Adaptation of chemosynthetic microorganisms to elevated mercury concentrations in deep-sea hydrothermal vents

Abstract

The response of deep-sea vent microorganisms to mercury (Hg) was investigated through measurements of total Hg (THg) concentrations in hydrothermal fluids from diffuse and focused flow vents on the East Pacific Rise at 9uN and the estimations of the proportion of Hg-resistant chemosynthetic thiosulfate-oxidizing microbes in a representative subset of diffuse flow fluids. Fluids were enriched in THg, with concentrations ranging from 15 to 445 pmol L 21 and 3.5 6 0.1 to 11.0 6 0.8 nmol L 21 in diffuse and focused flow emissions, respectively. In diffuse flow samples, most probable numbers (MPN) indicated that 0.25-24.6% of the total chemosynthetic thiosulfateoxidizing bacteria were resistant to Hg. The highest resistance levels were observed in samples with the highest THg concentrations, indicating that adaptation to life with toxic Hg had occurred in the diffuse flow environment. High THg concentrations in vent emissions and adaptation to Hg among chemosynthetic vent microbes indicate that (1) Hg in vent emissions may contribute to the oceanic Hg mass balance, and (2) activities of chemosynthetic microbes may mobilize solid-phase Hg in metal sulfide and contribute to Hg detoxification in deep-sea diffuse flow vents. Thus, the activities of chemosynthetic microbes may be critical to the mobility, geochemical cycling, and toxicity of Hg in the vent ecosystem.Metal resistance is common among microorganisms and is a critical factor modulating the effects of metals in the environment (Nies 1999). Although the evolutionary origin of microbial metal resistance is unknown, geothermal environments, such as deep-sea hydrothermal vents, where heavy metal concentrations may be comparable to those in contaminated sites, could represent ecological niches in which metal-microbe interactions occurred early during microbial evolution. In these environments, metals often form complexes with reduced sulfur compounds (Dopson et al. 2003). Deep-sea hydrothermal vents are associated with spreading centers along mid-oceanic ridge systems, with hydrothermal fluids occurring as either low-temperature diffuse flows (in which cold, oxygenated seawater 1 Corresponding author (barkay@aesop.rutgers.edu). AcknowledgmentsWe thank the crew of R/V Atlantis and the crew and pilots of the deep-submergence vehicle Alvin for their skillful operations at sea. Gratitude is extended to Eileen Ekstrom for the communication of unpublished data. The contribution of two anonymous reviewers, whose comments on a previous version of the manuscript have greatly improved this paper, is gratefully acknowledged.

Mercury biogeochemical cycling in the ocean and policy implications

“…Similar variability has been observed for other metals (Bagnato et al, 2009; Crespo-Medina et al, 2009; German and Von Damm, 2004). Nearfield removal of Hg from vents also may occur due to precipitation of sulfides and/or oxides, as found for Fe, Mn and other metals that complex strongly with sulfide (German and Von Damm, 2004).…”

“…Evasion of (CH 3 ) 2 Hg to the atmosphere is estimated at ∼0.01 Mmol yr −1 (Mason and Benoit, 2003). There are limited measurements of methylated Hg in hydrothermal fluids (Lamborg et al, 2006; Crespo-Medina et al, 2009) and methylated Hg ranges from <1 to 100% of the total Hg. The fluids with greater CH 3 Hg appear to be associated with sedimented or back arc environments, suggesting that fluid interaction with lithologies high in organic matter are important for the formation of organometallic Hg.…”

A thermophilic bacterial origin and subsequent constraints by redox, light and salinity on the evolution of the microbial mercuric reductase

“…The dominance of MerA from thermophiles in early lineages, when compared with more recently evolved lineages, is consistent with an origin for merA in hydro‐ or geo‐thermal environments. These results are consistent with reports of high Hg concentrations, 10 (King et al ., 2006) to 6800 ng l −1 (de Ronde et al ., 2002), in emissions from terrestrial hot springs (King et al ., 2006; Sherman et al ., 2009) and deep‐sea hydrothermal vents (Crespo‐Medina et al ., 2009). However, Hg(0) and cinnabar dominate inorganic Hg speciation in geothermal environments with low dissolved oxygen concentrations (Varekamp and Buseck, 1984; Barnes and Seward, 1997; Christenson and Mroczek, 2003).…”

Mercury Resistance and Mercuric Reductase Activities and Expression among Chemotrophic Thermophilic Aquificae

“…strain 128-5-R1-1 (R1-1) (34) form the deepest-branching lineage in a MerA phylogeny (2). Strain AAS1 was isolated from a small channel proximal to Obsidian Pool Prime, YNP, and R1-1 was isolated from the Eastern Lau Spreading Center, South Pacific (34), both of which are geothermal environments similar to those where elevated Hg concentrations were reported (12,21,31). The basal position of the Aquificae loci in the MerA phylogenetic reconstructions suggests that merA originated in an ancestor common to deepbranching thermophilic bacteria.…”