Distribution of mercury‐cycling genes in the Arctic and equatorial Pacific Oceans and their relationship to mercury speciation

Bowman, Katlin L.; Collins, R. Eric; Agather, Alison M.; Lamborg, Carl H.; Hammerschmidt, Chad R.; Kaul, Drishti; Dupont, Christopher L.; Christensen, Geoff A.; Elias, Dwayne A.

doi:10.1002/lno.11310

Cited by 44 publications

(50 citation statements)

References 72 publications

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“…Nevertheless, recent studies have shown that biological Hg II methylation is in most environments performed by a variety of microorganisms, carrying the hgcA and hgcB gene cluster (Gilmour et al , ; Parks et al ; Yu et al ). An increasing number of recent studies detailed below have intended to evaluate the biotic Hg II methylation by studying the biodiversity and activity of hgcAB + microorganisms (Gionfriddo et al ; Bravo et al , a ; Bowman et al ; Jones et al ; Villar et al ). Nevertheless, it is established that net MMHg production also depends on other concomitant processes, including (1) the composition and activity of the whole microbial community that in turn modulate the activity of hgcAB + microorganisms (Bravo et al ), (2) physico‐chemistry that controls Hg II bioavailability (Schaefer and Morel ; Jonsson et al ; Chiasson‐Gould et al ), and uptake in microorganisms (Schaefer et al ), and (3) biotic and abiotic MMHg demethylation (Du et al ).…”

Section: The Mercury Problemmentioning

confidence: 99%

“…A recent analysis of 243 seawater metagenome samples from 68 different sites of the Tara Oceans revealed high abundances of hgcAB corresponding to taxonomic relatives of known Hg II methylators from Deltaproteobacteria , Firmicutes , and Chloroflexi across all oceans, with the exception of the Arctic that was not studied (Villar et al ). More recently, Bowman et al (), combining PCR amplification and shotgun metagenomics, searched the hgcAB gene cluster in Arctic Ocean seawater without success. Out of all the hgcA ‐like genes found in the queries of marine metagenomes, the Nitrospina phylum, a marine nitrite oxidizing bacteria abundant in oxygen‐deficient zones, appeared to be widespread, predominant and likely a key player for MMHg production in the oxic subsurface waters of the global ocean (Villar et al ), including the Arctic (Bowman et al ) as well as Antarctic sea ice–brine–sea water interfaces (Gionfriddo et al ).…”

Section: Toward a Better Understanding Of Microbial Methylmercury Formentioning

confidence: 99%

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Biotic formation of methylmercury: A bio–physico–chemical conundrum

Bravo

Cosio

2019

Limnology & Oceanography

113

102

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Mercury (Hg) is a natural and widespread trace metal, but is considered a priority pollutant, particularly its organic form methylmercury (MMHg), because of human's exposure to MMHg through fish consumption. Pioneering studies showed the methylation of divalent Hg (HgII) to MMHg to occur under oxygen‐limited conditions and to depend on the activity of anaerobic microorganisms. Recent studies identified the hgcAB gene cluster in microorganisms with the capacity to methylate HgII and unveiled a much wider range of species and environmental conditions producing MMHg than previously expected. Here, we review the recent knowledge and approaches used to understand HgII‐methylation, microbial biodiversity and activity involved in these processes, and we highlight the current limits for predicting MMHg concentrations in the environment. The available data unveil the fact that HgII methylation is a bio‐physico‐chemical conundrum in which the efficiency of biological HgII methylation appears to depend chiefly on HgII and nutrients availability, the abundance of electron acceptors such as sulfate or iron, the abundance and composition of organic matter as well as the activity and structure of the microbial community. An increased knowledge of the relationship between microbial community composition, physico‐chemical conditions, MMHg production, and demethylation is necessary to predict variability in MMHg concentrations across environments.

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Section: The Mercury Problemmentioning

confidence: 99%

Section: Toward a Better Understanding Of Microbial Methylmercury Formentioning

confidence: 99%

Biotic formation of methylmercury: A bio–physico–chemical conundrum

Bravo

Cosio

2019

Limnology & Oceanography

113

102

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“…Podar et al (2015) only 60 detected hgcAB genes in a few metagenomes from marine pelagic waters (seven out of 138 61 metagenomes) but highlighted that limited sequencing depths of these metagenomes could have 62 hampered detection. A more recent study did not detect hgcA genes in waters from the Arctic and 63 equatorial Pacific Oceans (Bowman et al, 2019). Interestingly, the presence of hgcAB-like genes 64 was reported in normoxic water from open ocean and sea ice in Antarctica, with a fraction of those 65 genes being associated to microaerophilic nitrite oxidizing bacteria (Gionfriddo et al, 2016;Villar 66 et al, 2020).…”

Section: Introduction 41mentioning

confidence: 95%

“…54 55 Recent advances in metagenomics have yielded new insights into the microbial taxonomic and 56 functional diversity in various aquatic ecosystems (e.g., Mehrshad et al, 2016;Haro-Moreno et al, 57 2018; Nowinski et al, 2019). The approach has for example been applied to broadly assess the 58 presence and diversity of genes central to biological Hg cycling in marine systems (Podar et al,59 2015; Gionfriddo et al, 2016;Bowman et al, 2019;Villar et al, 2020). Podar et al (2015) only 60 detected hgcAB genes in a few metagenomes from marine pelagic waters (seven out of 138 61 metagenomes) but highlighted that limited sequencing depths of these metagenomes could have 62 hampered detection.…”

Section: Introduction 41mentioning

confidence: 99%

Marine snow as a habitat for microbial mercury methylators in the Baltic Sea

Capo

Bravo

et al. 2020

Preprint

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22Methylmercury (MeHg), a neurotoxic compound biomagnifying in aquatic food webs, can be a 23 threat to human health via fish consumption. However, the composition and distribution of the 24 microbial communities mediating the methylation of mercury (Hg) to MeHg in marine systems 25 remain largely unknown. In order to fill this gap of knowledge, we used the Baltic Sea Reference 26 Metagenome (BARM) dataset to study the distribution of the genes involved in Hg methylation (the 27 hgcAB gene cluster). We determined the relative abundance of the hgcAB genes and their 28 taxonomic identity in 81 brackish metagenomes that cover spatial, seasonal and redox variability in 29 the Baltic Sea water. The hgcAB genes were predominantly detected in anoxic water, but some 30 hgcAB genes were also detected in hypoxic and normoxic waters. Higher relative quantities of 31 hgcAB genes were found in metagenomes from marine snow compared to free-living communities 32 in anoxic water, suggesting that marine snow are hotspot habitats for Hg methylators in oxygen-33 depleted seawater. Phylogenetic analysis identified well-characterized Hg methylators such as 34 Deltaproteobacteria in oxygen-depleted water, but also uncovered Hg methylators within the 35 Spirochaetes and Lentisphaerae phyla. Altogether, our work unveils the diversity of the 36 microorganisms mediating MeHg production in the Baltic Sea and pinpoint the ecological niches of 37 these microorganisms within the marine water column. 38 39 40

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“…In addition to the Hg-methylators confirmed in culture, sulfate-and iron-reducing Deltaproteobacteria, acetogenic and syntrophic Firmicutes, and methanogenic Archaea (Compeau and Bartha, 1985;Fleming et al, 2006;Kerin et al, 2006;Ranchou-Peyruse et al, 2009;Gilmour et al, 2013;Yu et al, 2013;Gilmour et al, 2018;Goñi-Urriza et al, 2019)genomic analyses have identified hgcAB (and thus inferred the ability to produce MeHg) in many other lineages including Chloroflexi, Chrysiogenetes, Aminicenantes (Candidate Phylum OP8), Atribacteria (Candidate Phylum OP9), Nitrospira, Nitrospina, Elusimicrobia, Thermotogae and Spirochaetes (Podar et al, 2015a;Gionfriddo et al, 2016;Liu et al, 2018a;Bowman et al, 2019;Christensen et al, 2019;Jones et al, 2019). The occurrence of hgcAB in Bacterial and Archaeal genomes is rare but widely dispersed across phyla (Parks et al, 2013;Podar et al, 2015a;Jones et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

An improvedhgcABprimer set and direct high-throughput sequencing expand Hg-methylator diversity in nature

Gionfriddo

Wymore

Jones

et al. 2020

Preprint

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The gene pair hgcAB is essential for microbial mercury methylation. Our understanding of its abundance and diversity in nature is rapidly evolving. In this study we developed a new broadrange primer set for hgcAB, plus an expanded hgcAB reference library, and used these to characterize Hg-methylating communities from diverse environments. We applied this new Hgmethylator database to assign taxonomy to hgcA sequences from clone, amplicon, and metagenomic datasets. We evaluated potential biases introduced in primer design, sequence length, and classification, and suggest best practices for studying Hg-methylator diversity. Our study confirms the emerging picture of an expanded diversity of HgcAB-encoding microbes in many types of ecosystems, with abundant putative mercury methylators Nitrospirae and Chloroflexi in several new environments including salt marsh and peat soils. Other common microbes encoding HgcAB included Phycisphaerae, Aminicenantes, Spirochaetes, and Elusimicrobia. Gene abundance data also corroborate the important role of two "classic" groups of methylators (Deltaproteobacteria and Methanomicrobia) in many environments, but generally show a scarcity of hgcAB+ Firmicutes. The new primer set was developed to specifically target hgcAB sequences found in nature, reducing degeneracy and providing increased sensitivity while maintaining broad diversity capture. We evaluated mock communities to confirm primer improvements, including culture spikes to environmental samples with variable DNA extraction and PCR amplification efficiencies. For select sites, this new workflow was combined with direct high-throughput hgcAB sequencing. The hgcAB diversity generated by direct amplicon sequencing confirmed the potential for novel Hg-methylators previously identified using metagenomic screens. A new phylogenetic analysis using sequences from freshwater, saline, and terrestrial environments showed Deltaproteobacteria HgcA sequences generally clustered among themselves, while metagenome-resolved HgcA sequences in other phyla tended to cluster by environment, suggesting horizontal gene transfer into many clades. HgcA from marine metagenomes often formed distinct subtrees from those sequenced from freshwater ecosystems. Overall the majority of HgcA sequences branch from a cluster of HgcAB fused proteins related to Thermococci, Atribacteria (candidate division OP9), Aminicenantes (OP8), and Chloroflexi. The improved primer set and library, combined with direct amplicon sequencing, provide a significantly improved assessment of the abundance and diversity of hgcAB+ microbes in nature. Contribution to the Field StatementThe gene pair hgcAB is essential for microbial production of the neurotoxin methylmercury. In recent years these genes have been used as biomarkers to determine the potential of a microbiome to generate methylmercury via PCR amplification using degenerate primers from several research groups. However, improved techniques for capturing hgcAB diversity are necessary for identifying the major environmental p...

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Distribution of mercury‐cycling genes in the Arctic and equatorial Pacific Oceans and their relationship to mercury speciation

Cited by 44 publications

References 72 publications

Biotic formation of methylmercury: A bio–physico–chemical conundrum

Biotic formation of methylmercury: A bio–physico–chemical conundrum

Marine snow as a habitat for microbial mercury methylators in the Baltic Sea

An improvedhgcABprimer set and direct high-throughput sequencing expand Hg-methylator diversity in nature

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