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Sedimentary membrane lipids recycled by deep-sea benthic archaea

Nature Geoscience volume 3, pages 858–861 (2010)Cite this article

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Abstract

Deep-sea sediments harbour a vast biosphere. Archaea—one of the three domains of life1—are prevalent in marine environments2,3,4,5, and comprise a significant fraction of the biomass in marine sediments6. Archaeal membranes are well characterized, and are comprised of a glycerol backbone and a nonpolar isoprenoid chain. However, the ecology of sedimentary archaea remains elusive, because it is difficult to grow them in the laboratory. Here, we trace the fate of 13C-labelled glucose added to marine sediments in Sagami Bay, Japan, to determine the in situ mechanisms of membrane synthesis. Following the addition of labelled glucose to sediment samples collected in the region, we placed the cores on the sea floor and sampled them after 9 and 405 days. We found that the 13C was incorporated into the glycerol backbone of archaeal membranes; 13C was apparent after 9 days of incubation, but most pronounced after 405 days. However, the isoprenoid chain of the membranes remained unlabelled. On the basis of the differential uptake of 13C, we suggest that the glycerol unit is synthesized de novo, whereas the isoprenoid unit is synthesized from relic archaeal membranes and detritus, because of the prevalence of these compounds in marine sediments. We therefore suggest that some benthic archaea build their membranes by recycling sedimentary organic compounds.

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Figure 1: Distribution of benthic archaeal lipids and their carbon isotopic compositions during the in situ 13C-tracer experiments lasting 405 days.
Figure 2: Carbon isotopic compositions of δ13Ccaldarchaeol, δ13Ccrenarchaeol, δ13Cbiphytane and δ13C2,3-sn-glycerol during the course of the experiment.
Figure 3: Abundance of archaeal lipids and phylogeny of the benthic archaeal community.

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Acknowledgements

The authors thank T. Terada (Marine Works Japan), the shipboard scientists for their experimental and logistic support during cruises NT06-04,-05,-22 and NT08-02 by R/V Natsushima and for providing bathymetric data. This research was supported in part by a grant from the Japan Society for the Promotion of Science, Grant-in-Aid for Creative Scientific Research (19GS0211 & 22684030) and the internship program between Japan and Germany (FY2009).

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Authors and Affiliations

  1. Institute of Biogeosciences, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima, Yokosuka 237-0061, Japan

    Yoshinori Takano, Yoshito Chikaraishi, Nanako O. Ogawa, Hidetaka Nomaki, Hiroshi Kitazato & Naohiko Ohkouchi

  2. Kochi Institute for Core Sample Research, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Monobe B200, Nangoku, Kochi 783-8502, Japan

    Yuki Morono & Fumio Inagaki

  3. Department of Geosciences and MARUM Center for Marine Environmental Sciences, University of Bremen, D-28359 Bremen, Germany

    Kai-Uwe Hinrichs

  4. Department of Environmental Science and Technology, Tokyo Institute of Technology, 4259 Nagatsuda, Midori-ku, Yokohama, Kanagawa 226-8502, Japan

    Naohiko Ohkouchi

  5. Department of Earth and Planetary Sciences, University of Tokyo, 7-3-1 Hongo, Tokyo 113-0033, Japan

    Naohiko Ohkouchi

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  1. Yoshinori Takano
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Contributions

Y.T. carried out the lipids analysis and wrote the paper; Y.C. and N.O.O. supported the carbon isotope standard reagents and isotope ratio mass spectrometry analysis; H.N. and H.K. supported the 13C-substrate set-up, in situ deployment of the chamber, and core processing during cruises NT06-04, -05, -22 and NT08-02; Y.M. and F.I. supported phylogenic molecular analysis of 16S rRNA and qPCR; K-U.H. contributed to technical aspects and was involved in the study design; Y.T. and N.O. contributed to this study and all authors discussed the results and commented on the manuscript.

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Correspondence to Yoshinori Takano.

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Takano, Y., Chikaraishi, Y., Ogawa, N. et al. Sedimentary membrane lipids recycled by deep-sea benthic archaea. Nature Geosci 3, 858–861 (2010). https://doi.org/10.1038/ngeo983

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