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Omics-Inferred Partitioning and Expression of Diverse Biogeochemical Functions in a Low-O(2) Cyanobacterial Mat Community

Cyanobacterial mats profoundly influenced Earth’s biological and geochemical evolution and still play important ecological roles in the modern world. However, the biogeochemical functioning of cyanobacterial mats under persistent low-O(2) conditions, which dominated their evolutionary history, is no...

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Autores principales: Grim, Sharon L., Voorhies, Alexander A., Biddanda, Bopaiah A., Jain, Sunit, Nold, Stephen C., Green, Russ, Dick, Gregory J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8651085/
https://www.ncbi.nlm.nih.gov/pubmed/34874776
http://dx.doi.org/10.1128/mSystems.01042-21
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author Grim, Sharon L.
Voorhies, Alexander A.
Biddanda, Bopaiah A.
Jain, Sunit
Nold, Stephen C.
Green, Russ
Dick, Gregory J.
author_facet Grim, Sharon L.
Voorhies, Alexander A.
Biddanda, Bopaiah A.
Jain, Sunit
Nold, Stephen C.
Green, Russ
Dick, Gregory J.
author_sort Grim, Sharon L.
collection PubMed
description Cyanobacterial mats profoundly influenced Earth’s biological and geochemical evolution and still play important ecological roles in the modern world. However, the biogeochemical functioning of cyanobacterial mats under persistent low-O(2) conditions, which dominated their evolutionary history, is not well understood. To investigate how different metabolic and biogeochemical functions are partitioned among community members, we conducted metagenomics and metatranscriptomics on cyanobacterial mats in the low-O(2), sulfidic Middle Island sinkhole (MIS) in Lake Huron. Metagenomic assembly and binning yielded 144 draft metagenome assembled genomes, including 61 of medium quality or better, and the dominant cyanobacteria and numerous Proteobacteria involved in sulfur cycling. Strains of a Phormidium autumnale-like cyanobacterium dominated the metagenome and metatranscriptome. Transcripts for the photosynthetic reaction core genes psaA and psbA were abundant in both day and night. Multiple types of psbA genes were expressed from each cyanobacterium, and the dominant psbA transcripts were from an atypical microaerobic type of D1 protein from Phormidium. Further, cyanobacterial transcripts for photosystem I genes were more abundant than those for photosystem II, and two types of Phormidium sulfide quinone reductase were recovered, consistent with anoxygenic photosynthesis via photosystem I in the presence of sulfide. Transcripts indicate active sulfur oxidation and reduction within the cyanobacterial mat, predominately by Gammaproteobacteria and Deltaproteobacteria, respectively. Overall, these genomic and transcriptomic results link specific microbial groups to metabolic processes that underpin primary production and biogeochemical cycling in a low-O(2) cyanobacterial mat and suggest mechanisms for tightly coupled cycling of oxygen and sulfur compounds in the mat ecosystem. IMPORTANCE Cyanobacterial mats are dense communities of microorganisms that contain photosynthetic cyanobacteria along with a host of other bacterial species that play important yet still poorly understood roles in this ecosystem. Although such cyanobacterial mats were critical agents of Earth’s biological and chemical evolution through geological time, little is known about how they function under the low-oxygen conditions that characterized most of their natural history. Here, we performed sequencing of the DNA and RNA of modern cyanobacterial mat communities under low-oxygen and sulfur-rich conditions from the Middle Island sinkhole in Lake Huron. The results reveal the organisms and metabolic pathways that are responsible for both oxygen-producing and non-oxygen-producing photosynthesis as well as interconversions of sulfur that likely shape how much O(2) is produced in such ecosystems. These findings indicate tight metabolic reactions between community members that help to explain the limited the amount of O(2) produced in cyanobacterial mat ecosystems.
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spelling pubmed-86510852021-12-16 Omics-Inferred Partitioning and Expression of Diverse Biogeochemical Functions in a Low-O(2) Cyanobacterial Mat Community Grim, Sharon L. Voorhies, Alexander A. Biddanda, Bopaiah A. Jain, Sunit Nold, Stephen C. Green, Russ Dick, Gregory J. mSystems Research Article Cyanobacterial mats profoundly influenced Earth’s biological and geochemical evolution and still play important ecological roles in the modern world. However, the biogeochemical functioning of cyanobacterial mats under persistent low-O(2) conditions, which dominated their evolutionary history, is not well understood. To investigate how different metabolic and biogeochemical functions are partitioned among community members, we conducted metagenomics and metatranscriptomics on cyanobacterial mats in the low-O(2), sulfidic Middle Island sinkhole (MIS) in Lake Huron. Metagenomic assembly and binning yielded 144 draft metagenome assembled genomes, including 61 of medium quality or better, and the dominant cyanobacteria and numerous Proteobacteria involved in sulfur cycling. Strains of a Phormidium autumnale-like cyanobacterium dominated the metagenome and metatranscriptome. Transcripts for the photosynthetic reaction core genes psaA and psbA were abundant in both day and night. Multiple types of psbA genes were expressed from each cyanobacterium, and the dominant psbA transcripts were from an atypical microaerobic type of D1 protein from Phormidium. Further, cyanobacterial transcripts for photosystem I genes were more abundant than those for photosystem II, and two types of Phormidium sulfide quinone reductase were recovered, consistent with anoxygenic photosynthesis via photosystem I in the presence of sulfide. Transcripts indicate active sulfur oxidation and reduction within the cyanobacterial mat, predominately by Gammaproteobacteria and Deltaproteobacteria, respectively. Overall, these genomic and transcriptomic results link specific microbial groups to metabolic processes that underpin primary production and biogeochemical cycling in a low-O(2) cyanobacterial mat and suggest mechanisms for tightly coupled cycling of oxygen and sulfur compounds in the mat ecosystem. IMPORTANCE Cyanobacterial mats are dense communities of microorganisms that contain photosynthetic cyanobacteria along with a host of other bacterial species that play important yet still poorly understood roles in this ecosystem. Although such cyanobacterial mats were critical agents of Earth’s biological and chemical evolution through geological time, little is known about how they function under the low-oxygen conditions that characterized most of their natural history. Here, we performed sequencing of the DNA and RNA of modern cyanobacterial mat communities under low-oxygen and sulfur-rich conditions from the Middle Island sinkhole in Lake Huron. The results reveal the organisms and metabolic pathways that are responsible for both oxygen-producing and non-oxygen-producing photosynthesis as well as interconversions of sulfur that likely shape how much O(2) is produced in such ecosystems. These findings indicate tight metabolic reactions between community members that help to explain the limited the amount of O(2) produced in cyanobacterial mat ecosystems. American Society for Microbiology 2021-12-07 /pmc/articles/PMC8651085/ /pubmed/34874776 http://dx.doi.org/10.1128/mSystems.01042-21 Text en Copyright © 2021 Grim 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
Grim, Sharon L.
Voorhies, Alexander A.
Biddanda, Bopaiah A.
Jain, Sunit
Nold, Stephen C.
Green, Russ
Dick, Gregory J.
Omics-Inferred Partitioning and Expression of Diverse Biogeochemical Functions in a Low-O(2) Cyanobacterial Mat Community
title Omics-Inferred Partitioning and Expression of Diverse Biogeochemical Functions in a Low-O(2) Cyanobacterial Mat Community
title_full Omics-Inferred Partitioning and Expression of Diverse Biogeochemical Functions in a Low-O(2) Cyanobacterial Mat Community
title_fullStr Omics-Inferred Partitioning and Expression of Diverse Biogeochemical Functions in a Low-O(2) Cyanobacterial Mat Community
title_full_unstemmed Omics-Inferred Partitioning and Expression of Diverse Biogeochemical Functions in a Low-O(2) Cyanobacterial Mat Community
title_short Omics-Inferred Partitioning and Expression of Diverse Biogeochemical Functions in a Low-O(2) Cyanobacterial Mat Community
title_sort omics-inferred partitioning and expression of diverse biogeochemical functions in a low-o(2) cyanobacterial mat community
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8651085/
https://www.ncbi.nlm.nih.gov/pubmed/34874776
http://dx.doi.org/10.1128/mSystems.01042-21
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