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Novel Large Sulfur Bacteria in the Metagenomes of Groundwater-Fed Chemosynthetic Microbial Mats in the Lake Huron Basin

Little is known about large sulfur bacteria (LSB) that inhabit sulfidic groundwater seeps in large lakes. To examine how geochemically relevant microbial metabolisms are partitioned among community members, we conducted metagenomic analysis of a chemosynthetic microbial mat in the Isolated Sinkhole,...

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Autores principales: Sharrar, Allison M., Flood, Beverly E., Bailey, Jake V., Jones, Daniel S., Biddanda, Bopaiah A., Ruberg, Steven A., Marcus, Daniel N., Dick, Gregory J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5421297/
https://www.ncbi.nlm.nih.gov/pubmed/28533768
http://dx.doi.org/10.3389/fmicb.2017.00791
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author Sharrar, Allison M.
Flood, Beverly E.
Bailey, Jake V.
Jones, Daniel S.
Biddanda, Bopaiah A.
Ruberg, Steven A.
Marcus, Daniel N.
Dick, Gregory J.
author_facet Sharrar, Allison M.
Flood, Beverly E.
Bailey, Jake V.
Jones, Daniel S.
Biddanda, Bopaiah A.
Ruberg, Steven A.
Marcus, Daniel N.
Dick, Gregory J.
author_sort Sharrar, Allison M.
collection PubMed
description Little is known about large sulfur bacteria (LSB) that inhabit sulfidic groundwater seeps in large lakes. To examine how geochemically relevant microbial metabolisms are partitioned among community members, we conducted metagenomic analysis of a chemosynthetic microbial mat in the Isolated Sinkhole, which is in a deep, aphotic environment of Lake Huron. For comparison, we also analyzed a white mat in an artesian fountain that is fed by groundwater similar to Isolated Sinkhole, but that sits in shallow water and is exposed to sunlight. De novo assembly and binning of metagenomic data from these two communities yielded near complete genomes and revealed representatives of two families of LSB. The Isolated Sinkhole community was dominated by novel members of the Beggiatoaceae that are phylogenetically intermediate between known freshwater and marine groups. Several of these Beggiatoaceae had 16S rRNA genes that contained introns previously observed only in marine taxa. The Alpena fountain was dominated by populations closely related to Thiothrix lacustris and an SM1 euryarchaeon known to live symbiotically with Thiothrix spp. The SM1 genomic bin contained evidence of H(2)-based lithoautotrophy. Genomic bins of both the Thiothrix and Beggiatoaceae contained genes for sulfur oxidation via the rDsr pathway, H(2) oxidation via Ni-Fe hydrogenases, and the use of O(2) and nitrate as electron acceptors. Mats at both sites also contained Deltaproteobacteria with genes for dissimilatory sulfate reduction (sat, apr, and dsr) and hydrogen oxidation (Ni-Fe hydrogenases). Overall, the microbial mats at the two sites held low-diversity microbial communities, displayed evidence of coupled sulfur cycling, and did not differ largely in their metabolic potentials, despite the environmental differences. These results show that groundwater-fed communities in an artesian fountain and in submerged sinkholes of Lake Huron are a rich source of novel LSB, associated heterotrophic and sulfate-reducing bacteria, and archaea.
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spelling pubmed-54212972017-05-22 Novel Large Sulfur Bacteria in the Metagenomes of Groundwater-Fed Chemosynthetic Microbial Mats in the Lake Huron Basin Sharrar, Allison M. Flood, Beverly E. Bailey, Jake V. Jones, Daniel S. Biddanda, Bopaiah A. Ruberg, Steven A. Marcus, Daniel N. Dick, Gregory J. Front Microbiol Microbiology Little is known about large sulfur bacteria (LSB) that inhabit sulfidic groundwater seeps in large lakes. To examine how geochemically relevant microbial metabolisms are partitioned among community members, we conducted metagenomic analysis of a chemosynthetic microbial mat in the Isolated Sinkhole, which is in a deep, aphotic environment of Lake Huron. For comparison, we also analyzed a white mat in an artesian fountain that is fed by groundwater similar to Isolated Sinkhole, but that sits in shallow water and is exposed to sunlight. De novo assembly and binning of metagenomic data from these two communities yielded near complete genomes and revealed representatives of two families of LSB. The Isolated Sinkhole community was dominated by novel members of the Beggiatoaceae that are phylogenetically intermediate between known freshwater and marine groups. Several of these Beggiatoaceae had 16S rRNA genes that contained introns previously observed only in marine taxa. The Alpena fountain was dominated by populations closely related to Thiothrix lacustris and an SM1 euryarchaeon known to live symbiotically with Thiothrix spp. The SM1 genomic bin contained evidence of H(2)-based lithoautotrophy. Genomic bins of both the Thiothrix and Beggiatoaceae contained genes for sulfur oxidation via the rDsr pathway, H(2) oxidation via Ni-Fe hydrogenases, and the use of O(2) and nitrate as electron acceptors. Mats at both sites also contained Deltaproteobacteria with genes for dissimilatory sulfate reduction (sat, apr, and dsr) and hydrogen oxidation (Ni-Fe hydrogenases). Overall, the microbial mats at the two sites held low-diversity microbial communities, displayed evidence of coupled sulfur cycling, and did not differ largely in their metabolic potentials, despite the environmental differences. These results show that groundwater-fed communities in an artesian fountain and in submerged sinkholes of Lake Huron are a rich source of novel LSB, associated heterotrophic and sulfate-reducing bacteria, and archaea. Frontiers Media S.A. 2017-05-08 /pmc/articles/PMC5421297/ /pubmed/28533768 http://dx.doi.org/10.3389/fmicb.2017.00791 Text en Copyright © 2017 Sharrar, Flood, Bailey, Jones, Biddanda, Ruberg, Marcus and Dick. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Sharrar, Allison M.
Flood, Beverly E.
Bailey, Jake V.
Jones, Daniel S.
Biddanda, Bopaiah A.
Ruberg, Steven A.
Marcus, Daniel N.
Dick, Gregory J.
Novel Large Sulfur Bacteria in the Metagenomes of Groundwater-Fed Chemosynthetic Microbial Mats in the Lake Huron Basin
title Novel Large Sulfur Bacteria in the Metagenomes of Groundwater-Fed Chemosynthetic Microbial Mats in the Lake Huron Basin
title_full Novel Large Sulfur Bacteria in the Metagenomes of Groundwater-Fed Chemosynthetic Microbial Mats in the Lake Huron Basin
title_fullStr Novel Large Sulfur Bacteria in the Metagenomes of Groundwater-Fed Chemosynthetic Microbial Mats in the Lake Huron Basin
title_full_unstemmed Novel Large Sulfur Bacteria in the Metagenomes of Groundwater-Fed Chemosynthetic Microbial Mats in the Lake Huron Basin
title_short Novel Large Sulfur Bacteria in the Metagenomes of Groundwater-Fed Chemosynthetic Microbial Mats in the Lake Huron Basin
title_sort novel large sulfur bacteria in the metagenomes of groundwater-fed chemosynthetic microbial mats in the lake huron basin
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5421297/
https://www.ncbi.nlm.nih.gov/pubmed/28533768
http://dx.doi.org/10.3389/fmicb.2017.00791
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