Nitrospina-Like Bacteria Are Potential Mercury Methylators in the Mesopelagic Zone in the East China Sea

In natural environments, the production of neurotoxic and bioaccumulative methylmercury (MeHg) is mediated by microorganisms carrying the genes hgcA and hgcB. However, the contribution of these microorganisms to mercury (Hg) methylation or MeHg accumulation in the ocean is poorly understood. Here we...

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Main Authors: Yuya Tada, Kohji Marumoto, Akinori Takeuchi
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-07-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2020.01369/full
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author Yuya Tada
Kohji Marumoto
Akinori Takeuchi
author_facet Yuya Tada
Kohji Marumoto
Akinori Takeuchi
author_sort Yuya Tada
collection DOAJ
description In natural environments, the production of neurotoxic and bioaccumulative methylmercury (MeHg) is mediated by microorganisms carrying the genes hgcA and hgcB. However, the contribution of these microorganisms to mercury (Hg) methylation or MeHg accumulation in the ocean is poorly understood. Here we determined the total Hg (THg) and MeHg concentrations in seawater samples and conducted a metagenomic survey of the hgcAB genes and functional modules involved in metabolic pathways in the East China Sea (ECS). In the metagenomic analyses, we used paired-end reads and assembled contigs for hgcAB enumeration and phylogenetic analyses in the seawater column. To evaluate the relative abundance of hgcAB in the metagenomic data, we estimated the abundance of recA (single-copy gene of bacteria) as well and then compared them. Moreover, the profiles of prokaryotic community composition were analyzed by 16S rRNA gene (V4 region) deep-sequencing. In the mesopelagic layers, the hgcA sequences were detected, and there was a positive correlation between hgcA abundance relative to the recA and MeHg concentrations. Thus, the quantification of the hgcA sequences could provide valuable information to evaluate the potential environments of microbial MeHg accumulation in the seawater column. A phylogenetic analysis using the assembled contigs revealed that all of the hgcA sequences in the mesopelagic layers were affiliated with Nitrospina-like sequences. The 16S rRNA gene analysis revealed that Nitrospinae were abundant in the mesopelagic layers. Although the lineages of Deltaproteobacteria, Firmicutes, and Spirochaetes were detected in the seawater column, their hgcAB sequences were not detected in our metagenomes, despite the fact that they are closely related to previously identified Hg methylators. The metabolic pathway analysis revealed that the modules related to sulfur and methane metabolism were prominent in the mesopelagic layers. However, no hgcA sequences affiliated with sulfate-reducing bacteria (SRB) or methanogens were detected in these layers, suggesting that these bacteria could not be strongly involved in the Hg accumulation in the seawater column. Our results indicate that Nitrospina-like bacteria with hgcAB genes could play a critical role in microbial Hg accumulation in the oxygenated mesopelagic layers of the ECS.
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spelling doaj.art-91a92850a82443648b7bc2712f5c9ea22022-12-22T03:47:18ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-07-011110.3389/fmicb.2020.01369522692Nitrospina-Like Bacteria Are Potential Mercury Methylators in the Mesopelagic Zone in the East China SeaYuya Tada0Kohji Marumoto1Akinori Takeuchi2Department of Environment and Public Health, National Institute for Minamata Disease, Kumamoto, JapanDepartment of Environment and Public Health, National Institute for Minamata Disease, Kumamoto, JapanCenter for Environmental Measurement and Analysis, National Institute for Environmental Studies, Ibaraki, JapanIn natural environments, the production of neurotoxic and bioaccumulative methylmercury (MeHg) is mediated by microorganisms carrying the genes hgcA and hgcB. However, the contribution of these microorganisms to mercury (Hg) methylation or MeHg accumulation in the ocean is poorly understood. Here we determined the total Hg (THg) and MeHg concentrations in seawater samples and conducted a metagenomic survey of the hgcAB genes and functional modules involved in metabolic pathways in the East China Sea (ECS). In the metagenomic analyses, we used paired-end reads and assembled contigs for hgcAB enumeration and phylogenetic analyses in the seawater column. To evaluate the relative abundance of hgcAB in the metagenomic data, we estimated the abundance of recA (single-copy gene of bacteria) as well and then compared them. Moreover, the profiles of prokaryotic community composition were analyzed by 16S rRNA gene (V4 region) deep-sequencing. In the mesopelagic layers, the hgcA sequences were detected, and there was a positive correlation between hgcA abundance relative to the recA and MeHg concentrations. Thus, the quantification of the hgcA sequences could provide valuable information to evaluate the potential environments of microbial MeHg accumulation in the seawater column. A phylogenetic analysis using the assembled contigs revealed that all of the hgcA sequences in the mesopelagic layers were affiliated with Nitrospina-like sequences. The 16S rRNA gene analysis revealed that Nitrospinae were abundant in the mesopelagic layers. Although the lineages of Deltaproteobacteria, Firmicutes, and Spirochaetes were detected in the seawater column, their hgcAB sequences were not detected in our metagenomes, despite the fact that they are closely related to previously identified Hg methylators. The metabolic pathway analysis revealed that the modules related to sulfur and methane metabolism were prominent in the mesopelagic layers. However, no hgcA sequences affiliated with sulfate-reducing bacteria (SRB) or methanogens were detected in these layers, suggesting that these bacteria could not be strongly involved in the Hg accumulation in the seawater column. Our results indicate that Nitrospina-like bacteria with hgcAB genes could play a critical role in microbial Hg accumulation in the oxygenated mesopelagic layers of the ECS.https://www.frontiersin.org/article/10.3389/fmicb.2020.01369/fullmercurymethylmercurymarine bacteriahgcAB genes16S rRNA genefunctional module
spellingShingle Yuya Tada
Kohji Marumoto
Akinori Takeuchi
Nitrospina-Like Bacteria Are Potential Mercury Methylators in the Mesopelagic Zone in the East China Sea
Frontiers in Microbiology
mercury
methylmercury
marine bacteria
hgcAB genes
16S rRNA gene
functional module
title Nitrospina-Like Bacteria Are Potential Mercury Methylators in the Mesopelagic Zone in the East China Sea
title_full Nitrospina-Like Bacteria Are Potential Mercury Methylators in the Mesopelagic Zone in the East China Sea
title_fullStr Nitrospina-Like Bacteria Are Potential Mercury Methylators in the Mesopelagic Zone in the East China Sea
title_full_unstemmed Nitrospina-Like Bacteria Are Potential Mercury Methylators in the Mesopelagic Zone in the East China Sea
title_short Nitrospina-Like Bacteria Are Potential Mercury Methylators in the Mesopelagic Zone in the East China Sea
title_sort nitrospina like bacteria are potential mercury methylators in the mesopelagic zone in the east china sea
topic mercury
methylmercury
marine bacteria
hgcAB genes
16S rRNA gene
functional module
url https://www.frontiersin.org/article/10.3389/fmicb.2020.01369/full
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