Abstract
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.
Highlights
Active geothermal springs provide a modern analog for environments in which early life on Earth evolved metal(loid) resistance mechanisms (Stetter, 2006; Martin et al, 2008)
The DO saturation increased toward the margin of the pool to 45% at corresponds in location (CPc)
Dissolved organic carbon (DOC) concentrations declined below the detection limit of 0.5 mg l−1 at CPc
Summary
Active geothermal springs provide a modern analog for environments in which early life on Earth evolved metal(loid) resistance mechanisms (Stetter, 2006; Martin et al, 2008). In addition to high temperatures, high concentrations of dissolved toxic metal(loid)s present a strong selective pressure (Hirner et al, 1998) on extant hot spring microbial communities. There is evidence to support the evolution of several microbial metal(loid) tolerance mechanisms in geothermal settings (Barkay et al, 2003; Jackson and Dugas, 2003; Maezato and Blum, 2012). In this regard, understanding the structure, diversity and functionality of modern hot spring microbial communities in the context of arsenic speciation may yield insights into the environmental conditions and constraints under which specific arsenic tolerance strategies evolved. Arsenate is a phosphate analog, which displaces phosphate www.frontiersin.org
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