Bacterial diversity and ecosystem function of filamentous microbial mats from aphotic (cave) sulfidic springs dominated by chemolithoautotrophic “Epsilonproteobacteria

Authors

  • Annette Summers Engel,

    Corresponding author
    1. Department of Geological Sciences, Research Group for Microbial Geochemistry, University of Texas at Austin, Austin, TX 78712, USA
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    • 1

      Current address: Department of Geology and Geophysics, Louisiana State University, Baton Rouge, LA70803. Tel.: 1 225 578 2469; fax: 1 225 578 2302.

  • Megan L. Porter,

    1. Department of Microbiology and Molecular Biology, Brigham Young University, Provo, UT 84602, USA
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  • Libby A. Stern,

    1. Department of Geological Sciences, Research Group for Microbial Geochemistry, University of Texas at Austin, Austin, TX 78712, USA
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  • Sarah Quinlan,

    1. Department of Integrative Biology, Brigham Young University, Provo, UT 84602, USA
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  • Philip C. Bennett

    1. Department of Geological Sciences, Research Group for Microbial Geochemistry, University of Texas at Austin, Austin, TX 78712, USA
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*Corresponding author. Tel.: +1 512 471 5413; fax: +1 512 471 5766, E-mail address: aengel@geol.lsu.edu

Abstract

Filamentous microbial mats from three aphotic sulfidic springs in Lower Kane Cave, Wyoming, were assessed with regard to bacterial diversity, community structure, and ecosystem function using a 16S rDNA-based phylogenetic approach combined with elemental content and stable carbon isotope ratio analyses. The most prevalent mat morphotype consisted of white filament bundles, with low C:N ratios (3.5–5.4) and high sulfur content (16.1–51.2%). White filament bundles and two other mat morphotypes had organic carbon isotope values (mean δ13C =−34.7‰, 1σ= 3.6) consistent with chemolithoautotrophic carbon fixation from a dissolved inorganic carbon reservoir (cave water, mean δ13C =−7.4‰ for two springs, n= 8). Bacterial diversity was low overall in the clone libraries, and the most abundant taxonomic group was affiliated with the “Epsilonproteobacteria” (68%), with other bacterial sequences affiliated with Gammaproteobacteria (12.2%), Betaproteobacteria (11.7%), Deltaproteobacteria (0.8%), and the Acidobacterium (5.6%) and Bacteriodetes/Chlorobi (1.7%) divisions. Six distinct epsilonproteobacterial taxonomic groups were identified from the microbial mats. Epsilonproteobacterial and bacterial group abundances and community structure shifted from the spring orifices downstream, corresponding to changes in dissolved sulfide and oxygen concentrations and metabolic requirements of certain bacterial groups. Most of the clone sequences for epsilonproteobacterial groups were retrieved from areas with high sulfide and low oxygen concentrations, whereas Thiothrix spp. and Thiobacillus spp. had higher retrieved clone abundances where conditions of low sulfide and high oxygen concentrations were measured. Genetic and metabolic diversity among the “Epsilonproteobacteria” maximizes overall cave ecosystem function, and these organisms play a significant role in providing chemolithoautotrophic energy to the otherwise nutrient-poor cave habitat. Our results demonstrate that sulfur cycling supports subsurface ecosystems through chemolithoautotrophy and expand the evolutionary and ecological views of “Epsilonproteobacteria” in terrestrial habitats.

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