Widespread Microbial Mercury Methylation Genes in the Global Ocean
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See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/339451310 Widespread microbial mercury methylation genes in the global ocean Article in Environmental Microbiology Reports · February 2020 DOI: 10.1111/1758-2229.12829 CITATIONS READS 3 59 3 authors, including: Léa Cabrol Lars-Eric Heimbürger-Boavida Institute of Research for Development French National Centre for Scientific Research 40 PUBLICATIONS 412 CITATIONS 93 PUBLICATIONS 1,669 CITATIONS SEE PROFILE SEE PROFILE Some of the authors of this publication are also working on these related projects: ERANET – METHABASE - METHAnogenic Biodiversity and activity in Arctic and Subantarctic Ecosystems affected by climate change View project Concentration, Accumulation and Potential Risks of Anthropogenic Contaminants in Coastal Environments in the North-Western Mediterranean Sea (CAREMED) View project All content following this page was uploaded by Léa Cabrol on 02 March 2020. The user has requested enhancement of the downloaded file. Environmental Microbiology Reports (2020) 00(00), 00–00 doi:10.1111/1758-2229.12829 Brief Report Widespread microbial mercury methylation genes in the global ocean Emilie Villar,1,2 Léa Cabrol 1,3* and subsurface waters of the global ocean where the Lars-Eric Heimbürger-Boavida1 highest MeHg concentrations are typically observed. 1Aix Marseille Université, Univ Toulon, CNRS, IRD, Mediterranean Institute of Oceanography (MIO) UM 110, Introduction 13288, Marseille, France. 2Sorbonne Université, Université Pierre et Marie Curie - Human activities release 2500 tons of inorganic mercury Paris 6, CNRS, UMR 7144 (AD2M), Station Biologique (Hg) every year and have added 55 000 tons of Hg to the de Roscoff, Place Georges Teissier, CS90074, Roscoff, global ocean since the industrial revolution (Outridge et al., 29688, France. 2018). Humans are exposed to Hg in the form of methyl- 3Instituto de Ecologia y Biodiversidad, Departamento de mercury (MeHg), mainly via marine fish consumption. The Ciencias Ecologicas, Facultad de Ciencias, Universidad Minamata Convention (www.mercuryconvention.org) aims de Chile, Santiago de Chile, Chile. to protect human health from the adverse effects of Hg by decreasing anthropogenic inorganic Hg emissions. We must fully understand the origin of marine MeHg to evalu- Summary ate the efficacy and time-scales of lowered Hg emissions Methylmercury is a neurotoxin that bioaccumulates aimed at decreasing fish MeHg levels. Microorganisms from seawater to high concentrations in marine fish, play a central role in Hg transformations. We must identify putting human and ecosystem health at risk. High Hg methylating microbes and the factors controlling their methylmercury levels have been found in the oxic distribution to better constrain MeHg production in the subsurface waters of all oceans, but only anaerobic global ocean. microorganisms have been shown to efficiently pro- Since the only cultured microbes known to produce duce methylmercury in anoxic environments. The MeHg are anaerobic, research has focused for many microaerophilic nitrite-oxidizing bacteria Nitrospina years on a MeHg source in anoxic marine sediments have previously been suggested as possible mercury (Gilmour et al., 2011; Mason et al., 2012; Gilmour et al., methylating bacteria in Antarctic sea ice. However, 2013; Parks et al., 2013). However, several lines of inde- the microorganisms responsible for processing inor- pendent evidence support in situ MeHg production in oxic ganic mercury into methylmercury in oxic seawater seawater as the main source of fish MeHg. Recent large- remain unknown. Here, we show metagenomic and scale oceanographic expeditions found subsurface MeHg metatranscriptomic evidence that the genetic poten- maxima in every ocean basin (Mason et al., 2012; tial for microbial methylmercury production is wide- Schlitzer et al., 2018). The proportion of MeHg to inor- spread in oxic seawater. We find high abundance and ganic Hg throughout the oxic seawater column is higher expression of the key mercury methylating genes (about 40%) than in anoxic sediments (about 5%). Labo- hgcAB across all ocean basins, corresponding to the ratory experiments show that Hg methylation can occur taxonomic relatives of known mercury methylating in anoxic microniches that occur within sinking particles bacteria from Deltaproteobacteria, Firmicutes and in oxic waters (Ortiz et al., 2015). Bianchi and colleagues Chloroflexi. Our results identify Nitrospina as the pre- (2018) provide compelling evidence that anaerobic dominant and widespread microorganism carrying microbes thrive in the anoxic microenvironments of sink- and actively expressing hgcAB. The highest hgcAB abundance and expression occurs in the oxic ing particulate organic matter. Independently, incubation experiments with isotopically labelled Hg spikes show significant in situ Hg methylation in oxic seawater *For correspondence. E-mail [email protected]; Tel. (Lehnherr et al., 2011). Additional evidence stems from (56)-2-29787298. Hg stable isotope signatures of marine fish, which can © 2020 Society for Applied Microbiology and John Wiley & Sons Ltd 2 E. Villar, L. Cabrol and L.E. Heimbürger-Boavida only be explained if 60%–80% of the MeHg is produced incomplete assembly. Alignment of HgcA sequences rev- in open ocean subsurface waters (Blum, 2011). Finally, a ealed seven sequences with the conserved NVWCAA pioneering study found a compound-specific δ13C signa- motif (Parks et al., 2013) and one sequence with the modi- ture of fish tissue MeHg similar to algal δ13C, suggesting fied NIWCAA motif in the ‘cap helix’ region. Mutation that MeHg is produced in the open ocean water column experiments previously showed that the structure of the (Masbou et al., 2015). putative ‘cap helix’ region harbouring Cys93 is crucial for A major breakthrough was made with the discovery of methylation capacity (Smith et al., 2015). Two HgcA two key genes, hgcA and hgcB, which control Hg meth- sequences were truncated (OM-RGC.v1.019516181, OM- ylation in model anaerobic Hg-methylating bacteria RGC.v1.015822836), preventing inspection of their con- (Parks et al., 2013). The presence of the hgcAB operon served motif. However, they could be unequivocally predicts Hg methylation capacity in diverse microorgan- assigned to HgcA sequences based on their phylogenetic isms (Gilmour et al., 2013). A recent methodological eval- placement and high similarity with known HgcA sequences uation study established that hgcAB gene identification (Fig. 2). The five HgcB sequences contained the con- in metagenomic datasets using Pfam/HMM models is a served motif ECGAC (Parks et al., 2013) (Table S1). reliable method to determine Hg-methylating organism Eventually, 10 HgcA sequences were considered for the abundance and diversity (Christensen et al., 2019). A following analysis, based on the presence of the con- screening of publicly available microbial metagenomes served motif NVWCAA, and/or the presence of the neigh- found hgcAB genes in nearly all anoxic environments, bouring HgcB sequence on the scaftig, and the but the study only rarely detected the genes in pelagic corresponding complete protein sequence prediction in marine water column metagenomes in the open ocean Tara Oceans samples (Fig. 1). (Podar et al., 2015). In Antarctic sea ice marine micro- Fifty-four percent of the 77 metagenomic samples con- aerophilic nitrite-oxidizing bacteria belonging to the taining the hgcA gene with paired metatranscriptome Nitrospina genus haves been recently identified as data available contained the hgcA transcript with the potential Hg methylating bacteria with HgcA-like proteins identical sequence in the corresponding meta- (Gionfriddo et al., 2016). We aim to resolve the paradox transcriptome, indicating active expression of the gene between several biogeochemical evidences for in situ (Table S2, Fig. S3). MeHg production and the absence of known anaerobic Hg methylating prokaryotes in the open ocean. Meta- HgcA sequences found in the Tara Oceans assemblies genomic and metatranscriptomic data from 243 and covered nearly all known Hg methylating bacteria 187 Tara Oceans samples, collected from 68 and 108 open ocean locations covering most ocean basins The 10 HgcA sequences found in the Tara Oceans assem- respectively, were analysed to generate an ocean micro- blies were phylogenetically diverse (Fig. 2, Text S1). Nine bial reference gene catalogue (Sunagawa et al., 2015; of the 10 hgcA genes have a corresponding transcript in Salazar et al., 2019). We screened the Tara Oceans the metatranscriptomic dataset, indicating effective expres- metagenomes and metatranscriptomes for the presence sion and probable activity in all phylogenetically distinct of the key hgcA methylating gene. We provide compel- taxa (Table S2). Four sequences (OM-RGC.v1.007700098, ling evidence of the potential bacterial key players OM-RGC.v1.007737171, OM-RGC.v1.023305075 and involved in MeHg production in the open ocean. The OM-RGC.v1.007699863) were closely related to the HgcA- experimental demonstration of MeHg production by sea- like proteins described by Gionfriddo and colleagues water microorganisms was beyond the scope of this (2016) for Nitrospina sp. The Nitrospinae phylum is a phy- study. logenetically distinct group of lithoautotrophic nitrite- oxidizing bacteria exclusively found in marine environments (Lücker et al., 2013), and they are particularly abundant in Results and discussion oxygen-deficient zones (Spieck et