Novel Microorganisms Contribute to Biosulfidogenesis in the Deep Layer of an Acidic Pit Lake

Cueva de la Mora is a permanently stratified acidic pit lake with extremely high concentrations of heavy metals at depth. In order to evaluate the potential for in situ sulfide production, we characterized the microbial community in the deep layer using metagenomics and metatranscriptomics. We retri...

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Main Authors: Diana Ayala-Muñoz, William D. Burgos, Javier Sánchez-España, Carmen Falagán, Estelle Couradeau, Jennifer L. Macalady
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-07-01
Series:Frontiers in Bioengineering and Biotechnology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fbioe.2022.867321/full
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author Diana Ayala-Muñoz
William D. Burgos
Javier Sánchez-España
Carmen Falagán
Estelle Couradeau
Jennifer L. Macalady
author_facet Diana Ayala-Muñoz
William D. Burgos
Javier Sánchez-España
Carmen Falagán
Estelle Couradeau
Jennifer L. Macalady
author_sort Diana Ayala-Muñoz
collection DOAJ
description Cueva de la Mora is a permanently stratified acidic pit lake with extremely high concentrations of heavy metals at depth. In order to evaluate the potential for in situ sulfide production, we characterized the microbial community in the deep layer using metagenomics and metatranscriptomics. We retrieved 18 high quality metagenome-assembled genomes (MAGs) representing the most abundant populations. None of the MAGs were closely related to either cultured or non-cultured organisms from the Genome Taxonomy or NCBI databases (none with average nucleotide identity >95%). Despite oxygen concentrations that are consistently below detection in the deep layer, some archaeal and bacterial MAGs mapped transcripts of genes for sulfide oxidation coupled with oxygen reduction. Among these microaerophilic sulfide oxidizers, mixotrophic Thermoplasmatales archaea were the most numerous and represented 24% of the total community. Populations associated with the highest predicted in situ activity for sulfate reduction were affiliated with Actinobacteria, Chloroflexi, and Nitrospirae phyla, and together represented about 9% of the total community. These MAGs, in addition to a less abundant Proteobacteria MAG in the genus Desulfomonile, contained transcripts of genes in the Wood-Ljungdahl pathway. All MAGs had significant genetic potential for organic carbon oxidation. Our results indicate that novel acidophiles are contributing to biosulfidogenesis in the deep layer of Cueva de la Mora, and that in situ sulfide production is limited by organic carbon availability and sulfur oxidation.
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spelling doaj.art-ad5ab34574c34248b3a8662ace6fdc502022-12-22T03:01:54ZengFrontiers Media S.A.Frontiers in Bioengineering and Biotechnology2296-41852022-07-011010.3389/fbioe.2022.867321867321Novel Microorganisms Contribute to Biosulfidogenesis in the Deep Layer of an Acidic Pit LakeDiana Ayala-Muñoz0William D. Burgos1Javier Sánchez-España2Carmen Falagán3Estelle Couradeau4Jennifer L. Macalady5Department of Civil and Environmental Engineering, The Pennsylvania State University, University Park, PA, United StatesDepartment of Civil and Environmental Engineering, The Pennsylvania State University, University Park, PA, United StatesCentro Nacional Instituto Geológico Minero de España (IGME), CSIC, Madrid, SpainSchool of Biological Sciences, University of Portsmouth, Portsmouth, United KingdomDepartment of Ecosystem Science and Management, The Pennsylvania State University, University Park, PA, United StatesDepartment of Geosciences, The Pennsylvania State University, University Park, PA, United StatesCueva de la Mora is a permanently stratified acidic pit lake with extremely high concentrations of heavy metals at depth. In order to evaluate the potential for in situ sulfide production, we characterized the microbial community in the deep layer using metagenomics and metatranscriptomics. We retrieved 18 high quality metagenome-assembled genomes (MAGs) representing the most abundant populations. None of the MAGs were closely related to either cultured or non-cultured organisms from the Genome Taxonomy or NCBI databases (none with average nucleotide identity >95%). Despite oxygen concentrations that are consistently below detection in the deep layer, some archaeal and bacterial MAGs mapped transcripts of genes for sulfide oxidation coupled with oxygen reduction. Among these microaerophilic sulfide oxidizers, mixotrophic Thermoplasmatales archaea were the most numerous and represented 24% of the total community. Populations associated with the highest predicted in situ activity for sulfate reduction were affiliated with Actinobacteria, Chloroflexi, and Nitrospirae phyla, and together represented about 9% of the total community. These MAGs, in addition to a less abundant Proteobacteria MAG in the genus Desulfomonile, contained transcripts of genes in the Wood-Ljungdahl pathway. All MAGs had significant genetic potential for organic carbon oxidation. Our results indicate that novel acidophiles are contributing to biosulfidogenesis in the deep layer of Cueva de la Mora, and that in situ sulfide production is limited by organic carbon availability and sulfur oxidation.https://www.frontiersin.org/articles/10.3389/fbioe.2022.867321/fullbiosulfidogenesisacidic pit lakemetagenomicsmetatranscriptomicsmetagenome-assembled genomes (MAGs)acidophiles
spellingShingle Diana Ayala-Muñoz
William D. Burgos
Javier Sánchez-España
Carmen Falagán
Estelle Couradeau
Jennifer L. Macalady
Novel Microorganisms Contribute to Biosulfidogenesis in the Deep Layer of an Acidic Pit Lake
Frontiers in Bioengineering and Biotechnology
biosulfidogenesis
acidic pit lake
metagenomics
metatranscriptomics
metagenome-assembled genomes (MAGs)
acidophiles
title Novel Microorganisms Contribute to Biosulfidogenesis in the Deep Layer of an Acidic Pit Lake
title_full Novel Microorganisms Contribute to Biosulfidogenesis in the Deep Layer of an Acidic Pit Lake
title_fullStr Novel Microorganisms Contribute to Biosulfidogenesis in the Deep Layer of an Acidic Pit Lake
title_full_unstemmed Novel Microorganisms Contribute to Biosulfidogenesis in the Deep Layer of an Acidic Pit Lake
title_short Novel Microorganisms Contribute to Biosulfidogenesis in the Deep Layer of an Acidic Pit Lake
title_sort novel microorganisms contribute to biosulfidogenesis in the deep layer of an acidic pit lake
topic biosulfidogenesis
acidic pit lake
metagenomics
metatranscriptomics
metagenome-assembled genomes (MAGs)
acidophiles
url https://www.frontiersin.org/articles/10.3389/fbioe.2022.867321/full
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