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Microbial Ecology of Sulfur Biogeochemical Cycling at a Mesothermal Hot Spring Atop Northern Himalayas, India

Sulfur related prokaryotes residing in hot spring present good opportunity for exploring the limitless possibilities of integral ecosystem processes. Metagenomic analysis further expands the phylogenetic breadth of these extraordinary sulfur (S) metabolizing microorganisms as well as their complex m...

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Autores principales: Nagar, Shekhar, Talwar, Chandni, Motelica-Heino, Mikael, Richnow, Hans-Hermann, Shakarad, Mallikarjun, Lal, Rup, Negi, Ram Krishan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9044081/
https://www.ncbi.nlm.nih.gov/pubmed/35495730
http://dx.doi.org/10.3389/fmicb.2022.848010
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author Nagar, Shekhar
Talwar, Chandni
Motelica-Heino, Mikael
Richnow, Hans-Hermann
Shakarad, Mallikarjun
Lal, Rup
Negi, Ram Krishan
author_facet Nagar, Shekhar
Talwar, Chandni
Motelica-Heino, Mikael
Richnow, Hans-Hermann
Shakarad, Mallikarjun
Lal, Rup
Negi, Ram Krishan
author_sort Nagar, Shekhar
collection PubMed
description Sulfur related prokaryotes residing in hot spring present good opportunity for exploring the limitless possibilities of integral ecosystem processes. Metagenomic analysis further expands the phylogenetic breadth of these extraordinary sulfur (S) metabolizing microorganisms as well as their complex metabolic networks and syntrophic interactions in environmental biosystems. Through this study, we explored and expanded the microbial genetic repertoire with focus on S cycling genes through metagenomic analysis of S contaminated hot spring, located at the Northern Himalayas. The analysis revealed rich diversity of microbial consortia with established roles in S cycling such as Pseudomonas, Thioalkalivibrio, Desulfovibrio, and Desulfobulbaceae (Proteobacteria). The major gene families inferred to be abundant across microbial mat, sediment, and water were assigned to Proteobacteria as reflected from the reads per kilobase (RPKs) categorized into translation and ribosomal structure and biogenesis. An analysis of sequence similarity showed conserved pattern of both dsrAB genes (n = 178) retrieved from all metagenomes while other S disproportionation proteins were diverged due to different structural and chemical substrates. The diversity of S oxidizing bacteria (SOB) and sulfate reducing bacteria (SRB) with conserved (r)dsrAB suggests for it to be an important adaptation for microbial fitness at this site. Here, (i) the oxidative and reductive dsr evolutionary time–scale phylogeny proved that the earliest (but not the first) dsrAB proteins belong to anaerobic Thiobacillus with other (rdsr) oxidizers, also we confirm that (ii) SRBs belongs to δ-Proteobacteria occurring independent lateral gene transfer (LGT) of dsr genes to different and few novel lineages. Further, the structural prediction of unassigned DsrAB proteins confirmed their relatedness with species of Desulfovibrio (TM score = 0.86, 0.98, 0.96) and Archaeoglobus fulgidus (TM score = 0.97, 0.98). We proposed that the genetic repertoire might provide the basis of studying time–scale evolution and horizontal gene transfer of these genes in biogeochemical S cycling.
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spelling pubmed-90440812022-04-28 Microbial Ecology of Sulfur Biogeochemical Cycling at a Mesothermal Hot Spring Atop Northern Himalayas, India Nagar, Shekhar Talwar, Chandni Motelica-Heino, Mikael Richnow, Hans-Hermann Shakarad, Mallikarjun Lal, Rup Negi, Ram Krishan Front Microbiol Microbiology Sulfur related prokaryotes residing in hot spring present good opportunity for exploring the limitless possibilities of integral ecosystem processes. Metagenomic analysis further expands the phylogenetic breadth of these extraordinary sulfur (S) metabolizing microorganisms as well as their complex metabolic networks and syntrophic interactions in environmental biosystems. Through this study, we explored and expanded the microbial genetic repertoire with focus on S cycling genes through metagenomic analysis of S contaminated hot spring, located at the Northern Himalayas. The analysis revealed rich diversity of microbial consortia with established roles in S cycling such as Pseudomonas, Thioalkalivibrio, Desulfovibrio, and Desulfobulbaceae (Proteobacteria). The major gene families inferred to be abundant across microbial mat, sediment, and water were assigned to Proteobacteria as reflected from the reads per kilobase (RPKs) categorized into translation and ribosomal structure and biogenesis. An analysis of sequence similarity showed conserved pattern of both dsrAB genes (n = 178) retrieved from all metagenomes while other S disproportionation proteins were diverged due to different structural and chemical substrates. The diversity of S oxidizing bacteria (SOB) and sulfate reducing bacteria (SRB) with conserved (r)dsrAB suggests for it to be an important adaptation for microbial fitness at this site. Here, (i) the oxidative and reductive dsr evolutionary time–scale phylogeny proved that the earliest (but not the first) dsrAB proteins belong to anaerobic Thiobacillus with other (rdsr) oxidizers, also we confirm that (ii) SRBs belongs to δ-Proteobacteria occurring independent lateral gene transfer (LGT) of dsr genes to different and few novel lineages. Further, the structural prediction of unassigned DsrAB proteins confirmed their relatedness with species of Desulfovibrio (TM score = 0.86, 0.98, 0.96) and Archaeoglobus fulgidus (TM score = 0.97, 0.98). We proposed that the genetic repertoire might provide the basis of studying time–scale evolution and horizontal gene transfer of these genes in biogeochemical S cycling. Frontiers Media S.A. 2022-04-13 /pmc/articles/PMC9044081/ /pubmed/35495730 http://dx.doi.org/10.3389/fmicb.2022.848010 Text en Copyright © 2022 Nagar, Talwar, Motelica-Heino, Richnow, Shakarad, Lal and Negi. https://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) and the copyright owner(s) 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
Nagar, Shekhar
Talwar, Chandni
Motelica-Heino, Mikael
Richnow, Hans-Hermann
Shakarad, Mallikarjun
Lal, Rup
Negi, Ram Krishan
Microbial Ecology of Sulfur Biogeochemical Cycling at a Mesothermal Hot Spring Atop Northern Himalayas, India
title Microbial Ecology of Sulfur Biogeochemical Cycling at a Mesothermal Hot Spring Atop Northern Himalayas, India
title_full Microbial Ecology of Sulfur Biogeochemical Cycling at a Mesothermal Hot Spring Atop Northern Himalayas, India
title_fullStr Microbial Ecology of Sulfur Biogeochemical Cycling at a Mesothermal Hot Spring Atop Northern Himalayas, India
title_full_unstemmed Microbial Ecology of Sulfur Biogeochemical Cycling at a Mesothermal Hot Spring Atop Northern Himalayas, India
title_short Microbial Ecology of Sulfur Biogeochemical Cycling at a Mesothermal Hot Spring Atop Northern Himalayas, India
title_sort microbial ecology of sulfur biogeochemical cycling at a mesothermal hot spring atop northern himalayas, india
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9044081/
https://www.ncbi.nlm.nih.gov/pubmed/35495730
http://dx.doi.org/10.3389/fmicb.2022.848010
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