Mineralogy Drives Bacterial Biogeography of Hydrothermally Inactive Seafloor Sulfide Deposits

Brandy M. Toner, Ryan A. Lesniewski, Jeffrey J. Marlow, Lindsey J. Briscoe, Cara M. Santelli, Wolfgang Bach, Beth N. Orcutt, Katrina J. Edwards

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41 Scopus citations

Abstract

Mid-ocean ridge hydrothermal venting creates sulfide deposits containing gradients in mineralogy, fluid chemistry, and temperature. Even when hydrothermal circulation ceases, sulfides are known to host microbial communities. The relationship between mineralogy and microbial community composition in low-temperature, rock-hosted systems has not been resolved at any spatial scale, local or global. To examine the hypothesis that geochemistry of seafloor deposits is a dominant parameter driving environmental pressure for bacterial communities at low-temperature, the shared community membership, richness, and structure was measured using 16S rRNA gene sequences. The focus of the study was on hydrothermally inactive seafloor deposits from multiple locations within one deposit (e.g., single extinct chimney), within one vent field (intra-vent field), and among globally distributed vent fields from three ocean basins (inter-vent field). Distinct mineral substrates, such as hydrothermally inactive sulfides versus basalts, host different communities at low temperature in spite of close geographic proximity and contact with the same hydrothermally influenced deep-sea water. Furthermore, bacterial communities inhabiting hydrothermally inactive sulfide deposits from geographically distant locations cluster together in community cladograms to the exclusion of other deep-sea substrates and settings. From this study, we conclude that at low temperature, mineralogy was a more important variable determining microbial community composition than geographic factors. Supplemental materials are available for this article. Go to the publisher's online edition of Geomicrobiology Journal to view the supplemental file.

Original languageEnglish (US)
Pages (from-to)313-326
Number of pages14
JournalGeomicrobiology Journal
Volume30
Issue number4
DOIs
StatePublished - Feb 2013

Bibliographical note

Funding Information:
We thank PD Schloss and JA Huber for discussions regarding community comparisons and data treatment; JA Huber and WJ Brazelton for unpublished data; M. Manno and L. Sauer of the University of Minnesota Characterization Facility for assistance with X-ray diffraction; DR Rogers for sample collection. For financial support we thank the NASA Astrobiology Institute (NNA04CC04A); the National Research Council Associate and NASA Postdoctoral Programs (BMT); RIDGE 2000 (OCE-0241791; KJE and WB); CFANS University of Minnesota (BMT); Woods Hole Oceanographic Institution’s Summer Student Fellow program (JJM); the DFG-Research Center/Excellence Cluster The Ocean in the Earth System (WB), and the Danish National Research Foundation and the Max Planck Society (BNO). Parts of this work were carried out in the Characterization Facility, University of Minnesota, which receives partial support from NSF through the MRSEC program. ∗Address correspondence to Brandy M. Toner, Department of Soil, Water, and Climate, University of Minnesota, 1991 Upper Buford Circle, St. Paul, MN 55108, USA; Email: toner@umn.edu Volcanic activity along the global mid-ocean ridge releases heat and matter from Earth’s crust to the deep-ocean, causing the formation of a wide spectrum of biogeochemical provinces in the deep-ocean. These provinces are characterized by the juxtaposition of reduced compounds in hydrothermal fluids and mineral deposits with oxygenated seawater. The opposing gradients of inorganic reductants and oxidants provide energy having the potential to fuel microbial activity in these habitats. At sites of active hydrothermal venting, physical and chemical gradients should largely constrain the metabolic opportunities for microbial communities. Illustrations of this principle include evidence that active and hydrothermally inactive sulfide deposits host different microbial communities (Kato et al. 2010). In addition, it has been demonstrated that archaea dominate microbial communities at high temperature, while bacteria become prevalent as temperatures decrease (Kormas et al. 2006; Schrenk et al. 2003). During active hydrothermal venting, a mineralogical gradient is created within chimney walls (Tivey 1995); yet, the role of mineralogy and mineralogical gradients in microbial community composition, although often implicated, has not been resolved at any spatial scale. Striking similarities in microbial communities associated with geographically distant seafloor basaltic lavas (Santelli et al. 2008; Santelli et al. 2009) point to mineral composition as a potential master variable in bacterial community characteristics at low temperature in the deep-sea.

Keywords

  • East Pacific Rise
  • basalts
  • microbial ecology
  • mid-ocean ridge
  • sulfides

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