacialis. The high percentage (76.2%) of shared orthologous gene clusters between strain AAP5 and Sphingomonas paucimobilis NCTC 11030T, the type species of the genus, supports the classification of the two strains into the same genus. Strain AAP5 was found to contain C18:1ω7c (64.6%) as a predominant fatty acid (>10%) and the polar lipid profile contained phosphatidylglycerol, diphosphatidylglycerol, phosphatidylethanolamine, sphingoglycolipid, six unidentified glycolipids, one unidentified phospholipid, and two unidentified lipids. The main respiratory quinone was ubiquinone-10. Strain AAP5 is a facultative photoheterotroph containing type-2 photosynthetic reaction centers and, in addition, contains a xathorhodopsin gene. No CO2-fixation pathways were found. Full article
(This article belongs to the Special Issue Advances in the Biology of Phototrophic Bacteria)
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22 pages, 5054 KiB  
Article
In-Situ Metatranscriptomic Analyses Reveal the Metabolic Flexibility of the Thermophilic Anoxygenic Photosynthetic Bacterium Chloroflexus aggregans in a Hot Spring Cyanobacteria-Dominated Microbial Mat
by Shigeru Kawai, Joval N. Martinez, Mads Lichtenberg, Erik Trampe, Michael Kühl, Marcus Tank, Shin Haruta, Arisa Nishihara, Satoshi Hanada and Vera Thiel
Microorganisms 2021, 9(3), 652; https://doi.org/10.3390/microorganisms9030652 - 21 Mar 2021
Cited by 12 | Viewed by 6642
Abstract
Chloroflexus aggregans is a metabolically versatile, thermophilic, anoxygenic phototrophic member of the phylum Chloroflexota (formerly Chloroflexi), which can grow photoheterotrophically, photoautotrophically, chemoheterotrophically, and chemoautotrophically. In hot spring-associated microbial mats, C. aggregans co-exists with oxygenic cyanobacteria under dynamic micro-environmental conditions. To elucidate the [...] Read more.
Chloroflexus aggregans is a metabolically versatile, thermophilic, anoxygenic phototrophic member of the phylum Chloroflexota (formerly Chloroflexi), which can grow photoheterotrophically, photoautotrophically, chemoheterotrophically, and chemoautotrophically. In hot spring-associated microbial mats, C. aggregans co-exists with oxygenic cyanobacteria under dynamic micro-environmental conditions. To elucidate the predominant growth modes of C. aggregans, relative transcription levels of energy metabolism- and CO2 fixation-related genes were studied in Nakabusa Hot Springs microbial mats over a diel cycle and correlated with microscale in situ measurements of O2 and light. Metatranscriptomic analyses indicated two periods with different modes of energy metabolism of C. aggregans: (1) phototrophy around midday and (2) chemotrophy in the early morning hours. During midday, C. aggregans mainly employed photoheterotrophy when the microbial mats were hyperoxic (400–800 µmol L−1 O2). In the early morning hours, relative transcription peaks of genes encoding uptake hydrogenase, key enzymes for carbon fixation, respiratory complexes as well as enzymes for TCA cycle and acetate uptake suggest an aerobic chemomixotrophic lifestyle. This is the first in situ study of the versatile energy metabolism of C. aggregans based on gene transcription patterns. The results provide novel insights into the metabolic flexibility of these filamentous anoxygenic phototrophs that thrive under dynamic environmental conditions. Full article
(This article belongs to the Special Issue Advances in the Biology of Phototrophic Bacteria)
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32 pages, 1973 KiB  
Article
Osmotic Adaptation and Compatible Solute Biosynthesis of Phototrophic Bacteria as Revealed from Genome Analyses
by Johannes F. Imhoff, Tanja Rahn, Sven Künzel, Alexander Keller and Sven C. Neulinger
Microorganisms 2021, 9(1), 46; https://doi.org/10.3390/microorganisms9010046 - 26 Dec 2020
Cited by 30 | Viewed by 4545
Abstract
Osmotic adaptation and accumulation of compatible solutes is a key process for life at high osmotic pressure and elevated salt concentrations. Most important solutes that can protect cell structures and metabolic processes at high salt concentrations are glycine betaine and ectoine. The genome [...] Read more.
Osmotic adaptation and accumulation of compatible solutes is a key process for life at high osmotic pressure and elevated salt concentrations. Most important solutes that can protect cell structures and metabolic processes at high salt concentrations are glycine betaine and ectoine. The genome analysis of more than 130 phototrophic bacteria shows that biosynthesis of glycine betaine is common among marine and halophilic phototrophic Proteobacteria and their chemotrophic relatives, as well as in representatives of Pirellulaceae and Actinobacteria, but are also found in halophilic Cyanobacteria and Chloroherpeton thalassium. This ability correlates well with the successful toleration of extreme salt concentrations. Freshwater bacteria in general lack the possibilities to synthesize and often also to take up these compounds. The biosynthesis of ectoine is found in the phylogenetic lines of phototrophic Alpha- and Gammaproteobacteria, most prominent in the Halorhodospira species and a number of Rhodobacteraceae. It is also common among Streptomycetes and Bacilli. The phylogeny of glycine-sarcosine methyltransferase (GMT) and diaminobutyrate-pyruvate aminotransferase (EctB) sequences correlate well with otherwise established phylogenetic groups. Most significantly, GMT sequences of cyanobacteria form two major phylogenetic branches and the branch of Halorhodospira species is distinct from all other Ectothiorhodospiraceae. A variety of transport systems for osmolytes are present in the studied bacteria. Full article
(This article belongs to the Special Issue Advances in the Biology of Phototrophic Bacteria)
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17 pages, 20692 KiB  
Article
Simultaneous Genome Sequencing of Prosthecochloris ethylica and Desulfuromonas acetoxidans within a Syntrophic Mixture Reveals Unique Pili and Protein Interactions
by John A. Kyndt, Jozef J. Van Beeumen and Terry E. Meyer
Microorganisms 2020, 8(12), 1939; https://doi.org/10.3390/microorganisms8121939 - 07 Dec 2020
Cited by 8 | Viewed by 2559
Abstract
Strains of Chloropseudomonas ethylica, 2-K, N2, and N3 are known to be composed of a syntrophic mixture of a green sulfur bacterium and a sulfur-reducing colorless component. Upon sequence analysis, the green sulfur photosynthetic bacterial component of strain N3 was dominant and [...] Read more.
Strains of Chloropseudomonas ethylica, 2-K, N2, and N3 are known to be composed of a syntrophic mixture of a green sulfur bacterium and a sulfur-reducing colorless component. Upon sequence analysis, the green sulfur photosynthetic bacterial component of strain N3 was dominant and was readily sequenced, but the less abundant sulfur-reducing bacterial component was apparent only when analyzed by metagenomic binning. Whole-genome comparison showed that the green bacterium belonged to the genus Prosthecochloris and apparently was a species for which there was no genome sequence on file. For comparison, we also sequenced the genome of Prosthecochloris sp. DSM 1685, which had previously been isolated from the 2-K mixture in pure culture and have shown that all three Prosthecochloris genomes belong to a new species, which we propose to be named Prosthecochloris ethylica comb. nov. Whole genomes were also sequenced for the isolated Desulfuromonas strains DSM 1675 (from strain 2-K) and DSM 1676 (from strain N2) and shown to be nearly identical to the genome found in the N3 mixture. The genome of the green sulfur bacterium contains large genes for agglutination proteins, similar to the ones proposed to be involved in larger photosynthetic consortia of Chlorochromatium aggregatum. In addition, we also identified several unique “tight adhesion (tad)” pili genes that are presumably involved in the formation of cell–cell interactions. The colorless component, on the other hand, contained a unique large multiheme cytochrome C and unique genes for e-pili (geopilin) formation, genetically clustered with a conserved ferredoxin gene, which are all expected to play an electron transfer role in the closed sulfur cycle in the syntrophic mixture. The findings from the simultaneous genome sequencing of the components of Cp. ethylica have implications for the phenomenon of direct interspecies interactions and coupled electron transfer in photosynthetic symbionts. The mechanisms for such interactions appear to be more common in the environment than originally anticipated. Full article
(This article belongs to the Special Issue Advances in the Biology of Phototrophic Bacteria)
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15 pages, 1876 KiB  
Article
Interactions among Redox Regulators and the CtrA Phosphorelay in Dinoroseobacter shibae and Rhodobacter capsulatus
by Sonja Koppenhöfer and Andrew S. Lang
Microorganisms 2020, 8(4), 562; https://doi.org/10.3390/microorganisms8040562 - 14 Apr 2020
Cited by 6 | Viewed by 2722
Abstract
Bacteria employ regulatory networks to detect environmental signals and respond appropriately, often by adjusting gene expression. Some regulatory networks influence many genes, and many genes are affected by multiple regulatory networks. Here, we investigate the extent to which regulatory systems controlling aerobic–anaerobic energetics [...] Read more.
Bacteria employ regulatory networks to detect environmental signals and respond appropriately, often by adjusting gene expression. Some regulatory networks influence many genes, and many genes are affected by multiple regulatory networks. Here, we investigate the extent to which regulatory systems controlling aerobic–anaerobic energetics overlap with the CtrA phosphorelay, an important system that controls a variety of behavioral processes, in two metabolically versatile alphaproteobacteria, Dinoroseobacter shibae and Rhodobacter capsulatus. We analyzed ten available transcriptomic datasets from relevant regulator deletion strains and environmental changes. We found that in D. shibae, the CtrA phosphorelay represses three of the four aerobic–anaerobic Crp/Fnr superfamily regulator-encoding genes (fnrL, dnrD, and especially dnrF). At the same time, all four Crp/Fnr regulators repress all three phosphorelay genes. Loss of dnrD or dnrF resulted in activation of the entire examined CtrA regulon, regardless of oxygen tension. In R. capsulatus FnrL, in silico and ChIP-seq data also suggested regulation of the CtrA regulon, but it was only with loss of the redox regulator RegA where an actual transcriptional effect on the CtrA regulon was observed. For the first time, we show that there are complex interactions between redox regulators and the CtrA phosphorelays in these bacteria and we present several models for how these interactions might occur. Full article
(This article belongs to the Special Issue Advances in the Biology of Phototrophic Bacteria)
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15 pages, 1323 KiB  
Article
Niche Partitioning with Temperature among Heterocystous Cyanobacteria (Scytonema spp., Nostoc spp., and Tolypothrix spp.) from Biological Soil Crusts
by Ana Giraldo-Silva, Vanessa M. C. Fernandes, Julie Bethany and Ferran Garcia-Pichel
Microorganisms 2020, 8(3), 396; https://doi.org/10.3390/microorganisms8030396 - 12 Mar 2020
Cited by 15 | Viewed by 3846
Abstract
Heterocystous cyanobacteria of biocrusts are key players for biological fixation in drylands, where nitrogen is only second to water as a limiting resource. We studied the niche partitioning among the three most common biocrust heterocystous cyanobacteria sts using enrichment cultivation and the determination [...] Read more.
Heterocystous cyanobacteria of biocrusts are key players for biological fixation in drylands, where nitrogen is only second to water as a limiting resource. We studied the niche partitioning among the three most common biocrust heterocystous cyanobacteria sts using enrichment cultivation and the determination of growth responses to temperature in 30 representative isolates. Isolates of Scytonema spp. were most thermotolerant, typically growing up to 40 °C, whereas only those of Tolypothrix spp. grew at 4 °C. Nostoc spp. strains responded well at intermediate temperatures. We could trace the heat sensitivity in Nostoc spp. and Tolypothrix spp. to N2-fixation itself, because the upper temperature for growth increased under nitrogen replete conditions. This may involve an inability to develop heterocysts (specialized N2-fixing cells) at high temperatures. We then used a meta-analysis of biocrust molecular surveys spanning four continents to test the relevance of this apparent niche partitioning in nature. Indeed, the geographic distribution of the three types was clearly constrained by the mean local temperature, particularly during the growth season. This allows us to predict a potential shift in dominance in many locales as a result of global warming, to the benefit of Scytonema spp. populations. Full article
(This article belongs to the Special Issue Advances in the Biology of Phototrophic Bacteria)
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24 pages, 3378 KiB  
Article
Analysis of the Complete Genome of the Alkaliphilic and Phototrophic Firmicute Heliorestis convoluta Strain HHT
by Emma D. Dewey, Lynn M. Stokes, Brad M. Burchell, Kathryn N. Shaffer, Austin M. Huntington, Jennifer M. Baker, Suvarna Nadendla, Michelle G. Giglio, Kelly S. Bender, Jeffrey W. Touchman, Robert E. Blankenship, Michael T. Madigan and W. Matthew Sattley
Microorganisms 2020, 8(3), 313; https://doi.org/10.3390/microorganisms8030313 - 25 Feb 2020
Cited by 10 | Viewed by 3458
Abstract
Despite significant interest and past work to elucidate the phylogeny and photochemistry of species of the Heliobacteriaceae, genomic analyses of heliobacteria to date have been limited to just one published genome, that of the thermophilic species Heliobacterium (Hbt.) modesticaldum str. [...] Read more.
Despite significant interest and past work to elucidate the phylogeny and photochemistry of species of the Heliobacteriaceae, genomic analyses of heliobacteria to date have been limited to just one published genome, that of the thermophilic species Heliobacterium (Hbt.) modesticaldum str. Ice1T. Here we present an analysis of the complete genome of a second heliobacterium, Heliorestis (Hrs.) convoluta str. HHT, an alkaliphilic, mesophilic, and morphologically distinct heliobacterium isolated from an Egyptian soda lake. The genome of Hrs. convoluta is a single circular chromosome of 3.22 Mb with a GC content of 43.1% and 3263 protein-encoding genes. In addition to culture-based observations and insights gleaned from the Hbt. modesticaldum genome, an analysis of enzyme-encoding genes from key metabolic pathways supports an obligately photoheterotrophic lifestyle for Hrs. convoluta. A complete set of genes encoding enzymes for propionate and butyrate catabolism and the absence of a gene encoding lactate dehydrogenase distinguishes the carbon metabolism of Hrs. convoluta from its close relatives. Comparative analyses of key proteins in Hrs. convoluta, including cytochrome c553 and the Fo alpha subunit of ATP synthase, with those of related species reveal variations in specific amino acid residues that likely contribute to the success of Hrs. convoluta in its highly alkaline environment. Full article
(This article belongs to the Special Issue Advances in the Biology of Phototrophic Bacteria)
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22 pages, 2417 KiB  
Article
Adaptation to Photooxidative Stress: Common and Special Strategies of the Alphaproteobacteria Rhodobacter sphaeroides and Rhodobacter capsulatus
by Mathieu K. Licht, Aaron M. Nuss, Marcel Volk, Anne Konzer, Michael Beckstette, Bork A. Berghoff and Gabriele Klug
Microorganisms 2020, 8(2), 283; https://doi.org/10.3390/microorganisms8020283 - 19 Feb 2020
Cited by 15 | Viewed by 3961
Abstract
Photosynthetic bacteria have to deal with the risk of photooxidative stress that occurs in presence of light and oxygen due to the photosensitizing activity of (bacterio-) chlorophylls. Facultative phototrophs of the genus Rhodobacter adapt the formation of photosynthetic complexes to oxygen and light [...] Read more.
Photosynthetic bacteria have to deal with the risk of photooxidative stress that occurs in presence of light and oxygen due to the photosensitizing activity of (bacterio-) chlorophylls. Facultative phototrophs of the genus Rhodobacter adapt the formation of photosynthetic complexes to oxygen and light conditions, but cannot completely avoid this stress if environmental conditions suddenly change. R. capsulatus has a stronger pigmentation and faster switches to phototrophic growth than R. sphaeroides. However, its photooxidative stress response has not been investigated. Here, we compare both species by transcriptomics and proteomics, revealing that proteins involved in oxidation–reduction processes, DNA, and protein damage repair play pivotal roles. These functions are likely universal to many phototrophs. Furthermore, the alternative sigma factors RpoE and RpoHII are induced in both species, even though the genetic localization of the rpoE gene, the RpoE protein itself, and probably its regulon, are different. Despite sharing the same habitats, our findings also suggest individual strategies. The crtIB-tspO operon, encoding proteins for biosynthesis of carotenoid precursors and a regulator of photosynthesis, and cbiX, encoding a putative ferrochelatase, are induced in R. capsulatus. This specific response might support adaptation by maintaining high carotenoid-to-bacteriochlorophyll ratios and preventing the accumulation of porphyrin-derived photosensitizers. Full article
(This article belongs to the Special Issue Advances in the Biology of Phototrophic Bacteria)
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15 pages, 2805 KiB  
Article
Succession and Colonization Dynamics of Endolithic Phototrophs within Intertidal Carbonates
by Daniel Roush and Ferran Garcia-Pichel
Microorganisms 2020, 8(2), 214; https://doi.org/10.3390/microorganisms8020214 - 05 Feb 2020
Cited by 12 | Viewed by 2586
Abstract
Photosynthetic endolithic communities are common in shallow marine carbonates, contributing significantly to their bioerosion. Cyanobacteria are well known from these settings, where a few are euendoliths, actively boring into the virgin substrate. Recently, anoxygenic phototrophs were reported as significant inhabitants of endolithic communities, [...] Read more.
Photosynthetic endolithic communities are common in shallow marine carbonates, contributing significantly to their bioerosion. Cyanobacteria are well known from these settings, where a few are euendoliths, actively boring into the virgin substrate. Recently, anoxygenic phototrophs were reported as significant inhabitants of endolithic communities, but it is unknown if they are euendoliths or simply colonize available pore spaces secondarily. To answer this and to establish the dynamics of colonization, nonporous travertine tiles were anchored onto intertidal beach rock in Isla de Mona, Puerto Rico, and developing endolithic communities were examined with time, both molecularly and with photopigment biomarkers. By 9 months, while cyanobacterial biomass and diversity reached levels indistinguishable from those of nearby climax communities, anoxygenic phototrophs remained marginal, suggesting that they are secondary colonizers. Early in the colonization, a novel group of cyanobacteria (unknown boring cluster, UBC) without cultivated representatives, emerged as the most common euendolith, but by 6 months, canonical euendoliths such as Plectonema (Leptolyngbya) sp., Mastigocoleus sp., and Pleurocapsalean clades displaced UBC in dominance. Later, the proportion of euendolithic cyanobacterial biomass decreased, as nonboring endoliths outcompeted pioneers within the already excavated substrate. Our findings demonstrate that endolithic cyanobacterial succession within hard carbonates is complex but can attain maturity within a year’s time. Full article
(This article belongs to the Special Issue Advances in the Biology of Phototrophic Bacteria)
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19 pages, 7757 KiB  
Article
Distribution of Phototrophic Purple Nonsulfur Bacteria in Massive Blooms in Coastal and Wastewater Ditch Environments
by Akira Hiraishi, Nobuyoshi Nagao, Chinatsu Yonekawa, So Umekage, Yo Kikuchi, Toshihiko Eki and Yuu Hirose
Microorganisms 2020, 8(2), 150; https://doi.org/10.3390/microorganisms8020150 - 22 Jan 2020
Cited by 11 | Viewed by 6190
Abstract
The biodiversity of phototrophic purple nonsulfur bacteria (PNSB) in comparison with purple sulfur bacteria (PSB) in colored blooms and microbial mats that developed in coastal mudflats and pools and wastewater ditches was investigated. For this, a combination of photopigment and quinone profiling, pufM [...] Read more.
The biodiversity of phototrophic purple nonsulfur bacteria (PNSB) in comparison with purple sulfur bacteria (PSB) in colored blooms and microbial mats that developed in coastal mudflats and pools and wastewater ditches was investigated. For this, a combination of photopigment and quinone profiling, pufM gene-targeted quantitative PCR, and pufM gene clone library analysis was used in addition to conventional microscopic and cultivation methods. Red and pink blooms in the coastal environments contained PSB as the major populations, and smaller but significant densities of PNSB, with members of Rhodovulum predominating. On the other hand, red-pink blooms and mats in the wastewater ditches exclusively yielded PNSB, with Rhodobacter, Rhodopseudomonas, and/or Pararhodospirillum as the major constituents. The important environmental factors affecting PNSB populations were organic matter and sulfide concentrations and oxidation–reduction potential (ORP). Namely, light-exposed, sulfide-deficient water bodies with high-strength organic matter and in a limited range of ORP provide favorable conditions for the massive growth of PNSB over co-existing PSB. We also report high-quality genome sequences of Rhodovulum sp. strain MB263, previously isolated from a pink mudflat, and Rhodovulum sulfidophilum DSM 1374T, which would enhance our understanding of how PNSB respond to various environmental factors in the natural ecosystem. Full article
(This article belongs to the Special Issue Advances in the Biology of Phototrophic Bacteria)
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20 pages, 2583 KiB  
Article
Multiple Sense and Antisense Promoters Contribute to the Regulated Expression of the isc-suf Operon for Iron-Sulfur Cluster Assembly in Rhodobacter
by Xin Nie, Bernhard Remes and Gabriele Klug
Microorganisms 2019, 7(12), 671; https://doi.org/10.3390/microorganisms7120671 - 10 Dec 2019
Cited by 3 | Viewed by 2518
Abstract
A multitude of biological functions relies on iron-sulfur clusters. The formation of photosynthetic complexes goes along with an additional demand for iron-sulfur clusters for bacteriochlorophyll synthesis and photosynthetic electron transport. However, photooxidative stress leads to the destruction of iron-sulfur clusters, and the released [...] Read more.
A multitude of biological functions relies on iron-sulfur clusters. The formation of photosynthetic complexes goes along with an additional demand for iron-sulfur clusters for bacteriochlorophyll synthesis and photosynthetic electron transport. However, photooxidative stress leads to the destruction of iron-sulfur clusters, and the released iron promotes the formation of further reactive oxygen species. A balanced regulation of iron-sulfur cluster synthesis is required to guarantee the supply of this cofactor, on the one hand, but also to limit stress, on the other hand. The phototrophic alpha-proteobacterium Rhodobacter sphaeroides harbors a large operon for iron-sulfur cluster assembly comprising the iscRS and suf genes. IscR (iron-sulfur cluster regulator) is an iron-dependent regulator of isc-suf genes and other genes with a role in iron metabolism. We applied reporter gene fusions to identify promoters of the isc-suf operon and studied their activity alone or in combination under different conditions. Gel-retardation assays showed the binding of regulatory proteins to individual promoters. Our results demonstrated that several promoters in a sense and antisense direction influenced isc-suf expression and the binding of the IscR, Irr, and OxyR regulatory proteins to individual promoters. These findings demonstrated a complex regulatory network of several promoters and regulatory proteins that helped to adjust iron-sulfur cluster assembly to changing conditions in Rhodobacter sphaeroides. Full article
(This article belongs to the Special Issue Advances in the Biology of Phototrophic Bacteria)
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18 pages, 784 KiB  
Article
Phylogeny of Anoxygenic Photosynthesis Based on Sequences of Photosynthetic Reaction Center Proteins and a Key Enzyme in Bacteriochlorophyll Biosynthesis, the Chlorophyllide Reductase
by Johannes F. Imhoff, Tanja Rahn, Sven Künzel and Sven C. Neulinger
Microorganisms 2019, 7(11), 576; https://doi.org/10.3390/microorganisms7110576 - 19 Nov 2019
Cited by 24 | Viewed by 4812
Abstract
Photosynthesis is a key process for the establishment and maintenance of life on earth, and it is manifested in several major lineages of the prokaryote tree of life. The evolution of photosynthesis in anoxygenic photosynthetic bacteria is of major interest as these have [...] Read more.
Photosynthesis is a key process for the establishment and maintenance of life on earth, and it is manifested in several major lineages of the prokaryote tree of life. The evolution of photosynthesis in anoxygenic photosynthetic bacteria is of major interest as these have the most ancient roots of photosynthetic systems. The phylogenetic relations between anoxygenic phototrophic bacteria were compared on the basis of sequences of key proteins of the type-II photosynthetic reaction center, including PufLM and PufH (PuhA), and a key enzyme of bacteriochlorophyll biosynthesis, the light-independent chlorophyllide reductase BchXYZ. The latter was common to all anoxygenic phototrophic bacteria, including those with a type-I and those with a type-II photosynthetic reaction center. The phylogenetic considerations included cultured phototrophic bacteria from several phyla, including Proteobacteria (138 species), Chloroflexi (five species), Chlorobi (six species), as well as Heliobacterium modesticaldum (Firmicutes), Chloracidobacterium acidophilum (Acidobacteria), and Gemmatimonas phototrophica (Gemmatimonadetes). Whenever available, type strains were studied. Phylogenetic relationships based on a photosynthesis tree (PS tree, including sequences of PufHLM-BchXYZ) were compared with those of 16S rRNA gene sequences (RNS tree). Despite some significant differences, large parts were congruent between the 16S rRNA phylogeny and photosynthesis proteins. The phylogenetic relations demonstrated that bacteriochlorophyll biosynthesis had evolved in ancestors of phototrophic green bacteria much earlier as compared to phototrophic purple bacteria and that multiple events independently formed different lineages of aerobic phototrophic purple bacteria, many of which have very ancient roots. The Rhodobacterales clearly represented the youngest group, which was separated from other Proteobacteria by a large evolutionary gap. Full article
(This article belongs to the Special Issue Advances in the Biology of Phototrophic Bacteria)
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