Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru

Jennifer F. Biddle, Julius S. Lipp, Mark A. Lever, Karen G. Lloyd, Ketil B. Sørensen, Rika Anderson, Helen F. Fredricks, Marcus Elvert, Timothy J. Kelly, Daniel P. Schrag, Mitchell L. Sogin, Jean E. Brenchley, Andreas Teske, Christopher H. House, Kai Uwe Hinrichs

Research output: Contribution to journalArticle

466 Citations (Scopus)

Abstract

Studies of deeply buried, sedimentary microbial communities and associated biogeochemical processes during Ocean Drilling Program Leg 201 showed elevated prokaryotic cell numbers in sediment layers where methane is consumed anaerobically at the expense of sulfate. Here, we show that extractable archaeal rRNA, selecting only for active community members in these ecosystems, is dominated by sequences of uncultivated Archaea affiliated with the Marine Benthic Group B and the Miscellaneous Crenarchaeotal Group, whereas known methanotrophic Archaea are not detectable. Carbon flow reconstructions based on stable isotopic compositions of whole archaeal cells, intact archaeal membrane lipids, and other sedimentary carbon pools indicate that these Archaea assimilate sedimentary organic compounds other than methane even though methanotrophy accounts for a major fraction of carbon cycled in these ecosystems. Oxidation of methane by members of Marine Benthic Group B and the Miscellaneous Crenarchaeotal Group without assimilation of methane-carbon provides a plausible explanation. Maintenance energies of these subsurface communities appear to be orders of magnitude lower than minimum values known from laboratory observations, and ecosystem-level carbon budgets suggest that community turnover times are on the order of 100-2,000 years. Our study provides clues about the metabolic functionality of two cosmopolitan groups of uncultured Archaea.

Original languageEnglish (US)
Pages (from-to)3846-3851
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume103
Issue number10
DOIs
StatePublished - Mar 7 2006

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Peru
Archaea
Ecosystem
Methane
Carbon
Prokaryotic Cells
Budgets
Membrane Lipids
Oceans and Seas
Sulfates
Leg
Cell Count
Maintenance

All Science Journal Classification (ASJC) codes

  • General

Cite this

Biddle, J. F., Lipp, J. S., Lever, M. A., Lloyd, K. G., Sørensen, K. B., Anderson, R., ... Hinrichs, K. U. (2006). Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru. Proceedings of the National Academy of Sciences of the United States of America, 103(10), 3846-3851. https://doi.org/10.1073/pnas.0600035103
Biddle, Jennifer F. ; Lipp, Julius S. ; Lever, Mark A. ; Lloyd, Karen G. ; Sørensen, Ketil B. ; Anderson, Rika ; Fredricks, Helen F. ; Elvert, Marcus ; Kelly, Timothy J. ; Schrag, Daniel P. ; Sogin, Mitchell L. ; Brenchley, Jean E. ; Teske, Andreas ; House, Christopher H. ; Hinrichs, Kai Uwe. / Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru. In: Proceedings of the National Academy of Sciences of the United States of America. 2006 ; Vol. 103, No. 10. pp. 3846-3851.
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abstract = "Studies of deeply buried, sedimentary microbial communities and associated biogeochemical processes during Ocean Drilling Program Leg 201 showed elevated prokaryotic cell numbers in sediment layers where methane is consumed anaerobically at the expense of sulfate. Here, we show that extractable archaeal rRNA, selecting only for active community members in these ecosystems, is dominated by sequences of uncultivated Archaea affiliated with the Marine Benthic Group B and the Miscellaneous Crenarchaeotal Group, whereas known methanotrophic Archaea are not detectable. Carbon flow reconstructions based on stable isotopic compositions of whole archaeal cells, intact archaeal membrane lipids, and other sedimentary carbon pools indicate that these Archaea assimilate sedimentary organic compounds other than methane even though methanotrophy accounts for a major fraction of carbon cycled in these ecosystems. Oxidation of methane by members of Marine Benthic Group B and the Miscellaneous Crenarchaeotal Group without assimilation of methane-carbon provides a plausible explanation. Maintenance energies of these subsurface communities appear to be orders of magnitude lower than minimum values known from laboratory observations, and ecosystem-level carbon budgets suggest that community turnover times are on the order of 100-2,000 years. Our study provides clues about the metabolic functionality of two cosmopolitan groups of uncultured Archaea.",
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Biddle, JF, Lipp, JS, Lever, MA, Lloyd, KG, Sørensen, KB, Anderson, R, Fredricks, HF, Elvert, M, Kelly, TJ, Schrag, DP, Sogin, ML, Brenchley, JE, Teske, A, House, CH & Hinrichs, KU 2006, 'Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru', Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 10, pp. 3846-3851. https://doi.org/10.1073/pnas.0600035103

Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru. / Biddle, Jennifer F.; Lipp, Julius S.; Lever, Mark A.; Lloyd, Karen G.; Sørensen, Ketil B.; Anderson, Rika; Fredricks, Helen F.; Elvert, Marcus; Kelly, Timothy J.; Schrag, Daniel P.; Sogin, Mitchell L.; Brenchley, Jean E.; Teske, Andreas; House, Christopher H.; Hinrichs, Kai Uwe.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 103, No. 10, 07.03.2006, p. 3846-3851.

Research output: Contribution to journalArticle

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T1 - Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru

AU - Biddle, Jennifer F.

AU - Lipp, Julius S.

AU - Lever, Mark A.

AU - Lloyd, Karen G.

AU - Sørensen, Ketil B.

AU - Anderson, Rika

AU - Fredricks, Helen F.

AU - Elvert, Marcus

AU - Kelly, Timothy J.

AU - Schrag, Daniel P.

AU - Sogin, Mitchell L.

AU - Brenchley, Jean E.

AU - Teske, Andreas

AU - House, Christopher H.

AU - Hinrichs, Kai Uwe

PY - 2006/3/7

Y1 - 2006/3/7

N2 - Studies of deeply buried, sedimentary microbial communities and associated biogeochemical processes during Ocean Drilling Program Leg 201 showed elevated prokaryotic cell numbers in sediment layers where methane is consumed anaerobically at the expense of sulfate. Here, we show that extractable archaeal rRNA, selecting only for active community members in these ecosystems, is dominated by sequences of uncultivated Archaea affiliated with the Marine Benthic Group B and the Miscellaneous Crenarchaeotal Group, whereas known methanotrophic Archaea are not detectable. Carbon flow reconstructions based on stable isotopic compositions of whole archaeal cells, intact archaeal membrane lipids, and other sedimentary carbon pools indicate that these Archaea assimilate sedimentary organic compounds other than methane even though methanotrophy accounts for a major fraction of carbon cycled in these ecosystems. Oxidation of methane by members of Marine Benthic Group B and the Miscellaneous Crenarchaeotal Group without assimilation of methane-carbon provides a plausible explanation. Maintenance energies of these subsurface communities appear to be orders of magnitude lower than minimum values known from laboratory observations, and ecosystem-level carbon budgets suggest that community turnover times are on the order of 100-2,000 years. Our study provides clues about the metabolic functionality of two cosmopolitan groups of uncultured Archaea.

AB - Studies of deeply buried, sedimentary microbial communities and associated biogeochemical processes during Ocean Drilling Program Leg 201 showed elevated prokaryotic cell numbers in sediment layers where methane is consumed anaerobically at the expense of sulfate. Here, we show that extractable archaeal rRNA, selecting only for active community members in these ecosystems, is dominated by sequences of uncultivated Archaea affiliated with the Marine Benthic Group B and the Miscellaneous Crenarchaeotal Group, whereas known methanotrophic Archaea are not detectable. Carbon flow reconstructions based on stable isotopic compositions of whole archaeal cells, intact archaeal membrane lipids, and other sedimentary carbon pools indicate that these Archaea assimilate sedimentary organic compounds other than methane even though methanotrophy accounts for a major fraction of carbon cycled in these ecosystems. Oxidation of methane by members of Marine Benthic Group B and the Miscellaneous Crenarchaeotal Group without assimilation of methane-carbon provides a plausible explanation. Maintenance energies of these subsurface communities appear to be orders of magnitude lower than minimum values known from laboratory observations, and ecosystem-level carbon budgets suggest that community turnover times are on the order of 100-2,000 years. Our study provides clues about the metabolic functionality of two cosmopolitan groups of uncultured Archaea.

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