Microbes in mercury-enriched geothermal springs in western North America

Abstract

Because geothermal environments contain mercury (Hg) from natural sources, microorganisms that evolved in these systems have likely adapted to this element. Knowledge of the interactions between microorganisms and Hg in geothermal systems may assist in understanding the long-term evolution of microbial adaptation to Hg with relevance to other environments where Hg is introduced from anthropogenic sources. A number of microbiological studies with supporting geochemistry have been conducted in geothermal systems across western North America. Approximately 1 in 5 study sites include measurements of Hg. Of all prokaryotic taxa reported across sites with microbiological and accompanying physicochemical data, 42% have been detected at sites in which Hg was measured. Genes specifying Hg reduction and detoxification by microorganisms were detected in a number of hot springs across the region. Archaeal-like sequences, representing two crenarchaeal orders and one order each of the Euryarchaeota and Thaumarchaeota, dominated in metagenomes' MerA (the mercuric reductase protein) inventories, while bacterial homologs were mostly found in one deeply sequenced metagenome. MerA homologs were more frequently found in metagenomes of microbial communities in acidic springs than in circumneutral or high pH geothermal systems, possibly reflecting higher bioavailability of Hg under acidic conditions. MerA homologs were found in hot springs prokaryotic isolates affiliated with Bacteria and Archaea taxa. Acidic sites with high Hg concentrations contain more of Archaea than Bacteria taxa, while the reverse appears to be the case in circumneutral and high pH sites with high Hg concentrations. However, MerA was detected in only a small fraction of the Archaea and Bacteria taxa inhabiting sites containing Hg. Nevertheless, the presence of MerA homologs and their distribution patterns in systems, in which Hg has yet to be measured, demonstrates the potential for detoxification by Hg reduction in these geothermal systems, particularly the low pH springs that are dominated by Archaea.

Expression and regulation of the mer operon in Thermus thermophilus

“…The natural habitat for T . thermophilus is in hot springs with circumneutral to alkaline pH (Williams and Da Costa, ) where lower mercury concentrations were reported relative to acidic sulphidic springs (Geesey et al ., ). The mer systems of Thermus spp.…”

“…Here, we provide the first analysis of the transcriptional regulation of the earliest MerRregulated mer operon in T. thermophilus HB27. The natural habitat for T. thermophilus is in hot springs with circumneutral to alkaline pH (Williams and Da Costa, 1992) where lower mercury concentrations were reported relative to acidic sulphidic springs (Geesey et al, 2016). The mer systems of Thermus spp.…”

Genome-resolved metagenomics and detailed geochemical speciation analyses yield new insights into microbial mercury cycling in geothermal springs

“…Geothermal systems provide an environment in which relationships between the chemical and physical processes controlling Hg speciation and bioavailability, and microbial Hg transformations (4, 7), remain poorly understood. Temperature and pH constitute major drivers of microbial diversity in geothermal springs, with pH contributing to a greater extent (61, 62).…”

“…Geothermal springs and fumaroles emit substantial amounts of aqueous and gaseous mercury (Hg) (1). Aqueous Hg concentrations in these systems often exceed 100 ng L −1 and total Hg levels can approach 25 µg L −1 (2–4). Despite these ultra-high mercury levels, few studies have examined biotic and abiotic mechanisms for Hg transformations or Hg speciation in geothermal springs.…”

“…The efficiency of microbial methylation of Hg(II) to MeHg is still largely unknown in geothermal spring ecosystems, particularly under acidic conditions (<55 °C, pH < 4.5; (4, 5, 16)). However, the hgcAB genes required by microorganisms to methylate Hg (17) have been reported from many environments, including wetland sediments, rice paddy soils, thawing permafrost, hypersaline and hypersulfidic waters, soda lakes, and geothermal systems (16, 18–20).…”