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Research Article

Hydrogen-limited growth of hyperthermophilic methanogens at deep-sea hydrothermal vents

Helene C. Ver Eecke, David A. Butterfield, Julie A. Huber, Marvin D. Lilley, Eric J. Olson, Kevin K. Roe, Leigh J. Evans, Alexandr Y. Merkel, Holly V. Cantin, and James F. Holden
  1. aDepartment of Microbiology, University of Massachusetts, Amherst, MA 01003;
  2. bJoint Institute for the Study of the Atmosphere and Ocean and
  3. dSchool of Oceanography, University of Washington, Seattle, WA 98195;
  4. cJosephine Bay Paul Center, Marine Biological Laboratory, Woods Hole, MA 02543;
  5. eCooperative Institute for Marine Resources Studies, Oregon State University, Newport, OR 97365; and
  6. fWinogradsky Institute of Microbiology, Russian Academy of Sciences, Moscow 117312, Russia

See allHide authors and affiliations

PNAS first published August 6, 2012; https://doi.org/10.1073/pnas.1206632109
Helene C. Ver Eecke
aDepartment of Microbiology, University of Massachusetts, Amherst, MA 01003;
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David A. Butterfield
bJoint Institute for the Study of the Atmosphere and Ocean and
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Julie A. Huber
cJosephine Bay Paul Center, Marine Biological Laboratory, Woods Hole, MA 02543;
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Marvin D. Lilley
dSchool of Oceanography, University of Washington, Seattle, WA 98195;
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Eric J. Olson
dSchool of Oceanography, University of Washington, Seattle, WA 98195;
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Kevin K. Roe
bJoint Institute for the Study of the Atmosphere and Ocean and
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Leigh J. Evans
eCooperative Institute for Marine Resources Studies, Oregon State University, Newport, OR 97365; and
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Alexandr Y. Merkel
fWinogradsky Institute of Microbiology, Russian Academy of Sciences, Moscow 117312, Russia
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Holly V. Cantin
cJosephine Bay Paul Center, Marine Biological Laboratory, Woods Hole, MA 02543;
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James F. Holden
aDepartment of Microbiology, University of Massachusetts, Amherst, MA 01003;
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  • For correspondence: jholden@microbio.umass.edu
  1. Edited by David M. Karl, University of Hawaii, Honolulu, HI, and approved June 29, 2012 (received for review April 21, 2012)

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Abstract

Microbial productivity at hydrothermal vents is among the highest found anywhere in the deep ocean, but constraints on microbial growth and metabolism at vents are lacking. We used a combination of cultivation, molecular, and geochemical tools to verify pure culture H2 threshold measurements for hyperthermophilic methanogenesis in low-temperature hydrothermal fluids from Axial Volcano and Endeavour Segment in the northeastern Pacific Ocean. Two Methanocaldococcus strains from Axial and Methanocaldococcus jannaschii showed similar Monod growth kinetics when grown in a bioreactor at varying H2 concentrations. Their H2 half-saturation value was 66 μM, and growth ceased below 17–23 μM H2, 10-fold lower than previously predicted. By comparison, measured H2 and CH4 concentrations in fluids suggest that there was generally sufficient H2 for Methanocaldococcus growth at Axial but not at Endeavour. Fluids from one vent at Axial (Marker 113) had anomalously high CH4 concentrations and contained various thermal classes of methanogens based on cultivation and mcrA/mrtA analyses. At Endeavour, methanogens were largely undetectable in fluid samples based on cultivation and molecular screens, although abundances of hyperthermophilic heterotrophs were relatively high. Where present, Methanocaldococcus genes were the predominant mcrA/mrtA sequences recovered and comprised ∼0.2–6% of the total archaeal community. Field and coculture data suggest that H2 limitation may be partly ameliorated by H2 syntrophy with hyperthermophilic heterotrophs. These data support our estimated H2 threshold for hyperthermophilic methanogenesis at vents and highlight the need for coupled laboratory and field measurements to constrain microbial distribution and biogeochemical impacts in the deep sea.

Footnotes

  • ↵1To whom correspondence should be addressed. E-mail: jholden{at}microbio.umass.edu.
  • Author contributions: H.C.V., D.A.B., J.A.H., and J.F.H. designed research; H.C.V., D.A.B., J.A.H., E.J.O., K.K.R., L.J.E., A.Y.M., H.V.C., and J.F.H. performed research; H.C.V., D.A.B., J.A.H., M.D.L., and J.F.H. analyzed data; and H.C.V., D.A.B., J.A.H., and J.F.H. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. HQ635140–HQ635763).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1206632109/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Hydrogen-limited growth of methanogens at vents
Helene C. Ver Eecke, David A. Butterfield, Julie A. Huber, Marvin D. Lilley, Eric J. Olson, Kevin K. Roe, Leigh J. Evans, Alexandr Y. Merkel, Holly V. Cantin, James F. Holden
Proceedings of the National Academy of Sciences Aug 2012, 201206632; DOI: 10.1073/pnas.1206632109

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Hydrogen-limited growth of methanogens at vents
Helene C. Ver Eecke, David A. Butterfield, Julie A. Huber, Marvin D. Lilley, Eric J. Olson, Kevin K. Roe, Leigh J. Evans, Alexandr Y. Merkel, Holly V. Cantin, James F. Holden
Proceedings of the National Academy of Sciences Aug 2012, 201206632; DOI: 10.1073/pnas.1206632109
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