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Ecophysiology of the Cosmopolitan OM252 Bacterioplankton (Gammaproteobacteria)
Among the thousands of species that comprise marine bacterioplankton communities, most remain functionally obscure. One key cosmopolitan group in this understudied majority is the OM252 clade of Gammaproteobacteria. Although frequently found in sequence data and even previously cultured, the diversi...
Autores principales: | , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Microbiology
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8269220/ https://www.ncbi.nlm.nih.gov/pubmed/34184914 http://dx.doi.org/10.1128/mSystems.00276-21 |
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author | Savoie, Emily R. Lanclos, V. Celeste Henson, Michael W. Cheng, Chuankai Getz, Eric W. Barnes, Shelby J. LaRowe, Douglas E. Rappé, Michael S. Thrash, J. Cameron |
author_facet | Savoie, Emily R. Lanclos, V. Celeste Henson, Michael W. Cheng, Chuankai Getz, Eric W. Barnes, Shelby J. LaRowe, Douglas E. Rappé, Michael S. Thrash, J. Cameron |
author_sort | Savoie, Emily R. |
collection | PubMed |
description | Among the thousands of species that comprise marine bacterioplankton communities, most remain functionally obscure. One key cosmopolitan group in this understudied majority is the OM252 clade of Gammaproteobacteria. Although frequently found in sequence data and even previously cultured, the diversity, metabolic potential, physiology, and distribution of this clade has not been thoroughly investigated. Here, we examined these features of OM252 bacterioplankton using a newly isolated strain and genomes from publicly available databases. We demonstrated that this group constitutes a globally distributed novel genus (“Candidatus Halomarinus”), sister to Litoricola, comprising two subclades and multiple distinct species. OM252 organisms have small genomes (median, 2.21 Mbp) and are predicted obligate aerobes capable of alternating between chemoorganoheterotrophic and chemolithotrophic growth using reduced sulfur compounds as electron donors. Subclade I genomes encode genes for the Calvin-Benson-Bassham cycle for carbon fixation. One representative strain of subclade I, LSUCC0096, had extensive halotolerance and a mesophilic temperature range for growth, with a maximum rate of 0.36 doublings/h at 35°C. Cells were curved rod/spirillum-shaped, ∼1.5 by 0.2 μm. Growth yield on thiosulfate as the sole electron donor under autotrophic conditions was roughly one-third that of heterotrophic growth, even though calculations indicated similar Gibbs energies for both catabolisms. These phenotypic data show that some “Ca. Halomarinus” organisms can switch between serving as carbon sources or sinks and indicate the likely anabolic cost of lithoautotrophic growth. Our results thus provide new hypotheses about the roles of these organisms in global biogeochemical cycling of carbon and sulfur. IMPORTANCE Marine microbial communities are teeming with understudied taxa due to the sheer numbers of species in any given sample of seawater. One group, the OM252 clade of Gammaproteobacteria, has been identified in gene surveys from myriad locations, and one isolated organism has even been genome sequenced (HIMB30). However, further study of these organisms has not occurred. Using another isolated representative (strain LSUCC0096) and publicly available genome sequences from metagenomic and single-cell genomic data sets, we examined the diversity within the OM252 clade and the distribution of these taxa in the world’s oceans, reconstructed the predicted metabolism of the group, and quantified growth dynamics in LSUCC0096. Our results generate new knowledge about the previously enigmatic OM252 clade and point toward the importance of facultative chemolithoautotrophy for supporting some clades of ostensibly “heterotrophic” taxa. |
format | Online Article Text |
id | pubmed-8269220 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
spelling | pubmed-82692202021-08-02 Ecophysiology of the Cosmopolitan OM252 Bacterioplankton (Gammaproteobacteria) Savoie, Emily R. Lanclos, V. Celeste Henson, Michael W. Cheng, Chuankai Getz, Eric W. Barnes, Shelby J. LaRowe, Douglas E. Rappé, Michael S. Thrash, J. Cameron mSystems Research Article Among the thousands of species that comprise marine bacterioplankton communities, most remain functionally obscure. One key cosmopolitan group in this understudied majority is the OM252 clade of Gammaproteobacteria. Although frequently found in sequence data and even previously cultured, the diversity, metabolic potential, physiology, and distribution of this clade has not been thoroughly investigated. Here, we examined these features of OM252 bacterioplankton using a newly isolated strain and genomes from publicly available databases. We demonstrated that this group constitutes a globally distributed novel genus (“Candidatus Halomarinus”), sister to Litoricola, comprising two subclades and multiple distinct species. OM252 organisms have small genomes (median, 2.21 Mbp) and are predicted obligate aerobes capable of alternating between chemoorganoheterotrophic and chemolithotrophic growth using reduced sulfur compounds as electron donors. Subclade I genomes encode genes for the Calvin-Benson-Bassham cycle for carbon fixation. One representative strain of subclade I, LSUCC0096, had extensive halotolerance and a mesophilic temperature range for growth, with a maximum rate of 0.36 doublings/h at 35°C. Cells were curved rod/spirillum-shaped, ∼1.5 by 0.2 μm. Growth yield on thiosulfate as the sole electron donor under autotrophic conditions was roughly one-third that of heterotrophic growth, even though calculations indicated similar Gibbs energies for both catabolisms. These phenotypic data show that some “Ca. Halomarinus” organisms can switch between serving as carbon sources or sinks and indicate the likely anabolic cost of lithoautotrophic growth. Our results thus provide new hypotheses about the roles of these organisms in global biogeochemical cycling of carbon and sulfur. IMPORTANCE Marine microbial communities are teeming with understudied taxa due to the sheer numbers of species in any given sample of seawater. One group, the OM252 clade of Gammaproteobacteria, has been identified in gene surveys from myriad locations, and one isolated organism has even been genome sequenced (HIMB30). However, further study of these organisms has not occurred. Using another isolated representative (strain LSUCC0096) and publicly available genome sequences from metagenomic and single-cell genomic data sets, we examined the diversity within the OM252 clade and the distribution of these taxa in the world’s oceans, reconstructed the predicted metabolism of the group, and quantified growth dynamics in LSUCC0096. Our results generate new knowledge about the previously enigmatic OM252 clade and point toward the importance of facultative chemolithoautotrophy for supporting some clades of ostensibly “heterotrophic” taxa. American Society for Microbiology 2021-06-29 /pmc/articles/PMC8269220/ /pubmed/34184914 http://dx.doi.org/10.1128/mSystems.00276-21 Text en Copyright © 2021 Savoie et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Research Article Savoie, Emily R. Lanclos, V. Celeste Henson, Michael W. Cheng, Chuankai Getz, Eric W. Barnes, Shelby J. LaRowe, Douglas E. Rappé, Michael S. Thrash, J. Cameron Ecophysiology of the Cosmopolitan OM252 Bacterioplankton (Gammaproteobacteria) |
title | Ecophysiology of the Cosmopolitan OM252 Bacterioplankton (Gammaproteobacteria) |
title_full | Ecophysiology of the Cosmopolitan OM252 Bacterioplankton (Gammaproteobacteria) |
title_fullStr | Ecophysiology of the Cosmopolitan OM252 Bacterioplankton (Gammaproteobacteria) |
title_full_unstemmed | Ecophysiology of the Cosmopolitan OM252 Bacterioplankton (Gammaproteobacteria) |
title_short | Ecophysiology of the Cosmopolitan OM252 Bacterioplankton (Gammaproteobacteria) |
title_sort | ecophysiology of the cosmopolitan om252 bacterioplankton (gammaproteobacteria) |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8269220/ https://www.ncbi.nlm.nih.gov/pubmed/34184914 http://dx.doi.org/10.1128/mSystems.00276-21 |
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