MeHg production in eutrophic lakes: Focusing on the roles of algal organic matter and iron-sulfur-phosphorus dynamics (2023)

Mercury (Hg) is a toxic trace metal that can be emitted from natural sources such as volcanoes and weathering of Hg-bearing minerals in rock [85]. However, human activities, such as mining, fossil-fuel combustion and industrial (e.g., chlor-alkali) production, have greatly increased Hg flux in the global environment [105], [185]. The relatively long atmospheric lifetime (several months to a year) of gaseous elemental mercury (Hg⁰) allows for its long-distance transport globally [128], [52]. The subsequent deposition of atmospheric Hg and runoff lead to ubiquitous Hg pollution in even the most remote and pristine regions like the polar region [148], [246], [52] and hadal trenches (deepest parts of the oceans, 6,000- to 11,000-m depth) ([16], [187]; M. [127], [128]).

Methylmercury (MeHg), which can be effectively converted from inorganic mercury (IHg) in aquatic ecosystems, is a potent neurotoxin that threatens the health of aquatic animals and even humans owing to its efficient bioaccumulation and biomagnification through the food chain [194], [84]. Studies show that the majority of Hg (>85%) in fish is MeHg ([169], [17], [225], [60]; Córdoba-Tovar et al., 2023), the content of which can reach as high as 10⁶ times that in surrounding water [90]. It is thus crucial to understand the factors controlling the methylation of IHg in aquatic ecosystems for reducing such risks [23]. Hg methylation occurs predominantly in oxygen-deficient zones and mediated by certain anaerobic microorganisms possessing the gene pair hgcAB [151], [167] such as sulfate-reducing bacteria (SRB), iron-reducing bacteria (FeRB), methanogens, syntrophs and Asgard archaea [189], [210], [232], [39], [61], [68], [79], [90]. The methylation rates are largely dependent on the activity of Hg methylators and IHg bioavailability ([167], [90]; X. [224]), and thus regulated by various environmental factors including organic and inorganic ligands, temperature, pH, and redox potential (Eh) ([194], [62]; C. [237], [23]).

Eutrophication is also a public concern for its adverse impact on water quality and public health (B. [199], [56]), which is widely existing in lakes (Guo et al., 2007; [163], [164]), reservoirs [220], [86] and coastal areas [181], [47] and generally accompanied by algal blooms [42]. It has been found that eutrophication can significantly affect the migration and transformation (e.g., methylation) of Hg [109], [110], [157], [165]. Algae may serve as a huge Hg sink owing to its high rate of growth and large binding ability to trace metals [165], [230], [37]. Some studies have shown that algae can alleviate the bioaccumulation and trophic transfer of Hg and MeHg by “bloom dilution” [157], [30]. Nevertheless, algal organic matter (AOM) released during the decomposition and deposition of algae has been proved to aggravate Hg methylation in water and sediments by enhancing the abundance and activities of methylating microorganisms and/or increasing the bioavailability of Hg [109], [110], [149], [23], [242], [48].

In addition, eutrophication can greatly alter redox conditions, which have a profound influence on the species transformation and distribution of iron (Fe), sulfur (S) and phosphorus (P) [1], [12], [13], [198], [42], [62], [83], [86]. In general, the decomposition of dead algae and the mineralization of organic matter deplete dissolved oxygen (DO) and thus lead to the state of hypoxia/anoxic in the water column and sediments [100], [145], [249], [86], [94], [95]. Under highly reducing conditions, anaerobic microorganisms like SRB may become active and sulfides can accumulate in bottom waters [1], [13], [62]. On the one hand, active SRB carrying hgcAB genes could enhance Hg methylation [167], [39]; On the other hand, the abundant sulfides could bind with Hg to form less-soluble HgS, which is less bioavailable for the methylating microorganisms and thus may inhibit Hg methylation ([102], [119], [166], [62], [98]; J. [201], [239], [200]). Notably, the microbial and chemical reduction of iron oxyhydroxides (FeOOH) makes the release of Fe(II) from the sediments under eutrophication, which can further react with sulfide to form FeS (mackinawite) and FeS₂ (pyrite) ([83]; Y. [241], [2], [34], [35], [200]). Studies have shown that Fe-S interactions can affect Hg bioavailability and thus Hg methylation [122], [18], [200], [215], [217], [90]. Furthermore, P originally bound to FeOOH could be co-released with Fe(II) [13], [19], [231], [71] and further exacerbate eutrophication and thus cause a more anoxic condition, which is more conducive to Hg methylation [211]. Therefore, the Fe-S-P dynamics caused by eutrophication may regulate Hg methylation in a complex way.

To date, the mechanisms by which eutrophication affects MeHg production have not been comprehensively summarized and analyzed, which hinders accurately predicting the MeHg risk in eutrophic aquatic environments. Given the increasing frequency, magnitude, and duration of algal blooms globally, a systematic and detailed review focusing on the influencing mechanisms of eutrophication on MeHg production turns into a necessity and urgency. In this review, we first summarized the current understanding of eutrophication on biogeochemical cycle of Hg. Special attentions were paid to the roles of AOM on Hg methylation and MeHg demethylation as well as how the migration and species transformations of Fe, S and P under eutrophication influence Hg methylation. Finally, the knowledge gaps and future prospects concerning the mechanisms of MeHg production and MeHg risk control in eutrophic lakes were identified. This work would help us better understand the effect mechanisms of eutrophication on MeHg production and provide theoretical guidance for MeHg risk control.