Prevalence of Heterotrophic Methylmercury Detoxifying Bacteria across Oceanic Regions.

Microbial reduction of inorganic divalent mercury (Hg2+) and methylmercury (MeHg) demethylation is performed by the mer operon, specifically by merA and merB genes, respectively, but little is known about the mercury tolerance capacity of marine microorganisms and its prevalence in the ocean. Here, combining culture-dependent analyses with metagenomic and metatranscriptomic data, we show that marine bacteria that encode mer genes are widespread and active in the global ocean. We explored the distribution of these genes in 290 marine heterotrophic bacteria (Alteromonas and Marinobacter spp.) isolated from different oceanographic regions and depths, and assessed their tolerance to diverse concentrations of Hg2+ and MeHg. In particular, the Alteromonas sp. ISS312 strain presented the highest tolerance capacity and a degradation efficiency for MeHg of 98.2% in 24 h. Fragment recruitment analyses of Alteromonas sp. genomes (ISS312 strain and its associated reconstructed metagenome assembled genome MAG-0289) against microbial bathypelagic metagenomes confirm their prevalence in the deep ocean. Moreover, we retrieved 54 merA and 6 merB genes variants related to the Alteromonas sp. ISS312 strain from global metagenomes and metatranscriptomes from Tara Oceans. Our findings highlight the biological reductive MeHg degradation as a relevant pathway of the ocean Hg biogeochemical cycle.

Genomic and transcriptomic characterization of methylmercury detoxification in a deep ocean Alteromonas mediterranea ISS312.

Methylmercury (MeHg) is one of the most worrisome pollutants in marine systems. MeHg detoxification is mediated by merB and merA genes, responsible for the demethylation of MeHg and the reduction of inorganic mercury, respectively. Little is known about the biological capacity to detoxify this compound in marine environments, and even less the bacterial transcriptional changes during MeHg detoxification. This study provides the genomic and transcriptomic characterization of the deep ocean bacteria Alteromonas mediterranea ISS312 with capacity for MeHg degradation. Its genome sequence revealed four mer operons containing three merA gene and two merB gene copies, that could be horizontally transferred among distant related genomes by mobile genetic elements. The transcriptomic profiling in the presence of 5 µM MeHg showed that merA and merB genes are within the most expressed genes, although not all mer genes were equally transcribed. Besides, we aimed to identify functional orthologous genes that displayed expression profiles highly similar or identical to those genes within the mer operons, which could indicate they are under the same regulatory controls. We found contrasting expression profiles for each mer operon that were positively correlated with a wide array of functions mostly related to amino acid metabolism, but also to flagellar assembly or two component systems. Also, this study highlights that all merAB genes of the four operons were globally distributed across oceans layers with higher transcriptional activity in the mesopelagic deeper waters. Our study provides new insights about the transcriptional patterns related to the capacity of marine bacteria to detoxify MeHg, with important implications for the understanding of this process in marine ecosystems.

Unmasking the physiology of mercury detoxifying bacteria from polluted sediments.

Marine sediments polluted from anthropogenic activities can be major reservoirs of toxic mercury species. Some microorganisms in these environments have the capacity to detoxify these pollutants, by using the mer operon. In this study, we characterized microbial cultures isolated from polluted marine sediments growing under diverse environmental conditions of salinity, oxygen availability and mercury tolerance. Specific growth rates and percentage of mercury removal were measured in batch cultures for a selection of isolates. A culture affiliated with Pseudomonas putida (MERCC_1942), which contained a mer operon as well as other genes related to metal resistances, was selected as the best candidate for mercury elimination. In order to optimize mercury detoxification conditions for strain MERCC_1942 in continuous culture, three different dilution rates were tested in bioreactors until the cultures achieved steady state, and they were subsequently exposed to a mercury spike; after 24 h, strain MERCC_1942 removed up to 76% of the total mercury. Moreover, when adapted to high growth rates in bioreactors, this strain exhibited the highest specific mercury detoxification rates. Finally, an immobilization protocol using the sol-gel technology was optimized. These results highlight that some sediment bacteria show capacity to detoxify mercury and could be used for bioremediation applications.