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Environmental Conditions Constrain the Distribution and Diversity of Archaeal merA in Yellowstone National Park, Wyoming, U.S.A.

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Abstract

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.

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Acknowledgments

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.

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Authors and Affiliations

  1. Department of Biochemistry and Microbiology, Rutgers University, New Brunswick, NJ, USA

    Yanping Wang, Sharron Crane, Patricia Lu-Irving & Tamar Barkay

  2. Department of Chemistry and Biochemistry and the Astrobiology Biogeocatalysis Research Center, Montana State University, Bozeman, MT, USA

    Eric Boyd

  3. Graduate Program in Ecology and Evolution, Rutgers University, New Brunswick, NJ, USA

    Sharron Crane

  4. U.S. Geological Survey, Middleton, WI, USA

    David Krabbenhoft

  5. Chemical and Biological Engineering Department and Thermal Biology Institute, Montana State University, Bozeman, MT, USA

    Susan King

  6. Rutgers Pinelands Field Station, New Lisbon, NJ, USA

    John Dighton

  7. Department of Microbiology and Thermal Biology Institute, Montana State University, Bozeman, MT, USA

    Gill Geesey

  8. Department of Biology, The University of Washington, Box 351800, Seattle, WA, 98195, USA

    Patricia Lu-Irving

  9. 2908 3rd Ave., Great Falls, MT, 59401, USA

    Susan King

  10. Department of Microbiology, Montana State University, 109 Lewis Hall, P.O. Box 173520, Bozeman, MT, 59717–3520, USA

    Gill Geesey

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  1. Yanping Wang
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Correspondence to Gill Geesey.

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Table S1

Primer sets and respective PCR conditions used to target diversity of merA sequences in samples used for this study (DOC 38 kb)

Table S2

Specificity range of the six degenerate merA primer sets (DOC 42 kb)

Table S3

Clones constructed from amplicons generated with primer sets 2, 3, and 4 from Hg-containing sites in geothermal springs of Yellowstone National Park (XLS 38 kb)

Figure S1

A neighbor-joining tree of MerA sequences used for the design of the merA primer sets. MerA protein sequences were downloaded from the NCBI database. The sequences were aligned using ClustalW2.0, trimmed in ClustalX, and a the neighbor-joining phylogenetic tree were constructed using PAUP* 4.0 (Swofford, D. L. 2003. PAUP*. Phylogenetic Analysis Using Parsimony [*and Other Methods]. Version 4. Sinauer Associates, Sunderland, Massachusetts) with 1, 000 bootstrap replicates. The range of organisms whose merA genes were targeted by each primer set is indicated by brackets. Numbers alongside brackets correspond to the PCR primer set designed to amplify merA sequences in the bracketed species. The asterisk following A. pernix K1 denotes the merA of this organism was a part of the alignments that were used for the design of both primer sets 5 and 6. Bar—50 base substitutions. Bootstrap values are indicated at branching points. Underlined species name implies that mercuric reductase activity was documented in this species. (DOCX 76 kb)

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Wang, Y., Boyd, E., Crane, S. et al. Environmental Conditions Constrain the Distribution and Diversity of Archaeal merA in Yellowstone National Park, Wyoming, U.S.A.. Microb Ecol 62, 739–752 (2011). https://doi.org/10.1007/s00248-011-9890-z

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