Widespread microbial mercury methylation genes in the global ocean

Abstract

11Methylmercury is a neurotoxin that bioaccumulates from seawater to high concentrations in 12 marine fish, putting human and ecosystem health at risk. High methylmercury levels have 13 been found in the oxic subsurface waters of all oceans, yet only anaerobic microorganisms 14 have been identified so far as efficient methylmercury producers in anoxic environments. 15The microaerophilic nitrite oxidizing bacteria Nitrospina has been previously suggested as a 16 possible mercury methylator in Antarctic sea ice. However, the microorganisms processing 17 inorganic mercury into methylmercury in oxic seawater remain unknown. Here we show 18metagenomic evidence from open ocean for widespread microbial methylmercury 19 production in oxic subsurface waters. We find high abundances of the key mercury 20 methylating genes hgcAB across all oceans corresponding to taxonomic relatives of known 21 mercury methylators from Deltaproteobacteria, Firmicutes and Chloroflexi. Our results 22 7 132

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

“…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 ).…”

“…Similarly, a query of more than 3500 publicly available microbial metagenomes performed by Podar et al () unveiled the presence of hgcAB ‐like genes in sediments and in previously unsuspected environments, including invertebrate digestive tracts, thawing permafrost soils, coastal “dead zones,” soils and extreme environments. Moreover, a recent study assessing 243 metagenomes from the Tara Oceans expedition reported high abundances of hgcAB genes in 77 samples across all oceans (Villar et al ). The progress in genetics (Gilmour et al ; Parks et al ; Podar et al ; Bravo et al , a ; Liu et al ; Jones et al ) combined with recent advances in the use of stable isotopes to determine Hg II methylation rate constants in sediments (Monperrus et al ; Jonsson et al ; Bravo et al , ), lakes (Eckley and Hintelmann ), water columns and oceans (Munson et al ) as well as in sinking particles of marine and lake waters (Lehnherr et al ; Gascón Díez et al ) have demonstrated that the potential for MMHg formation in the environment is widespread across ecosystems.…”

“…Podar et al () showed that hgcAB appeared to be abundant in marine sediments but they rarely found it in pelagic marine water column, as from 138 metagenome samples analyzed, only seven showed evidence of hgcAB . 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.…”

“…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 ). However, despite metagenomic evidence for the abundance of Nitrospina in the global ocean, the few cultured strains harboring a fused hgcAB‐ like gene ( Methanococcoides methylutens and Pyrococcus furiosus ) were unable to produce MMHg in experimental conditions (Podar et al ; Gilmour et al ).…”

“…at the moment of the sampling (metatranscriptomics and metaproteomics). Nonetheless, available metagenomics approaches have seldom identified hgcA sequences (i.e., 63 out of 203 metagenome projects revealed hgcA occurrence; Podar et al ; and 77 out 243, Villar et al ) supporting that new study should be conducted in environments relevant for Hg II methylation. Furthermore, metatranscriptomics and metaproteomics are still rarely applied, most likely because they are expensive and time‐consuming.…”