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Freshwater Chlorobia Exhibit Metabolic Specialization among Cosmopolitan and Endemic Populations
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Limnology. Stockholm Univ, Dept Ecol Environm & Plant Sci, Sci Life Lab, Stockholm, Sweden.ORCID iD: 0000-0002-8622-0308
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Limnology. Swedish Univ Agr Sci, Dept Aquat Sci & Assessment, Uppsala, Sweden.ORCID iD: 0000-0002-1108-6888
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Limnology. Swedish Univ Agr Sci, Dept Aquat Sci & Assessment, Uppsala, Sweden.ORCID iD: 0000-0001-6632-5324
Univ Waterloo, Dept Biol, Waterloo, ON, Canada.ORCID iD: 0000-0001-7244-4709
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2021 (English)In: mSystems, E-ISSN 2379-5077, Vol. 6, no 3, article id e01196-20Article in journal (Refereed) Published
Abstract [en]

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.

Place, publisher, year, edition, pages
American Society for Microbiology American Society for Microbiology, 2021. Vol. 6, no 3, article id e01196-20
Keywords [en]
Chlorobia, freshwater, photosynthetic bacteria, planktonic
National Category
Microbiology
Identifiers
URN: urn:nbn:se:uu:diva-458706DOI: 10.1128/mSystems.01196-20ISI: 000709811800011PubMedID: 33975970OAI: oai:DiVA.org:uu-458706DiVA, id: diva2:1614506
Funder
Knut and Alice Wallenberg Foundation, KAW 2013.0091Swedish Research CouncilSwedish Research Council FormasSwedish National Infrastructure for Computing (SNIC), SNIC2020/5-19Science for Life Laboratory, SciLifeLabThe Royal Swedish Academy of SciencesAvailable from: 2021-11-25 Created: 2021-11-25 Last updated: 2024-01-15Bibliographically approved

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Garcia, Sarahi L.Mehrshad, MalihehBuck, MoritzBertilsson, Stefan

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