Expanded Phylogenetic Diversity and Metabolic Flexibility of Mercury-Methylating Microorganisms

ABSTRACT Methylmercury is a potent bioaccumulating neurotoxin that is produced by specific microorganisms that methylate inorganic mercury. Methylmercury production in diverse anaerobic bacteria and archaea was recently linked to the hgcAB genes. However, the full phylogenetic and metabolic diversit...

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Autores principales:	Elizabeth A. McDaniel, Benjamin D. Peterson, Sarah L. R. Stevens, Patricia Q. Tran, Karthik Anantharaman, Katherine D. McMahon
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	genomics mercury metagenomics methylmercury Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/f2c904d0a6d1450a9967aabef43ad877
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spelling	oai:doaj.org-article:f2c904d0a6d1450a9967aabef43ad8772021-12-02T19:47:35ZExpanded Phylogenetic Diversity and Metabolic Flexibility of Mercury-Methylating Microorganisms10.1128/mSystems.00299-202379-5077https://doaj.org/article/f2c904d0a6d1450a9967aabef43ad8772020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00299-20https://doaj.org/toc/2379-5077ABSTRACT Methylmercury is a potent bioaccumulating neurotoxin that is produced by specific microorganisms that methylate inorganic mercury. Methylmercury production in diverse anaerobic bacteria and archaea was recently linked to the hgcAB genes. However, the full phylogenetic and metabolic diversity of mercury-methylating microorganisms has not been fully unraveled due to the limited number of cultured experimentally verified methylators and the limitations of primer-based molecular methods. Here, we describe the phylogenetic diversity and metabolic flexibility of putative mercury-methylating microorganisms by hgcAB identification in publicly available isolate genomes and metagenome-assembled genomes (MAGs) as well as novel freshwater MAGs. We demonstrate that putative mercury methylators are much more phylogenetically diverse than previously known and that hgcAB distribution among genomes is most likely due to several independent horizontal gene transfer events. The microorganisms we identified possess diverse metabolic capabilities spanning carbon fixation, sulfate reduction, nitrogen fixation, and metal resistance pathways. We identified 111 putative mercury methylators in a set of previously published permafrost metatranscriptomes and demonstrated that different methylating taxa may contribute to hgcA expression at different depths. Overall, we provide a framework for illuminating the microbial basis of mercury methylation using genome-resolved metagenomics and metatranscriptomics to identify putative methylators based upon hgcAB presence and describe their putative functions in the environment. IMPORTANCE Accurately assessing the production of bioaccumulative neurotoxic methylmercury by characterizing the phylogenetic diversity, metabolic functions, and activity of methylators in the environment is crucial for understanding constraints on the mercury cycle. Much of our understanding of methylmercury production is based on cultured anaerobic microorganisms within the Deltaproteobacteria, Firmicutes, and Euryarchaeota. Advances in next-generation sequencing technologies have enabled large-scale cultivation-independent surveys of diverse and poorly characterized microorganisms from numerous ecosystems. We used genome-resolved metagenomics and metatranscriptomics to highlight the vast phylogenetic and metabolic diversity of putative mercury methylators and their depth-discrete activities in thawing permafrost. This work underscores the importance of using genome-resolved metagenomics to survey specific putative methylating populations of a given mercury-impacted ecosystem.Elizabeth A. McDanielBenjamin D. PetersonSarah L. R. StevensPatricia Q. TranKarthik AnantharamanKatherine D. McMahonAmerican Society for MicrobiologyarticlegenomicsmercurymetagenomicsmethylmercuryMicrobiologyQR1-502ENmSystems, Vol 5, Iss 4 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	genomics mercury metagenomics methylmercury Microbiology QR1-502
spellingShingle	genomics mercury metagenomics methylmercury Microbiology QR1-502 Elizabeth A. McDaniel Benjamin D. Peterson Sarah L. R. Stevens Patricia Q. Tran Karthik Anantharaman Katherine D. McMahon Expanded Phylogenetic Diversity and Metabolic Flexibility of Mercury-Methylating Microorganisms
description	ABSTRACT Methylmercury is a potent bioaccumulating neurotoxin that is produced by specific microorganisms that methylate inorganic mercury. Methylmercury production in diverse anaerobic bacteria and archaea was recently linked to the hgcAB genes. However, the full phylogenetic and metabolic diversity of mercury-methylating microorganisms has not been fully unraveled due to the limited number of cultured experimentally verified methylators and the limitations of primer-based molecular methods. Here, we describe the phylogenetic diversity and metabolic flexibility of putative mercury-methylating microorganisms by hgcAB identification in publicly available isolate genomes and metagenome-assembled genomes (MAGs) as well as novel freshwater MAGs. We demonstrate that putative mercury methylators are much more phylogenetically diverse than previously known and that hgcAB distribution among genomes is most likely due to several independent horizontal gene transfer events. The microorganisms we identified possess diverse metabolic capabilities spanning carbon fixation, sulfate reduction, nitrogen fixation, and metal resistance pathways. We identified 111 putative mercury methylators in a set of previously published permafrost metatranscriptomes and demonstrated that different methylating taxa may contribute to hgcA expression at different depths. Overall, we provide a framework for illuminating the microbial basis of mercury methylation using genome-resolved metagenomics and metatranscriptomics to identify putative methylators based upon hgcAB presence and describe their putative functions in the environment. IMPORTANCE Accurately assessing the production of bioaccumulative neurotoxic methylmercury by characterizing the phylogenetic diversity, metabolic functions, and activity of methylators in the environment is crucial for understanding constraints on the mercury cycle. Much of our understanding of methylmercury production is based on cultured anaerobic microorganisms within the Deltaproteobacteria, Firmicutes, and Euryarchaeota. Advances in next-generation sequencing technologies have enabled large-scale cultivation-independent surveys of diverse and poorly characterized microorganisms from numerous ecosystems. We used genome-resolved metagenomics and metatranscriptomics to highlight the vast phylogenetic and metabolic diversity of putative mercury methylators and their depth-discrete activities in thawing permafrost. This work underscores the importance of using genome-resolved metagenomics to survey specific putative methylating populations of a given mercury-impacted ecosystem.
format	article
author	Elizabeth A. McDaniel Benjamin D. Peterson Sarah L. R. Stevens Patricia Q. Tran Karthik Anantharaman Katherine D. McMahon
author_facet	Elizabeth A. McDaniel Benjamin D. Peterson Sarah L. R. Stevens Patricia Q. Tran Karthik Anantharaman Katherine D. McMahon
author_sort	Elizabeth A. McDaniel
title	Expanded Phylogenetic Diversity and Metabolic Flexibility of Mercury-Methylating Microorganisms
title_short	Expanded Phylogenetic Diversity and Metabolic Flexibility of Mercury-Methylating Microorganisms
title_full	Expanded Phylogenetic Diversity and Metabolic Flexibility of Mercury-Methylating Microorganisms
title_fullStr	Expanded Phylogenetic Diversity and Metabolic Flexibility of Mercury-Methylating Microorganisms
title_full_unstemmed	Expanded Phylogenetic Diversity and Metabolic Flexibility of Mercury-Methylating Microorganisms
title_sort	expanded phylogenetic diversity and metabolic flexibility of mercury-methylating microorganisms
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/f2c904d0a6d1450a9967aabef43ad877
work_keys_str_mv	AT elizabethamcdaniel expandedphylogeneticdiversityandmetabolicflexibilityofmercurymethylatingmicroorganisms AT benjamindpeterson expandedphylogeneticdiversityandmetabolicflexibilityofmercurymethylatingmicroorganisms AT sarahlrstevens expandedphylogeneticdiversityandmetabolicflexibilityofmercurymethylatingmicroorganisms AT patriciaqtran expandedphylogeneticdiversityandmetabolicflexibilityofmercurymethylatingmicroorganisms AT karthikanantharaman expandedphylogeneticdiversityandmetabolicflexibilityofmercurymethylatingmicroorganisms AT katherinedmcmahon expandedphylogeneticdiversityandmetabolicflexibilityofmercurymethylatingmicroorganisms
_version_	1718376000513900544

Expanded Phylogenetic Diversity and Metabolic Flexibility of Mercury-Methylating Microorganisms

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