Environmental Conditions Constrain the Distribution and Diversity of Archaeal merA in Yellowstone National Park, Wyoming, U.S.A.
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The distribution and phylogeny of extant protein-encoding genes recovered from geochemically diverse environments can provide insight into the physical and chemical parameters that led to the origin and which constrained the evolution of a functional process. Mercuric reductase (MerA) plays an integral role in mercury (Hg) biogeochemistry by catalyzing the transformation of Hg(II) to Hg(0). Putative merA sequences were amplified from DNA extracts of microbial communities associated with mats and sulfur precipitates from physicochemically diverse Hg-containing springs in Yellowstone National Park, Wyoming, using four PCR primer sets that were designed to capture the known diversity of merA. The recovery of novel and deeply rooted MerA lineages from these habitats supports previous evidence that indicates merA originated in a thermophilic environment. Generalized linear models indicate that the distribution of putative archaeal merA lineages was constrained by a combination of pH, dissolved organic carbon, dissolved total mercury and sulfide. The models failed to identify statistically well supported trends for the distribution of putative bacterial merA lineages as a function of these or other measured environmental variables, suggesting that these lineages were either influenced by environmental parameters not considered in the present study, or the bacterial primer sets were designed to target too broad of a class of genes which may have responded differently to environmental stimuli. The widespread occurrence of merA in the geothermal environments implies a prominent role for Hg detoxification in these environments. Moreover, the differences in the distribution of the merA genes amplified with the four merA primer sets suggests that the organisms putatively engaged in this activity have evolved to occupy different ecological niches within the geothermal gradient.
KeywordsmerA Yellowstone National Park merA Sequence merA Gene Mercuric Reductase
We thank Jesse Bennett and Kim Slack for assisting with fieldwork in YNP, John DeWild and personnel of USGS mercury Lab (Middleton, WI) for supporting Hg analyses, and Christie Hendrix and her colleagues at the YNP Research Permit Office for their enthusiastic support and field access. This research was supported by the Thermal Biology Institute at Montana State University, through NASA award NAG5-8807: Center for Studying Life in Extreme Environments, by the Environmental Remediation Science Program (ERSP), Biological and Environmental Research (BER), U.S. Department of Energy (Grant DE-FG02-05ER63969), by a European Union Marie Curie Actions—International Incoming Fellowship (FP7-PEOPLE-IIF-2008), and by the National Science Foundation Microbial Observatories program (grant MCB0132022). ESB was supported by an Inland Northwest Research Alliance Graduate Fellowship grant DE-FG07-02ID14277, a Montana University System Water Center Fellowship, and a NASA Astrobiology Institute postdoctoral fellowship. ESB also acknowledges support for the Astrobiology Biogeocatalysis Research Center from the NAI.
- 4.Andersson A (1979) Mercury in soils. In: Nriagu O (ed) The biogeochemistry of mercury in the environment. Esevier, North Holland Biomedical Press, Amsterdam, pp 79–112Google Scholar
- 5.Ball JW, McCleskey RB, Nordstrom DK, Holloway JM (2007) Water-chemistry data for selected springs, geysers, and streams in Yellowstone National Park, Wyoming, 2003–2005. U.S. Geological Survey Open-File Report 2006–1339. U.S. Department of the Interior, City, pp. 183Google Scholar
- 9.Boyd ES, Jackson RA, Encarnacion G, Zahn JA, Beard T, Leavitt WD, Pi Y, Zhang CL, Pearson A, Geesey GG (2007) Isolation, characterization, and ecology of sulfur-respiring crenarchaea inhabiting acid-sulfate-chloride-containing geothermal springs in Yellowstone National Park. Appl Environ Microbiol 73:6669–6677CrossRefPubMedPubMedCentralGoogle Scholar
- 24.Inskeep WP, McDermott TR (2007) Geomicrobiology of acid-sulfate-chloride springs in Yellowstone National Park. In: Inskeep WP, McDermott TR (eds) Geothermal biology and geochemistry in Yellowstone National Park. Montana State University, Bozeman, pp 143–162Google Scholar
- 25.Inskeep WP, Rusch DB, Jay Z, Herrgard MJ, Kozubal MA, Richardson TH, Macur RE, Hamamura N, Rd J, Fouke BW, Reysenbach A-L, Roberto F, Young M, Schwartz A, Boyd ES, Badger J, Mathur EJ, Ortmann AC, Bateson M, Geesey G, Frazier M (2010) Metagenomes from high-temperature chemotrophic systems reveal geochemical controls on microbial community structure and function. PLoS One 5:e9773CrossRefPubMedPubMedCentralGoogle Scholar
- 27.Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 115–175Google Scholar
- 30.McCleskey RB, Ball JW, Nordstrom DK, Holloway JM, Taylor HE (2004) Water-chemistry data for selected hot springs, geysers, and streams in Yellowstone National Park Wyoming 2001–2002. U.S. Geological Survey, U.S. Department of the Interior, Boulder, CO, 95 pagesGoogle Scholar
- 35.Nakagawa R (1974) The mercury content in hot springs. Nippon Kagaku Kaishi:71–74Google Scholar
- 36.Nakagawa R (1984) Amounts of mercury discharged to atmosphere from fumarols and hot spring gases in geothermal areas. Nippon Kagaku Kaishi:709–715Google Scholar
- 44.Nunoura T, Hirayama H, Takami H, Oida H, Nishi S, Shimamura S, Suzuki Y, Inagaki F, Takai K, Nealson KH, Horikoshi K (2005) Genetic and functional properties of uncultivated thermophilic crenarchaeotes from a subsurface gold mine as revealed by analysis of genome fragments. Environ Microbiol 7:1967–1984CrossRefPubMedGoogle Scholar
- 46.Palsson B (2011) Adaptive laboratory evolution. Microbe 6:69–74Google Scholar
- 63.Swofford DL (2003) PAUP*: Phylogenetic analysis using parsimony version 4.0b10 (*and other methods). Sinauer Associates, SunderlandGoogle Scholar
- 64.Team RDC (2010) R Foundation for Statistical Computing. Austria, ViennaGoogle Scholar
- 67.Zillig W, Stetter KO, Schafer W, Janekovic D, Wunderl S, Holz I, Palm P (1981) Thermoproteales: a novel type of extremely thermoacidophilic anaerobic archaebacteria isolated from Icelandic solfataras. Zentralbl Mikrobiol Parasitenkd Infektionskr Hyg Abt 1 Orig C2:205–227Google Scholar