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Archaea in metazoan diets: implications for food webs and biogeochemical cycling

Thurber, Andrew R. and Levin, Lisa A. and Orphan, Victoria J. and Marlow, Jeffrey J. (2012) Archaea in metazoan diets: implications for food webs and biogeochemical cycling. ISME Journal, 6 (8). pp. 1602-1612. ISSN 1751-7362. PMCID PMC3400411. https://resolver.caltech.edu/CaltechAUTHORS:20120817-140759648

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Abstract

Although the importance of trophic linkages, including ‘top-down forcing’, on energy flow and ecosystem productivity is recognized, the influence of metazoan grazing on Archaea and the biogeochemical processes that they mediate is unknown. Here, we test if: (1) Archaea provide a food source sufficient to allow metazoan fauna to complete their life cycle; (2) neutral lipid biomarkers (including crocetane) can be used to identify Archaea consumers; and (3) archaeal aggregates are a dietary source for methane seep metazoans. In the laboratory, we demonstrated that a dorvilleid polychaete, Ophryotrocha labronica, can complete its life cycle on two strains of Euryarchaeota with the same growth rate as when fed bacterial and eukaryotic food. Archaea were therefore confirmed as a digestible and nutritious food source sufficient to sustain metazoan populations. Both strains of Euryarchaeota used as food sources had unique lipids that were not incorporated into O. labronica tissues. At methane seeps, sulfate-reducing bacteria that form aggregations and live syntrophically with anaerobic-methane oxidizing Archaea contain isotopically and structurally unique fatty acids (FAs). These biomarkers were incorporated into tissues of an endolithofaunal dorvilleid polychaete species from Costa Rica (mean bulk δ^(13)C=−92±4‰; polar lipids −116‰) documenting consumption of archaeal-bacterial aggregates. FA composition of additional soft-sediment methane seep species from Oregon and California provided evidence that consumption of archaeal-bacterial aggregates is widespread at methane seeps. This work is the first to show that Archaea are consumed by heterotrophic metazoans, a trophic process we coin as ‘archivory’.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1038/ismej.2012.16DOIArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3400411/PubMed CentralArticle
ORCID:
AuthorORCID
Levin, Lisa A.0000-0002-2858-8622
Orphan, Victoria J.0000-0002-5374-6178
Additional Information:© 2012 International Society for Microbial Ecology. Received 29 July 2011; revised 2 February 2012; accepted 2 February 2012; published online 8 March 2012. We are indebted to the Captains, Crew, Alvin group and Science parties from RV Atlantis legs 15-9; 15-11; 15-44; and 15-59. Guillermo Mendoza, Jennifer Gonzalez and Drs Brigitte Ebbe, Ken Halanych, Ray Lee and Greg Rouse all helped tremendously at sea with sorting and identification of the dorvilleid species. Dr Shana Goffredi kindly checked for archaeal symbionts within the Costa Rican Dorvilleid. Dr William Gerwick provided access to the analytical instrumentation necessary to carry out this research and Cameron Coates, Jo Nunnery and Tak Suyama were always present to help trouble shoot analytical problems. Two anonymous reviewers, and Drs G Rouse and Lihini Aluwihare provided helpful comments on an earlier version of this manuscript. This research was supported by NSF Grants OCE 0425317, OCE 0826254 and OCE-0939557, and grant UAF-050141 from the West Coast National Undersea Research Center to LA Levin, OCE-0939559 and OCE-0825791 grants to VJ Orphan and a UC Marine Council award to W Gerwick and LA Levin, in addition to the Michael M Mullin Memorial fellowship, Sidney E Frank Foundation Fellowship, UC Marine Council CEQI Fellowship and the graduate office of Scripps Institution of Oceanography’s support of AR Thurber.
Funders:
Funding AgencyGrant Number
NSFOCE 0425317
NSFOCE 0826254
NSFOCE-0939557
West Coast National Undersea Research CenterUAF-050141
NSFOCE-0939559
NSFOCE-0825791
UC Marine CouncilUNSPECIFIED
Michael M. Mullin Memorial fellowshipUNSPECIFIED
Sidney E. Frank Foundation FellowshipUNSPECIFIED
Scripps Institution of OceanographyUNSPECIFIED
Subject Keywords:anaerobic methane oxidation; archivory; authigenic carbonate; biomarker; microbial–metazoan interactions; cold seep
Issue or Number:8
PubMed Central ID:PMC3400411
Record Number:CaltechAUTHORS:20120817-140759648
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20120817-140759648
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:33305
Collection:CaltechAUTHORS
Deposited By: Jason Perez
Deposited On:17 Aug 2012 22:06
Last Modified:15 Apr 2020 17:48

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