Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: 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
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
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
_version_ 1783720529563222016
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
work_keys_str_mv AT savoieemilyr ecophysiologyofthecosmopolitanom252bacterioplanktongammaproteobacteria
AT lanclosvceleste ecophysiologyofthecosmopolitanom252bacterioplanktongammaproteobacteria
AT hensonmichaelw ecophysiologyofthecosmopolitanom252bacterioplanktongammaproteobacteria
AT chengchuankai ecophysiologyofthecosmopolitanom252bacterioplanktongammaproteobacteria
AT getzericw ecophysiologyofthecosmopolitanom252bacterioplanktongammaproteobacteria
AT barnesshelbyj ecophysiologyofthecosmopolitanom252bacterioplanktongammaproteobacteria
AT larowedouglase ecophysiologyofthecosmopolitanom252bacterioplanktongammaproteobacteria
AT rappemichaels ecophysiologyofthecosmopolitanom252bacterioplanktongammaproteobacteria
AT thrashjcameron ecophysiologyofthecosmopolitanom252bacterioplanktongammaproteobacteria