Le mercure en Arctique, de l’environnement à la santé humaine : photodéméthylation aquatique, bioaccessibilité alimentaire et interactions avec le microbiome intestinal humain

Mercury (Hg) is a contaminant of major interest in the Arctic, both for human and ecosystem health. Produced at industrialized latitudes by human activity, Hg is easily carried to the Arctic. It can then be deposited in the North and accumulate in aquatic ecosystems, where it can be transformed into its organic and toxic form of methylmercury (MeHg). As MeHg can biomagnify through foodwebs, it can have important health consequences on the Inuit, whose traditional diet relies on fauna that can be contaminated. The goal of this thesis is to improve our understanding of the cycle of Hg and MeHg in the North, to better assess the risk it represents to aquatic ecosystem health and to the Inuit. First, we focus on the photodemethylation of MeHg, an abiotic process occurring in aquatic ecosystems that degrades MeHg into the less toxic Hg. Our results show that while photodemethylation occurs in permafrost thaw ponds, it is barely detectable in Arctic oligotrophic lakes. This contradicts the commonly accepted idea that photodemethylation is ubiquitous in aquatic ecosystems, and we hypothesized that the lack of organic matter in oligotrophic lakes may explain this difference. Finally, by manipulating an entire pond, we show that photodemethylation did not impact this small ecosystem’s net MeHg budget. However, we suggest that the importance of photodemethylation may change with increased input of organic matter and Hg into thaw ponds due to climate warming (Girard et al. 2016). MeHg that is not degraded by photodemethylation can enter food webs and bioamplify in aquatic animals, and thus be absorbed by humans through their diet. Guidelines aiming to protect consumers from Hg assume that 100% of MeHg in fish is absorbed by the human body, but recent studies suggest this may be an overestimate. Indeed, these recommendations do not take into account dietary practices, which may alter speciation and complexation of MeHg, changing the way it is absorbed. We used an in vitro digestion model to study the impact of dietary practices on bioaccessibility (the fraction of a contaminant solubilized in the gastrointestinal tract) of MeHg. Our results show that cooking and co-ingesting polyphenol-rich foods (such as tea) can significantly reduce bioaccessibility, and both treatments can have a cumulative effect. While this in vitro study must be validated in an in vivo model, it improves our understanding of the mechanistic fate of Hg in the body, and offers novel ways of improving current guidelines (Girard et al. 2017a). iii Another variable that could potentially affect how MeHg behaves in the human body is the gut microbiome, the complex microbial ecosystem that colonizes the human intestine. Since microorganisms are the drivers of biogeochemical cycling of Hg in the environment, it is possible bacterial members of the microbiome can interact with Hg and MeHg ingested with food, notably in the Inuit who are exposed to MeHg through their traditional diet. Here, we provide the first description of the Inuit microbiome using next generation sequencing of a marker gene. We show that the taxonomic composition and diversity of the Inuit microbiome is broadly similar to that of Westerners, likely due to the dietary transition currently underway in Northern communities. However, using fine-scale strain-level analyses, we identified many markers associated with the traditional Inuit diet (Girard et al. 2017b). Using shotgun metagenomic sequencing, we also present the first functional profile of the Inuit microbiome, and show that mobile genes such as plasmids have a unique signature in the Inuit. We then explored how the Inuit microbiome can interact with dietary Hg: first, we show evidence for the presence of the Hg resistance operon (mer) in the human gut microbiome, which shows that Hg could be volatilized in the human gut into a less bioavailable species. Finally, we present our survey of the methylator gene hgcAB, and suggest that it is unlikely that Hg is methylated into toxic MeHg in the human microbiome (Girard et al. in prep). This thesis contributes novel observations on Hg and MeHg in the Arctic, especially in its cycling in the human body. Climate change is likely to increase Hg input into Arctic aquatic ecosystems and facilitate its methylation into MeHg, as well as to contribute to altering the Inuit diet. It is thus critical to better understand how this contaminant behaves in the environment and in the human body. This knowledge on the transformations of MeHg in the Arctic will allow us to improve our assessments of potential health risks Inuit populations face, while encouraging traditional food consumption.

Keyphrases: microbiome, Mercury, Methylmercury, Arctic, Photodemethylation, Bioaccessibility, Polyphenols, Microbiome, Traditional Inuit diet, Mercury resistance (mer operon), Mercury methylation (hgcAB)