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Acid-sulfide hot springs are analogs of early Earth geothermal systems where microbial metal(loid) resistance likely first evolved. Arsenic is a metalloid enriched in the acid-sulfide hot spring Champagne Pool (Waiotapu, New Zealand). Arsenic speciation in Champagne Pool follows reaction paths not yet fully understood with respect to biotic contributions and coupling to biogeochemical sulfur cycling. Here we present quantitative arsenic speciation from Champagne Pool, finding arsenite dominant in the pool, rim and outflow channel (55–75% total arsenic), and dithio- and trithioarsenates ubiquitously present as 18–25% total arsenic. In the outflow channel, dimethylmonothioarsenate comprised ≤9% total arsenic, while on the outflow terrace thioarsenates were present at 55% total arsenic. We also quantified sulfide, thiosulfate, sulfate and elemental sulfur, finding sulfide and sulfate as major species in the pool and outflow terrace, respectively. Elemental sulfur concentration reached a maximum at the terrace. Phylogenetic analysis of 16S rRNA genes from metagenomic sequencing revealed the dominance of Sulfurihydrogenibium at all sites and an increased archaeal population at the rim and outflow channel. Several phylotypes were found closely related to known sulfur- and sulfide-oxidizers, as well as sulfur- and sulfate-reducers. Bioinformatic analysis revealed genes underpinning sulfur redox transformations, consistent with sulfur speciation data, and illustrating a microbial role in sulfur-dependent transformation of arsenite to thioarsenate. Metagenomic analysis also revealed genes encoding for arsenate reductase at all sites, reflecting the ubiquity of thioarsenate and a need for microbial arsenate resistance despite anoxic conditions. Absence of the arsenite oxidase gene, aio, at all sites suggests prioritization of arsenite detoxification over coupling to energy conservation. Finally, detection of methyl arsenic in the outflow channel, in conjunction with increased sequences from Aquificaceae, supports a role for methyltransferase in thermophilic arsenic resistance. Our study highlights microbial contributions to coupled arsenic and sulfur cycling at Champagne Pool, with implications for understanding the evolution of microbial arsenic resistance in sulfidic geothermal systems.

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Several studies have analyzed biogeographic distribution patterns of microbial communities across broad spatial scales. However, it is often unclear to what extent differences in community composition across different regions are caused by dispersal limitation or selection, and if selection is caused by local environmental conditions alone or additional broad-scale region-specific factors. This is especially true for groundwater environments, which have been understudied in this context relative to other non-subsurface habitats. Here, we analyzed microbial community composition based on exact 16S rRNA amplicon sequence variants (ASVs) from four geographically separated aquifers located in different regions along a latitudinal transect of ∼700 km across Germany. Using a combination of variation partitioning and ecological null models revealed that differences in microbial community composition were mainly the product of selection imposed by local environmental conditions and to a smaller but still significant extent dispersal limitation and drift across regions. Only ∼23% of the total variation in microbial community composition remained unexplained, possibly due to underestimated effects of dispersal limitation among local communities within regions and temporal drift. No evidence was found for selection due to region-specific factors independent of local environmental conditions.

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