Mercury, organic matter, iron, and sulfur co-cycling in a ferruginous meromictic lake

Tisserand, Delphine; Guédron, Stéphane; Viollier, Éric; Jézéquel, Didier; Rigaud, Sylvain; Campillo, Sylvain; Sarret, Géraldine; Charlet, Laurent; Cossa, Daniel

doi:10.1016/j.apgeochem.2022.105463

Cited by 11 publications

(3 citation statements)

References 108 publications

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“…This disagrees with earlier studies where persistently high sulfide concentrations were believed to inhibit Hg methylation in the AOL of the Black Sea ( 24 ) and other systems ( 50 , 51 ). Similar to our results, maximal methylation activity was also reported under sulfidic conditions in stratified brackish water ( 19 ) and a meromictic lake ( 52 ). The dual role of sulfide in Hg methylation is complex and still uncertain ( 51 , 53 ).…”

Section: Discussionsupporting

confidence: 91%

Redox gradient shapes the abundance and diversity of mercury-methylating microorganisms along the water column of the Black Sea

et al. 2023

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In the global context of seawater deoxygenation triggered by climate change and anthropogenic activities, changes in redox gradients impacting biogeochemical transformations of pollutants, such as mercury, become more likely. Being the largest anoxic basin worldwide, with high concentrations of the potent neurotoxic methylmercury (MeHg), the Black Sea is an ideal natural laboratory to provide new insights about the link between dissolved oxygen concentration and hgcAB gene-carrying ( hgc + ) microorganisms involved in the formation of MeHg. We combined geochemical and microbial approaches to assess the effect of vertical redox gradients on abundance, diversity, and metabolic potential of hgc + microorganisms in the Black Sea water column. The abundance of hgcA genes [congruently estimated by quantitative PCR (qPCR) and metagenomics] correlated with MeHg concentration, both maximal in the upper part of the anoxic water. Besides the predominant Desulfobacterales , hgc + microorganisms belonged to a unique assemblage of diverse—previously underappreciated—anaerobic fermenters from Anaerolineales , Phycisphaerae (characteristic of the anoxic and sulfidic zone), Kiritimatiellales, and Bacteroidales (characteristic of the suboxic zone). The metabolic versatility of Desulfobacterota differed from strict sulfate reduction in the anoxic water to reduction of various electron acceptors in the suboxic water. Linking microbial activity and contaminant concentration in environmental studies is rare due to the complexity of biological pathways. In this study, we disentangle the role of oxygen in shaping the distribution of Hg-methylating microorganisms consistently with MeHg concentration, and we highlight their taxonomic and metabolic niche partitioning across redox gradients, improving the prediction of the response of marine communities to the expansion of oxygen-deficient zones. IMPORTANCE Methylmercury (MeHg) is a neurotoxin detected at high concentrations in certain marine ecosystems, posing a threat to human health. MeHg production is mainly mediated by hgcAB gene-carrying ( hgc + ) microorganisms. Oxygen is one of the main factors controlling Hg methylation; however, its effect on the diversity and ecology of hgc + microorganisms remains unknown. Under the current context of seawater deoxygenation, mercury cycling is expected to be disturbed. Here, we show the strong effect of oxygen gradients on the distribution of potential Hg methylators. In addition, we show for the first time the significant contribution of a unique assemblage of potential fermenters from Anaerolineales , Phycisphaerae , and Kiritimatiellales to Hg methylation, stratified in different redox niches along the Black Sea gradient. Our results considerably expand the known taxonomic diversity and ecological niches prone to the formation of MeHg and contribute to better apprehend the consequences of oxygen depletion in seawater.

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Section: Discussionsupporting

confidence: 91%

Redox gradient shapes the abundance and diversity of mercury-methylating microorganisms along the water column of the Black Sea

et al. 2023

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“…Our results show that like other similar lakes, the availability of oxygen across the water column and shallow sediments of Lac Pavin can be linked to changes in both microbial community composition and the metabolic capacities of its members. This oxygen gradient, alongside gradients of dissolved organic/inorganic carbon, sulfur, and iron, which also vary substantially with depth [66][67][68][69], likely play an important role in determining distributions of key bacterial and archaeal lineages in this ecosystem. Here, we provide high-quality genomic data for many of these lineages, including abundant members of the Actinobacteria, which dominate in the shallow water column of Pavin and other similar lakes [70,71].…”

Section: Discussionmentioning

confidence: 99%

Variable impact of geochemical gradients on the functional potential of bacteria, archaea, and phages from the permanently stratified Lac Pavin

et al. 2023

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Background Permanently stratified lakes contain diverse microbial communities that vary with depth and so serve as useful models for studying the relationships between microbial community structure and geochemistry. Recent work has shown that these lakes can also harbor numerous bacteria and archaea from novel lineages, including those from the Candidate Phyla Radiation (CPR). However, the extent to which geochemical stratification differentially impacts carbon metabolism and overall genetic potential in CPR bacteria compared to other organisms is not well defined. Results Here, we determine the distribution of microbial lineages along an oxygen gradient in Lac Pavin, a deep, stratified lake in central France, and examine the influence of this gradient on their metabolism. Genome-based analyses revealed an enrichment of distinct C1 and CO2 fixation pathways in the oxic lake interface and anoxic zone/sediments, suggesting that oxygen likely plays a role in structuring metabolic strategies in non-CPR bacteria and archaea. Notably, we find that the oxidation of methane and its byproducts is largely spatially separated from methane production, which is mediated by diverse communities of sediment methanogens that vary on the centimeter scale. In contrast, we detected evidence for RuBisCO throughout the water column and sediments, including form II/III and form III-related enzymes encoded by CPR bacteria in the water column and DPANN archaea in the sediments. On the whole, though, CPR bacteria and phages did not show strong signals of gene content differentiation by depth, despite the fact that distinct species groups populate different lake and sediment compartments. Conclusions Overall, our analyses suggest that environmental gradients in Lac Pavin select for capacities of CPR bacteria and phages to a lesser extent than for other bacteria and archaea. This may be due to the fact that selection in the former groups is indirect and depends primarily on host characteristics.

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“…Some systems do not exhibit a relation to TOC and Hg may instead be adsorbed onto (fine-grained) detrital minerals and detected by a correlation between Hg and mineral dominating elements such as aluminium (Al), titanium (Ti), zirconium (Zr), rubidium (Rb), or potassium (K) (Sanei et al, 2012;Sial et al, 2013;. In few cases, sulphide minerals may act as important Hg hosts (Benoit et al, 1999;Han et al, 2008), however this is less common in freshwater lacustrine systems where sulphate-reduction is often limited and only a small fraction of non-organic sulfur is buried (Ding et al, 2016;Holmer and Storkholm, 2001;Tisserand et al, 2022;Watanabe et al, 2004).…”

Section: Sedimentary Mercury Recordsmentioning

confidence: 99%

Mercury records covering the past 90 kyr from lakes Prespa and Ohrid, SE Europe

Paine

Fendley

Frieling

et al. 2023

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Abstract. The element mercury (Hg) is a key pollutant, and much insight has been gained by studying the present-day Hg cycle. However, many important processes within this cycle operate on timescales responsive to centennial to millennial-scale environmental variability, highlighting the importance of also investigating the longer-term Hg records in sedimentary archives. To this end, we here explore the timing, magnitude, and expression of Hg signals retained in sediments over the past ~90 ka from two lakes, linked by a subterranean karst system: Lake Prespa (Greece/North Macedonia/Albania) and Lake Ohrid (North Macedonia/Albania). Results suggest that Hg fluctuates largely independent of variability in common host phases in each lake, and the recorded sedimentary Hg signals show distinct differences first during the late Pleistocene (Marine Isotope Stages 2–5). The Hg signals in Lake Prespa sediments highlights an abrupt, short-lived, peak in Hg accumulation coinciding with local deglaciation. In contrast, Lake Ohrid shows a broader interval with enhanced Hg accumulation, and, superimposed, a series of low-amplitude oscillations in Hg concentration peaking during the Last Glacial Maximum, that may result from elevated clastic inputs. Divergent Hg signals are also recorded during the early and middle Holocene (Marine Isotope Stage 1). Here, Lake Prespa sediments show a series of large Hg peaks; while Lake Ohrid sediments show a progression to lower Hg values. Around 3 ka, anthropogenic influences overwhelm local fluxes in both lakes. The lack of coherence in Hg accumulation between the two lakes suggests that, in the absence of an exceptional perturbation, local differences in sediment composition, lake structure, and water balance all influence the local Hg cycle, and determine the extent to which Hg signals reflect local or global-scale environmental changes.

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Mercury, organic matter, iron, and sulfur co-cycling in a ferruginous meromictic lake

Cited by 11 publications

References 108 publications

Redox gradient shapes the abundance and diversity of mercury-methylating microorganisms along the water column of the Black Sea

Redox gradient shapes the abundance and diversity of mercury-methylating microorganisms along the water column of the Black Sea

Variable impact of geochemical gradients on the functional potential of bacteria, archaea, and phages from the permanently stratified Lac Pavin

Mercury records covering the past 90 kyr from lakes Prespa and Ohrid, SE Europe

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