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Significant contribution of Archaea to extant biomass in marine subsurface sediments

Abstract

Deep drilling into the marine sea floor has uncovered a vast sedimentary ecosystem of microbial cells1,2. Extrapolation of direct counts of stained microbial cells to the total volume of habitable marine subsurface sediments suggests that between 56 Pg (ref. 1) and 303 Pg (ref. 3) of cellular carbon could be stored in this largely unexplored habitat. From recent studies using various culture-independent techniques, no clear picture has yet emerged as to whether Archaea or Bacteria are more abundant in this extensive ecosystem4,5,6,7. Here we show that in subsurface sediments buried deeper than 1 m in a wide range of oceanographic settings at least 87% of intact polar membrane lipids, biomarkers for the presence of live cells7,8, are attributable to archaeal membranes, suggesting that Archaea constitute a major fraction of the biomass. Results obtained from modified quantitative polymerase chain reaction and slot-blot hybridization protocols support the lipid-based evidence and indicate that these techniques have previously underestimated archaeal biomass. The lipid concentrations are proportional to those of total organic carbon. On the basis of this relationship, we derived an independent estimate of amounts of cellular carbon in the global marine subsurface biosphere. Our estimate of 90 Pg of cellular carbon is consistent, within an order of magnitude, with previous estimates, and underscores the importance of marine subsurface habitats for global biomass budgets.

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Figure 1: Depth profiles of IPLs in marine sediments.
Figure 2: Relative abundance of archaeal 16S rRNA genes to total archaeal and bacterial 16S rRNA genes.
Figure 3: Correlation of concentrations of IPLs and TOC.

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Acknowledgements

Samples for this research were provided by the Integrated Ocean Drilling Program (IODP, expeditions 301 and 311), the Ocean Drilling Program (ODP, legs 201, 204 and 207; sponsored by the US National Science Foundation and participating countries under the Joint Oceanographic Institutions, Inc.), and cruises Sonne SO147, Kaiyo KY04-11, Professor Logatchev TTR15 and Chikyu Shakedown Expedition CK06-06. We thank the participating crews and scientists for sample recovery and data; U. Proske and N. Buchs for assistance with lipid extraction and sample preparation; J. M. Hayes and A. Teske for comments on an earlier version of this manuscript; H. F. Fredricks and F. Schubotz for discussion of data; V. Heuer, A. Schippers and T. Toki for sample donation; B. Kockisch for TOC analysis; and T. Terada and N. Masui for DNA extraction and analyses. This work was supported by Deutsche Forschungsgemeinschaft (through MARUM Center for Marine Environmental Sciences and grant Hi616-4 from the priority program IODP/ODP) and JAMSTEC Multidisciplinary Research Promotion Award 2007 (to Y.M. and F.I.). This is MARUM publication number 0585.

Author Contributions J.S.L., geochemical and lipid analysis, geochemical modelling, method development and paper writing; Y.M. and F.I., DNA extraction and molecular analyses; K.-U.H., study design, paper writing and geochemical modelling. All authors participated in data analysis and interpretation and provided editorial comments on the manuscript.

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Correspondence to Kai-Uwe Hinrichs.

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This file contains Supplementary Methods, Supplementary Figures 1-4, Supplementary Tables 1-5, and additional references. (PDF 512 kb)

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Lipp, J., Morono, Y., Inagaki, F. et al. Significant contribution of Archaea to extant biomass in marine subsurface sediments. Nature 454, 991–994 (2008). https://doi.org/10.1038/nature07174

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