Genome-Resolved Metagenomics and Detailed Geochemical Speciation Analyses Yield New Insights into Microbial Mercury Cycling in Geothermal Springs

Abstract

Geothermal systems emit substantial amounts of aqueous, gaseous and methylated mercury, but little is known about microbial influences on mercury speciation. Here we report results from genome-resolved metagenomics and mercury speciation analysis of acid warm springs in the Ngawha Geothermal Field (-1 and 0.5–13.9 ng L^-1, respectively). Total solid mercury concentrations in spring sediments ranged from 1273 to 7000 μg g^-1. In the context of such ultra-high mercury levels, the geothermal microbiome was unexpectedly diverse, and dominated by acidophilic and mesophilic sulfur- and iron-cycling bacteria, mercury- and arsenic-resistant bacteria, and thermophilic and acidophilic archaea. Integrating microbiome structure and metagenomic potential with geochemical constraints, we constructed a conceptual model for biogeochemical mercury cycling in geothermal springs. The model includes abiotic and biotic controls on mercury speciation, and illustrates how geothermal mercury cycling may couple to microbial community dynamics and sulfur and iron biogeochemistry. IMPORTANCE Little is currently known about biogeochemical mercury cycling in geothermal systems. This manuscript presents a new conceptual model, supported by genome-resolved metagenomic analysis and detailed geochemical measurements. The model illustrates environmental factors that influence mercury cycling in acidic springs, including transitions between solid (mineral) and aqueous phases of mercury, as well as the interconnections among mercury, sulfur and iron cycles. This work provides a framework for studying natural geothermal mercury emissions globally. Specifically, our findings have implications for mercury speciation in wastewaters from geothermal power plants and the potential environmental impacts of microbially and abiotically formed mercury species, particularly where mobilized in spring waters that mix with surface- or ground-waters. Furthermore, in the context of thermophilic origins for microbial mercury volatilization, this report yields new insights into how such processes may have evolved alongside microbial mercury methylation/demethylation, and the environmental constraints imposed by the geochemistry and mineralogy of geothermal systems.