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Microbial Adaptations and Genomes under Extreme Conditions

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

Deadline for manuscript submissions: closed (31 March 2023) | Viewed by 26438

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Special Issue Editors

Dr. Alain Dolla

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Guest Editor

Mediterranean Institute of Oceanography, Aix Marseille Université, Université de Toulon, CNRS, IRD, Marseille, France
Interests: microbial adapatation to pressure; anaerobic microorganisms; functional genomics
Special Issues, Collections and Topics in MDPI journals

Dr. Jean Luc Cayol

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Guest Editor

Mediterranean Institute of Oceanography, Aix Marseille Univ, Université de Toulon, CNRS, IRD, Marseille, France
Interests: halophiles; anaerobiosis; methanogens; phylogeny of extremophiles

Special Issue Information

Dear Colleagues,

Life under extreme conditions has been a subject under scrutiny in the last few decades for numerous studies. Extreme conditions are often defined from anthropocentric criteria and include physical extremes such as temperature, radiation or pressure and geochemical extremes such as salinity, pH, oxygen tension or desiccation. For every extreme environmental condition investigated, a variety of organisms have shown that not only can they tolerate these conditions, but also that they often require these extreme conditions for living. These extremophilic or extremotolerant organisms exhibit genomic, structural and metabolic adaptations to cope with their specific environmental conditions. Their studies have implications for prediction of the boundaries of life, origin of life and exobiology, as well as for biotechnological applications.

In this Special Issue of Microorganisms, we invite you to send contributions, in the form of original research or review papers, concerning any aspects related to the microbial adaptations and genomes under extreme conditions, from the identification and characterization of microbial communities inhabiting extreme environments to the macromolecules and metabolism adaptation to extreme conditions.

Dr. Alain Dolla
Dr. Jean Luc Cayol
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

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

Extreme environment
microbial communities
(poly)extremophile
extremotolerance
response to extreme conditions
macromolecules adaptation
metabolism adaptation

Published Papers (10 papers)

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Research

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14 pages, 2335 KiB

Open AccessArticle

Bioluminescence Contributes to the Adaptation of Deep-Sea Bacterium Photobacterium phosphoreum ANT-2200 to High Hydrostatic Pressure

by Xu-Chong Bao, Hong-Zhi Tang, Xue-Gong Li, An-Qi Li, Xiao-Qing Qi, Deng-Hui Li, Shan-Shan Liu, Long-Fei Wu and Wei-Jia Zhang

Microorganisms 2023, 11(6), 1362; https://doi.org/10.3390/microorganisms11061362 - 23 May 2023

Viewed by 1591

Abstract

Bioluminescence is a common phenomenon in nature, especially in the deep ocean. The physiological role of bacterial bioluminescence involves protection against oxidative and UV stresses. Yet, it remains unclear if bioluminescence contributes to deep-sea bacterial adaptation to high hydrostatic pressure (HHP). In this study, we constructed a non-luminescent mutant of ΔluxA and its complementary strain c-ΔluxA of Photobacterium phosphoreum ANT-2200, a deep-sea piezophilic bioluminescent bacterium. The wild-type strain, mutant and complementary strain were compared from aspects of pressure tolerance, intracellular reactive oxygen species (ROS) level and expression of ROS-scavenging enzymes. The results showed that, despite similar growth profiles, HHP induced the accumulation of intracellular ROS and up-regulated the expression of ROS-scavenging enzymes such as dyp, katE and katG, specifically in the non-luminescent mutant. Collectively, our results suggested that bioluminescence functions as the primary antioxidant system in strain ANT-2200, in addition to the well-known ROS-scavenging enzymes. Bioluminescence contributes to bacterial adaptation to the deep-sea environment by coping with oxidative stress generated from HHP. These results further expanded our understanding of the physiological significance of bioluminescence as well as a novel strategy for microbial adaptation to a deep-sea environment. Full article

(This article belongs to the Special Issue Microbial Adaptations and Genomes under Extreme Conditions)

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17 pages, 1798 KiB

Open AccessArticle

Adaptation Strategies to High Hydrostatic Pressures in Pseudothermotoga species Revealed by Transcriptional Analyses

by Romain Fenouil, Nathalie Pradel, Hassiba Belahbib, Marie Roumagnac, Manon Bartoli, Wajdi Ben Hania, Yann Denis, Marc Garel, Christian Tamburini, Bernard Ollivier, Zarath Summers, Fabrice Armougom and Alain Dolla

Microorganisms 2023, 11(3), 773; https://doi.org/10.3390/microorganisms11030773 - 17 Mar 2023

Cited by 1 | Viewed by 1507

Abstract

Pseudothermotoga elfii strain DSM9442 and P. elfii subsp. lettingae strain DSM14385 are hyperthermophilic bacteria. P. elfii DSM9442 is a piezophile and was isolated from a depth of over 1600 m in an oil-producing well in Africa. P. elfii subsp. lettingae is piezotolerant and was isolated from a thermophilic bioreactor fed with methanol as the sole carbon and energy source. In this study, we analyzed both strains at the genomic and transcriptomic levels, paying particular attention to changes in response to pressure increases. Transcriptomic analyses revealed common traits of adaptation to increasing hydrostatic pressure in both strains, namely, variations in transport membrane or carbohydrate metabolism, as well as species-specific adaptations such as variations in amino acid metabolism and transport for the deep P. elfii DSM9442 strain. Notably, this work highlights the central role played by the amino acid aspartate as a key intermediate of the pressure adaptation mechanisms in the deep strain P. elfii DSM9442. Our comparative genomic and transcriptomic analysis revealed a gene cluster involved in lipid metabolism that is specific to the deep strain and that was differentially expressed at high hydrostatic pressures and might, thus, be a good candidate for a piezophilic gene marker in Pseudothermotogales. Full article

(This article belongs to the Special Issue Microbial Adaptations and Genomes under Extreme Conditions)

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13 pages, 1632 KiB

Open AccessArticle

Piezophilic Phenotype Is Growth Condition Dependent and Correlated with the Regulation of Two Sets of ATPase in Deep-Sea Piezophilic Bacterium Photobacterium profundum SS9

by An-Qi Li, Wei-Jia Zhang, Xue-Gong Li, Xu-Chong Bao, Xiao-Qing Qi, Long-Fei Wu and Douglas H. Bartlett

Microorganisms 2023, 11(3), 637; https://doi.org/10.3390/microorganisms11030637 - 2 Mar 2023

Cited by 1 | Viewed by 1387

Abstract

Alteration of respiratory components as a function of pressure is a common strategy developed in deep-sea microorganisms, presumably to adapt to high hydrostatic pressure (HHP). While the electron transport chain and terminal reductases have been extensively studied in deep-sea bacteria, little is known about their adaptations for ATP generation. In this study, we showed that the deep-sea bacterium Photobacterium profundum SS9 exhibits a more pronounced piezophilic phenotype when grown in minimal medium supplemented with glucose (MG) than in the routinely used MB2216 complex medium. The intracellular ATP level varied with pressure, but with opposite trends in the two culture media. Between the two ATPase systems encoded in SS9, ATPase-I played a dominant role when cultivated in MB2216, whereas ATPase-II was more abundant in the MG medium, especially at elevated pressure when cells had the lowest ATP level among all conditions tested. Further analyses of the ΔatpI, ΔatpE1 and ΔatpE2 mutants showed that disrupting ATPase-I induced expression of ATPase-II and that the two systems are functionally redundant in MB2216. Collectively, we provide the first examination of the differences and relationships between two ATPase systems in a piezophilic bacterium, and expanded our understanding of the involvement of energy metabolism in pressure adaptation. Full article

(This article belongs to the Special Issue Microbial Adaptations and Genomes under Extreme Conditions)

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15 pages, 1905 KiB

Open AccessArticle

Environmental Adaptability and Organic Pollutant Degradation Capacity of a Novel Rhodococcus Species Derived from Soil in the Uninhabited Area of the Qinghai-Tibet Plateau

by Jiao Huang, Guomin Ai, Ning Liu and Ying Huang

Microorganisms 2022, 10(10), 1935; https://doi.org/10.3390/microorganisms10101935 - 29 Sep 2022

Cited by 1 | Viewed by 1436

Abstract

The Qinghai-Tibet Plateau (QTP) is known for extreme natural environments and, surprisingly, has been reported to contain widespread organic pollutants. Rhodococcus can survive a variety of extreme environments and degrade many organic contaminants. Here, we isolated a Rhodococcus strain (FXJ9.536 = CGMCC 4.7853) from a soil sample collected in the QTP. Phylogenomic analysis indicated that the strain represents a novel Rhodococcus species, for which the name Rhodococcus tibetensis sp. nov. is proposed. Interestingly, R. tibetensis FXJ9.536 maintained a fast growth rate and degraded 6.2% of p-nitrophenol (4-NP) and 50.0% of malathion even at 10 °C. It could degrade 53.6% of 4-NP and 99.9% of malathion at a moderate temperature. The genome of R. tibetensis FXJ9.536 contains 4-hydroxyphenylacetate 3-monoxygenase and carboxylesterase genes, which are likely associated with the degradation of 4-NP and malathion, respectively. Further genomic analysis revealed that the strain might employ multiple strategies to adapt to the harsh QTP environment. These include synthesizing cold shock proteins, compatible solutes, secondary metabolites, and storage compounds, utilizing inorganic compounds as energy and nutrition sources, as well as degrading a range of organic pollutants. Overall, our study reveals the potential of a QTP-derived new actinobacterial species for environmental adaptation and remediation in cold regions. Full article

(This article belongs to the Special Issue Microbial Adaptations and Genomes under Extreme Conditions)

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20 pages, 1761 KiB

Open AccessArticle

Unraveling the Genomic Potential of the Thermophilic Bacterium Anoxybacillus flavithermus from an Antarctic Geothermal Environment

by Júnia Schultz, Mariana Teixeira Dornelles Parise, Doglas Parise, Laenne G. Medeiros, Thiago J. Sousa, Rodrigo B. Kato, Ana Paula Trovatti Uetanabaro, Fabrício Araújo, Rommel Thiago Jucá Ramos, Siomar de Castro Soares, Bertram Brenig, Vasco Ariston de Carvalho Azevedo, Aristóteles Góes-Neto and Alexandre S. Rosado

Microorganisms 2022, 10(8), 1673; https://doi.org/10.3390/microorganisms10081673 - 19 Aug 2022

Cited by 2 | Viewed by 3385

Abstract

Antarctica is a mosaic of extremes. It harbors active polar volcanoes, such as Deception Island, a marine stratovolcano having notable temperature gradients over very short distances, with the temperature reaching up to 100 °C near the fumaroles and subzero temperatures being noted in the glaciers. From the sediments of Deception Island, we isolated representatives of the genus Anoxybacillus, a widely spread genus that is mainly encountered in thermophilic environments. However, the phylogeny of this genus and its adaptive mechanisms in the geothermal sites of cold environments remain unknown. To the best of our knowledge, this is the first study to unravel the genomic features and provide insights into the phylogenomics and metabolic potential of members of the genus Anoxybacillus inhabiting the Antarctic thermophilic ecosystem. Here, we report the genome sequencing data of seven A. flavithermus strains isolated from two geothermal sites on Deception Island, Antarctic Peninsula. Their genomes were approximately 3.0 Mb in size, had a G + C ratio of 42%, and were predicted to encode 3500 proteins on average. We observed that the strains were phylogenomically closest to each other (Average Nucleotide Identity (ANI) > 98%) and to A. flavithermus (ANI 95%). In silico genomic analysis revealed 15 resistance and metabolic islands, as well as genes related to genome stabilization, DNA repair systems against UV radiation threats, temperature adaptation, heat- and cold-shock proteins (Csps), and resistance to alkaline conditions. Remarkably, glycosyl hydrolase enzyme-encoding genes, secondary metabolites, and prophage sequences were predicted, revealing metabolic and cellular capabilities for potential biotechnological applications. Full article

(This article belongs to the Special Issue Microbial Adaptations and Genomes under Extreme Conditions)

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12 pages, 2369 KiB

Open AccessArticle

Adaptation of Cyanobacteria to the Endolithic Light Spectrum in Hyper-Arid Deserts

by Bayleigh Murray, Emine Ertekin, Micah Dailey, Nathan T. Soulier, Gaozhong Shen, Donald A. Bryant, Cesar Perez-Fernandez and Jocelyne DiRuggiero

Microorganisms 2022, 10(6), 1198; https://doi.org/10.3390/microorganisms10061198 - 11 Jun 2022

Cited by 7 | Viewed by 2486

Abstract

In hyper-arid deserts, endolithic microbial communities survive in the pore spaces and cracks of rocks, an environment that enhances water retention and filters UV radiation. The rock colonization zone is enriched in far-red light (FRL) and depleted in visible light. This poses a challenge to cyanobacteria, which are the primary producers of endolithic communities. Many species of cyanobacteria are capable of Far-Red-Light Photoacclimation (FaRLiP), a process in which FRL induces the synthesis of specialized chlorophylls and remodeling of the photosynthetic apparatus, providing the ability to grow in FRL. While FaRLiP has been reported in cyanobacteria from various low-light environments, our understanding of light adaptations for endolithic cyanobacteria remains limited. Here, we demonstrated that endolithic Chroococcidiopsis isolates from deserts around the world synthesize chlorophyll f, an FRL-specialized chlorophyll when FRL is the sole light source. The metagenome-assembled genomes of these isolates encoded chlorophyll f synthase and all the genes required to implement the FaRLiP response. We also present evidence of FRL-induced changes to the major light-harvesting complexes of a Chroococcidiopsis isolate. These findings indicate that endolithic cyanobacteria from hyper-arid deserts use FRL photoacclimation as an adaptation to the unique light transmission spectrum of their rocky habitat. Full article

(This article belongs to the Special Issue Microbial Adaptations and Genomes under Extreme Conditions)

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14 pages, 2094 KiB

Open AccessArticle

Metabolism of the Genus Guyparkeria Revealed by Pangenome Analysis

by Maggie C. Y. Lau Vetter, Baowei Huang, Linda Fenske and Jochen Blom

Microorganisms 2022, 10(4), 724; https://doi.org/10.3390/microorganisms10040724 - 28 Mar 2022

Viewed by 2469

Abstract

Halophilic sulfur-oxidizing bacteria belonging to the genus Guyparkeria occur at both marine and terrestrial habitats. Common physiological characteristics displayed by Guyparkeria isolates have not yet been linked to the metabolic potential encoded in their genetic inventory. To provide a genetic basis for understanding the metabolism of Guyparkeria, nine genomes were compared to reveal the metabolic capabilities and adaptations. A detailed account is given on Guyparkeria’s ability to assimilate carbon by fixation, to oxidize reduced sulfur, to oxidize thiocyanate, and to cope with salinity stress. Full article

(This article belongs to the Special Issue Microbial Adaptations and Genomes under Extreme Conditions)

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14 pages, 1139 KiB

Open AccessArticle

Characterisation of Waterborne Psychrophilic Massilia Isolates with Violacein Production and Description of Massilia antarctica sp. nov.

by Ivo Sedláček, Pavla Holochová, Hans-Jürgen Busse, Vendula Koublová, Stanislava Králová, Pavel Švec, Roman Sobotka, Eva Staňková, Jan Pilný, Ondrej Šedo, Jana Smolíková and Karel Sedlář

Microorganisms 2022, 10(4), 704; https://doi.org/10.3390/microorganisms10040704 - 24 Mar 2022

Cited by 14 | Viewed by 3596

Abstract

A group of seven bacterial strains producing blue-purple pigmented colonies on R2A agar was isolated from freshwater samples collected in a deglaciated part of James Ross Island and Eagle Island, Antarctica, from 2017–2019. The isolates were psychrophilic, oligotrophic, resistant to chloramphenicol, and exhibited strong hydrolytic activities. To clarify the taxonomic position of these isolates, a polyphasic taxonomic approach was applied based on sequencing of the 16S rRNA, gyrB and lepA genes, whole-genome sequencing, rep-PCR, MALDI-TOF MS, chemotaxonomy analyses and biotyping. Phylogenetic analysis of the 16S rRNA gene sequences revealed that the entire group are representatives of the genus Massilia. The closest relatives of the reference strain P8398^T were Massilia atriviolacea, Massilia violaceinigra, Massilia rubra, Massilia mucilaginosa, Massilia aquatica, Massilia frigida, Massilia glaciei and Massilia eurypsychrophila with a pairwise similarity of 98.6–100% in the 16S rRNA. The subsequent gyrB and lepA sequencing results showed the novelty of the analysed group, and the average nucleotide identity and digital DNA–DNA hybridisation values clearly proved that P8398^T represents a distinct Massilia species. After all these results, we nominate a new species with the proposed name Massilia antarctica sp. nov. The type strain is P8398^T (= CCM 8941^T = LMG 32108^T). Full article

(This article belongs to the Special Issue Microbial Adaptations and Genomes under Extreme Conditions)

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19 pages, 3465 KiB

Open AccessArticle

Comparative Genomic Analyses of the Genus Nesterenkonia Unravels the Genomic Adaptation to Polar Extreme Environments

by Daoxin Dai, Huibin Lu, Peng Xing and Qinglong Wu

Microorganisms 2022, 10(2), 233; https://doi.org/10.3390/microorganisms10020233 - 21 Jan 2022

Cited by 9 | Viewed by 2881

Abstract

The members of the Nesterenkonia genus have been isolated from various habitats, like saline soil, salt lake, sponge-associated and the human gut, some of which are even located in polar areas. To identify their stress resistance mechanisms and draw a genomic profile across this genus, we isolated four Nesterenkonia strains from the lakes in the Tibetan Plateau, referred to as the third pole, and compared them with all other 30 high-quality Nesterenkonia genomes that are deposited in NCBI. The Heaps’ law model estimated that the pan-genome of this genus is open and the number of core, shell, cloud, and singleton genes were 993 (6.61%), 2782 (18.52%), 4117 (27.40%), and 7132 (47.47%), respectively. Phylogenomic and ANI/AAI analysis indicated that all genomes can be divided into three main clades, named NES-1, NES-2, and NES-3. The strains isolated from lakes in the Tibetan Plateau were clustered with four strains from different sources in the Antarctic and formed a subclade within NES-2, described as NES-AT. Genome features of this subclade, including GC (guanine + cytosine) content, tRNA number, carbon/nitrogen atoms per residue side chain (C/N-ARSC), and amino acid composition, in NES-AT individuals were significantly different from other strains, indicating genomic adaptation to cold, nutrient-limited, osmotic, and ultraviolet conditions in polar areas. Functional analysis revealed the enrichment of specific genes involved in bacteriorhodopsin synthesis, biofilm formation, and more diverse nutrient substance metabolism genes in the NES-AT clade, suggesting potential adaptation strategies for energy metabolism in polar environments. This study provides a comprehensive profile of the genomic features of the Nesterenkonia genus and reveals the possible mechanism for the survival of Nesterenkonia isolates in polar areas. Full article

(This article belongs to the Special Issue Microbial Adaptations and Genomes under Extreme Conditions)

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Review

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21 pages, 1737 KiB

Open AccessReview

“Freezing” Thermophiles: From One Temperature Extreme to Another

by Tetyana Milojevic, Margaret Anne Cramm, Casey R. J. Hubert and Frances Westall

Microorganisms 2022, 10(12), 2417; https://doi.org/10.3390/microorganisms10122417 - 6 Dec 2022

Cited by 3 | Viewed by 4152

Abstract

New detections of thermophiles in psychrobiotic (i.e., bearing cold-tolerant life forms) marine and terrestrial habitats including Arctic marine sediments, Antarctic accretion ice, permafrost, and elsewhere are continually being reported. These microorganisms present great opportunities for microbial ecologists to examine biogeographical processes for spore-formers and non-spore-formers alike, including dispersal histories connecting warm and cold biospheres. In this review, we examine different examples of thermophiles in cryobiotic locations, and highlight exploration of thermophiles at cold temperatures under laboratory conditions. The survival of thermophiles in psychrobiotic environments provokes novel considerations of physiological and molecular mechanisms underlying natural cryopreservation of microorganisms. Cultures of thermophiles maintained at low temperature may serve as a non-sporulating laboratory model for further exploration of metabolic potential of thermophiles at psychrobiotic temperatures, as well as for elucidating molecular mechanisms behind natural preservation and adaptation to psychrobiotic environments. These investigations are highly relevant for the search for life on other cold and icy planets in the Solar System, such as Mars, Europa and Enceladus. Full article

(This article belongs to the Special Issue Microbial Adaptations and Genomes under Extreme Conditions)

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