Shedding Light on Microbial “Dark Matter”: Insights Into Novel Cloacimonadota and Omnitrophota From an Antarctic Lake

The potential metabolism and ecological roles of many microbial taxa remain unknown because insufficient genomic data are available to assess their functional potential. Two such microbial “dark matter” taxa are the Candidatus bacterial phyla Cloacimonadota and Omnitrophota, both of which have been...

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Published in:Frontiers in Microbiology
Main Authors: Timothy J. Williams, Michelle A. Allen, Jonathan F. Berengut, Ricardo Cavicchioli
Format: Article in Journal/Newspaper
Language:English
Published: Frontiers Media S.A. 2021
Subjects:
Online Access:https://doi.org/10.3389/fmicb.2021.741077
https://doaj.org/article/39be4e0b2efa40a89bc8e7f8fb78358b
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spelling ftdoajarticles:oai:doaj.org/article:39be4e0b2efa40a89bc8e7f8fb78358b 2023-05-15T13:37:01+02:00 Shedding Light on Microbial “Dark Matter”: Insights Into Novel Cloacimonadota and Omnitrophota From an Antarctic Lake Timothy J. Williams Michelle A. Allen Jonathan F. Berengut Ricardo Cavicchioli 2021-10-01T00:00:00Z https://doi.org/10.3389/fmicb.2021.741077 https://doaj.org/article/39be4e0b2efa40a89bc8e7f8fb78358b EN eng Frontiers Media S.A. https://www.frontiersin.org/articles/10.3389/fmicb.2021.741077/full https://doaj.org/toc/1664-302X 1664-302X doi:10.3389/fmicb.2021.741077 https://doaj.org/article/39be4e0b2efa40a89bc8e7f8fb78358b Frontiers in Microbiology, Vol 12 (2021) Cloacimonadota Omnitrophota cellulosome autotrophy metagenome Antarctic bacteria Microbiology QR1-502 article 2021 ftdoajarticles https://doi.org/10.3389/fmicb.2021.741077 2022-12-31T12:56:17Z The potential metabolism and ecological roles of many microbial taxa remain unknown because insufficient genomic data are available to assess their functional potential. Two such microbial “dark matter” taxa are the Candidatus bacterial phyla Cloacimonadota and Omnitrophota, both of which have been identified in global anoxic environments, including (but not limited to) organic-carbon-rich lakes. Using 24 metagenome-assembled genomes (MAGs) obtained from an Antarctic lake (Ace Lake, Vestfold Hills), novel lineages and novel metabolic traits were identified for both phyla. The Cloacimonadota MAGs exhibited a capacity for carbon fixation using the reverse tricarboxylic acid cycle driven by oxidation of hydrogen and sulfur. Certain Cloacimonadota MAGs encoded proteins that possess dockerin and cohesin domains, which is consistent with the assembly of extracellular cellulosome-like structures that are used for degradation of polypeptides and polysaccharides. The Omnitrophota MAGs represented phylogenetically diverse taxa that were predicted to possess a strong biosynthetic capacity for amino acids, nucleosides, fatty acids, and essential cofactors. All of the Omnitrophota were inferred to be obligate fermentative heterotrophs that utilize a relatively narrow range of organic compounds, have an incomplete tricarboxylic acid cycle, and possess a single hydrogenase gene important for achieving redox balance in the cell. We reason that both Cloacimonadota and Omnitrophota form metabolic interactions with hydrogen-consuming partners (methanogens and Desulfobacterota, respectively) and, therefore, occupy specific niches in Ace Lake. Article in Journal/Newspaper Antarc* Antarctic Directory of Open Access Journals: DOAJ Articles Antarctic Vestfold Hills Vestfold Ace Lake ENVELOPE(78.188,78.188,-68.472,-68.472) Frontiers in Microbiology 12
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic Cloacimonadota
Omnitrophota
cellulosome
autotrophy
metagenome
Antarctic bacteria
Microbiology
QR1-502
spellingShingle Cloacimonadota
Omnitrophota
cellulosome
autotrophy
metagenome
Antarctic bacteria
Microbiology
QR1-502
Timothy J. Williams
Michelle A. Allen
Jonathan F. Berengut
Ricardo Cavicchioli
Shedding Light on Microbial “Dark Matter”: Insights Into Novel Cloacimonadota and Omnitrophota From an Antarctic Lake
topic_facet Cloacimonadota
Omnitrophota
cellulosome
autotrophy
metagenome
Antarctic bacteria
Microbiology
QR1-502
description The potential metabolism and ecological roles of many microbial taxa remain unknown because insufficient genomic data are available to assess their functional potential. Two such microbial “dark matter” taxa are the Candidatus bacterial phyla Cloacimonadota and Omnitrophota, both of which have been identified in global anoxic environments, including (but not limited to) organic-carbon-rich lakes. Using 24 metagenome-assembled genomes (MAGs) obtained from an Antarctic lake (Ace Lake, Vestfold Hills), novel lineages and novel metabolic traits were identified for both phyla. The Cloacimonadota MAGs exhibited a capacity for carbon fixation using the reverse tricarboxylic acid cycle driven by oxidation of hydrogen and sulfur. Certain Cloacimonadota MAGs encoded proteins that possess dockerin and cohesin domains, which is consistent with the assembly of extracellular cellulosome-like structures that are used for degradation of polypeptides and polysaccharides. The Omnitrophota MAGs represented phylogenetically diverse taxa that were predicted to possess a strong biosynthetic capacity for amino acids, nucleosides, fatty acids, and essential cofactors. All of the Omnitrophota were inferred to be obligate fermentative heterotrophs that utilize a relatively narrow range of organic compounds, have an incomplete tricarboxylic acid cycle, and possess a single hydrogenase gene important for achieving redox balance in the cell. We reason that both Cloacimonadota and Omnitrophota form metabolic interactions with hydrogen-consuming partners (methanogens and Desulfobacterota, respectively) and, therefore, occupy specific niches in Ace Lake.
format Article in Journal/Newspaper
author Timothy J. Williams
Michelle A. Allen
Jonathan F. Berengut
Ricardo Cavicchioli
author_facet Timothy J. Williams
Michelle A. Allen
Jonathan F. Berengut
Ricardo Cavicchioli
author_sort Timothy J. Williams
title Shedding Light on Microbial “Dark Matter”: Insights Into Novel Cloacimonadota and Omnitrophota From an Antarctic Lake
title_short Shedding Light on Microbial “Dark Matter”: Insights Into Novel Cloacimonadota and Omnitrophota From an Antarctic Lake
title_full Shedding Light on Microbial “Dark Matter”: Insights Into Novel Cloacimonadota and Omnitrophota From an Antarctic Lake
title_fullStr Shedding Light on Microbial “Dark Matter”: Insights Into Novel Cloacimonadota and Omnitrophota From an Antarctic Lake
title_full_unstemmed Shedding Light on Microbial “Dark Matter”: Insights Into Novel Cloacimonadota and Omnitrophota From an Antarctic Lake
title_sort shedding light on microbial “dark matter”: insights into novel cloacimonadota and omnitrophota from an antarctic lake
publisher Frontiers Media S.A.
publishDate 2021
url https://doi.org/10.3389/fmicb.2021.741077
https://doaj.org/article/39be4e0b2efa40a89bc8e7f8fb78358b
long_lat ENVELOPE(78.188,78.188,-68.472,-68.472)
geographic Antarctic
Vestfold Hills
Vestfold
Ace Lake
geographic_facet Antarctic
Vestfold Hills
Vestfold
Ace Lake
genre Antarc*
Antarctic
genre_facet Antarc*
Antarctic
op_source Frontiers in Microbiology, Vol 12 (2021)
op_relation https://www.frontiersin.org/articles/10.3389/fmicb.2021.741077/full
https://doaj.org/toc/1664-302X
1664-302X
doi:10.3389/fmicb.2021.741077
https://doaj.org/article/39be4e0b2efa40a89bc8e7f8fb78358b
op_doi https://doi.org/10.3389/fmicb.2021.741077
container_title Frontiers in Microbiology
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