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Freshwater Chlorobia Exhibit Metabolic Specialization among Cosmopolitan and Endemic Populations

Photosynthetic bacteria from the class Chlorobia (formerly phylum Chlorobi) sustain carbon fixation in anoxic water columns. They harvest light at extremely low intensities and use various inorganic electron donors to fix carbon dioxide into biomass. Until now, most information on the functional eco...

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Autores principales: Garcia, Sarahi L., Mehrshad, Maliheh, Buck, Moritz, Tsuji, Jackson M., Neufeld, Josh D., McMahon, Katherine D., Bertilsson, Stefan, Greening, Chris, Peura, Sari
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8125076/
https://www.ncbi.nlm.nih.gov/pubmed/33975970
http://dx.doi.org/10.1128/mSystems.01196-20
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author Garcia, Sarahi L.
Mehrshad, Maliheh
Buck, Moritz
Tsuji, Jackson M.
Neufeld, Josh D.
McMahon, Katherine D.
Bertilsson, Stefan
Greening, Chris
Peura, Sari
author_facet Garcia, Sarahi L.
Mehrshad, Maliheh
Buck, Moritz
Tsuji, Jackson M.
Neufeld, Josh D.
McMahon, Katherine D.
Bertilsson, Stefan
Greening, Chris
Peura, Sari
author_sort Garcia, Sarahi L.
collection PubMed
description Photosynthetic bacteria from the class Chlorobia (formerly phylum Chlorobi) sustain carbon fixation in anoxic water columns. They harvest light at extremely low intensities and use various inorganic electron donors to fix carbon dioxide into biomass. Until now, most information on the functional ecology and local adaptations of Chlorobia members came from isolates and merely 26 sequenced genomes that may not adequately represent natural populations. To address these limitations, we analyzed global metagenomes to profile planktonic Chlorobia cells from the oxyclines of 42 freshwater bodies, spanning subarctic to tropical regions and encompassing all four seasons. We assembled and compiled over 500 genomes, including metagenome-assembled genomes (MAGs), single-amplified genomes (SAGs), and reference genomes from cultures, clustering them into 71 metagenomic operational taxonomic units (mOTUs or “species”). Of the 71 mOTUs, 57 were classified within the genus Chlorobium, and these mOTUs represented up to ∼60% of the microbial communities in the sampled anoxic waters. Several Chlorobium-associated mOTUs were globally distributed, whereas others were endemic to individual lakes. Although most clades encoded the ability to oxidize hydrogen, many lacked genes for the oxidation of specific sulfur and iron substrates. Surprisingly, one globally distributed Scandinavian clade encoded the ability to oxidize hydrogen, sulfur, and iron, suggesting that metabolic versatility facilitated such widespread colonization. Overall, these findings provide new insight into the biogeography of the Chlorobia and the metabolic traits that facilitate niche specialization within lake ecosystems. IMPORTANCE The reconstruction of genomes from metagenomes has helped explore the ecology and evolution of environmental microbiota. We applied this approach to 274 metagenomes collected from diverse freshwater habitats that spanned oxic and anoxic zones, sampling seasons, and latitudes. We demonstrate widespread and abundant distributions of planktonic Chlorobia-associated bacteria in hypolimnetic waters of stratified freshwater ecosystems and show they vary in their capacities to use different electron donors. Having photoautotrophic potential, these Chlorobia members could serve as carbon sources that support metalimnetic and hypolimnetic food webs.
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spelling pubmed-81250762021-06-09 Freshwater Chlorobia Exhibit Metabolic Specialization among Cosmopolitan and Endemic Populations Garcia, Sarahi L. Mehrshad, Maliheh Buck, Moritz Tsuji, Jackson M. Neufeld, Josh D. McMahon, Katherine D. Bertilsson, Stefan Greening, Chris Peura, Sari mSystems Research Article Photosynthetic bacteria from the class Chlorobia (formerly phylum Chlorobi) sustain carbon fixation in anoxic water columns. They harvest light at extremely low intensities and use various inorganic electron donors to fix carbon dioxide into biomass. Until now, most information on the functional ecology and local adaptations of Chlorobia members came from isolates and merely 26 sequenced genomes that may not adequately represent natural populations. To address these limitations, we analyzed global metagenomes to profile planktonic Chlorobia cells from the oxyclines of 42 freshwater bodies, spanning subarctic to tropical regions and encompassing all four seasons. We assembled and compiled over 500 genomes, including metagenome-assembled genomes (MAGs), single-amplified genomes (SAGs), and reference genomes from cultures, clustering them into 71 metagenomic operational taxonomic units (mOTUs or “species”). Of the 71 mOTUs, 57 were classified within the genus Chlorobium, and these mOTUs represented up to ∼60% of the microbial communities in the sampled anoxic waters. Several Chlorobium-associated mOTUs were globally distributed, whereas others were endemic to individual lakes. Although most clades encoded the ability to oxidize hydrogen, many lacked genes for the oxidation of specific sulfur and iron substrates. Surprisingly, one globally distributed Scandinavian clade encoded the ability to oxidize hydrogen, sulfur, and iron, suggesting that metabolic versatility facilitated such widespread colonization. Overall, these findings provide new insight into the biogeography of the Chlorobia and the metabolic traits that facilitate niche specialization within lake ecosystems. IMPORTANCE The reconstruction of genomes from metagenomes has helped explore the ecology and evolution of environmental microbiota. We applied this approach to 274 metagenomes collected from diverse freshwater habitats that spanned oxic and anoxic zones, sampling seasons, and latitudes. We demonstrate widespread and abundant distributions of planktonic Chlorobia-associated bacteria in hypolimnetic waters of stratified freshwater ecosystems and show they vary in their capacities to use different electron donors. Having photoautotrophic potential, these Chlorobia members could serve as carbon sources that support metalimnetic and hypolimnetic food webs. American Society for Microbiology 2021-05-11 /pmc/articles/PMC8125076/ /pubmed/33975970 http://dx.doi.org/10.1128/mSystems.01196-20 Text en Copyright © 2021 Garcia 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
Garcia, Sarahi L.
Mehrshad, Maliheh
Buck, Moritz
Tsuji, Jackson M.
Neufeld, Josh D.
McMahon, Katherine D.
Bertilsson, Stefan
Greening, Chris
Peura, Sari
Freshwater Chlorobia Exhibit Metabolic Specialization among Cosmopolitan and Endemic Populations
title Freshwater Chlorobia Exhibit Metabolic Specialization among Cosmopolitan and Endemic Populations
title_full Freshwater Chlorobia Exhibit Metabolic Specialization among Cosmopolitan and Endemic Populations
title_fullStr Freshwater Chlorobia Exhibit Metabolic Specialization among Cosmopolitan and Endemic Populations
title_full_unstemmed Freshwater Chlorobia Exhibit Metabolic Specialization among Cosmopolitan and Endemic Populations
title_short Freshwater Chlorobia Exhibit Metabolic Specialization among Cosmopolitan and Endemic Populations
title_sort freshwater chlorobia exhibit metabolic specialization among cosmopolitan and endemic populations
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8125076/
https://www.ncbi.nlm.nih.gov/pubmed/33975970
http://dx.doi.org/10.1128/mSystems.01196-20
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