Endospore abundance, microbial growth and necromass turnover in deep sub-seafloor sediment

Abstract

Two decades of scientific ocean drilling have demonstrated widespread microbial life in deep sub-seafloor sediment, and surprisingly high microbial-cell numbers. Despite the ubiquity of life in the deep biosphere, the large community sizes and the low energy fluxes in this vast buried ecosystem are not yet understood1,2. It is not known whether organisms of the deep biosphere are specifically adapted to extremely low energy fluxes or whether most of the observed cells are in a dormant, spore-like state3. Here we apply a new approachthe d:l-amino-acid modelto quantify the distributions and turnover times of living microbial biomass, endospores and microbial necromass, as well as to determine their role in the sub-seafloor carbon budget. The approach combines sensitive analyses of unique bacterial markers (muramic acid and D-amino acids) and the bacterial endospore marker, dipicolinic acid, with racemization dynamics of stereo-isomeric amino acids. Endospores are as abundant as vegetative cells and microbial activity is extremely low, leading to microbial biomass turnover times of hundreds to thousands of years. We infer from model calculations that biomass production is sustained by organic carbon deposited from the surface photosynthetic world millions of years ago and that microbial necromass is recycled over timescales of hundreds of thousands of years.

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Figure 1: Profiles of AODCs and estimated endospore numbers on the Peruvian continental shelf (sites 1227 and 1229) and in the Trench in Peru (site 1230).
Figure 2: d:l -Asp model.
Figure 3: d:l -model estimates of microbial biomass turnover times, necromass turnover times and carbon-oxidation rates.

References

  1. 1

    D’Hondt, S. et al. Distributions of microbial activities in deep subseafloor sediments. Science 306, 2216–2221 (2004)

    ADS  Article  Google Scholar 

  2. 2

    Jørgensen, B. B. & D’Hondt, S. A starving majority deep beneath the seafloor. Science 314, 932–934 (2006)

    Article  Google Scholar 

  3. 3

    Schrenk, M. O., Huber, J. A. & Edwards, K. J. Microbial provinces in the subseafloor. Annu. Rev. Mar. Sci. 2, 279–304 (2010)

    ADS  Article  Google Scholar 

  4. 4

    Jørgensen, B. B., D’Hondt, S., Miller, D. J., eds. Leg 201 synthesis: controls on microbial communities in deeply buried sediments. Proc. ODP Sci. Res. 1–45 (2006)

  5. 5

    Lipp, J. S., Morono, Y., Inagaki, F. & Hinrichs, K. U. Significant contribution of Archaea to extant biomass in marine subsurface sediments. Nature 454, 991–994 (2008)

    ADS  CAS  Article  Google Scholar 

  6. 6

    Schippers, A. et al. Prokaryotic cells of the deep sub-seafloor biosphere identified as living bacteria. Nature 433, 861–864 (2005)

    ADS  CAS  Article  Google Scholar 

  7. 7

    Biddle, J. F., Fitz-Gibbon, S., Schuster, S. C., Brenchley, J. E. & House, C. H. Metagenomic signatures of the Peru Margin subseafloor biosphere show a genetically distinct environment. Proc. Natl Acad. Sci. USA 105, 10583–10588 (2008)

    ADS  CAS  Article  Google Scholar 

  8. 8

    Fichtel, J., Koster, J., Rullkotter, J. & Sass, H. Spore dipicolinic acid contents used for estimating the number of endospores in sediments. FEMS Microbiol. Ecol. 61, 522–532 (2007)

    CAS  Article  Google Scholar 

  9. 9

    Madigan, M. T. & Martinko, J. M. Brock Biology of Microorganisms 11th edn (Prentice Hall, 2006)

    Google Scholar 

  10. 10

    Schichnes, D., Nemson, J. A. & Ruzin, S. E. Fluorescent staining method for bacterial endospores. Microscope 54, 91–93 (2006)

    CAS  Google Scholar 

  11. 11

    Hsieh, L. K. & Vary, J. C. Germination and peptidoglycan solubilization in Bacillus megaterium spores. J. Bacteriol. 123, 463–470 (1975)

    CAS  PubMed  PubMed Central  Google Scholar 

  12. 12

    Whitman, W. B., Coleman, D. C. & Wiebe, W. J. Prokaryotes: the unseen majority. Proc. Natl Acad. Sci. USA 95, 6578–6583 (1998)

    ADS  CAS  Article  Google Scholar 

  13. 13

    Parkes, R. J. et al. A quantitative study of microbial decomposition of biopolymers in Recent sediments from the Peru Margin. Mar. Geol. 113, 55–66 (1993)

    ADS  CAS  Article  Google Scholar 

  14. 14

    Hartgers, W. A. et al. Evidence for only minor contributions from bacteria sedimentary carbon. Nature 369, 224–227 (1994)

    ADS  CAS  Article  Google Scholar 

  15. 15

    Schleifer, K. H. & Kandler, O. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol. Rev. 36, 407–477 (1972)

    CAS  PubMed  PubMed Central  Google Scholar 

  16. 16

    Bada, J. L. Racemization of amino acids in nature. Interdiscip. Sci. Rev. 7, 30–46 (1982)

    CAS  Article  Google Scholar 

  17. 17

    Takano, Y., Sato, R., Kaneko, T., Kobayashi, K. & Marumo, K. Biological origin for amino acids in a deep subterranean hydrothermal vent, Toyoha mine, Hokkaido, Japan. Org. Geochem. 34, 1491–1496 (2003)

    CAS  Article  Google Scholar 

  18. 18

    Er, C., Nagy, B. & Riser, E. C. Analysis of muramic acid in holocene microbial environments by gas chromatography, electrone impact, and fast atom bombardment mass spectrometry. Geomicrobiol. J. 5, 57–78 (1987)

    CAS  Article  Google Scholar 

  19. 19

    Heijnen, J. J. & van Dijken, J. P. In search of a thermodynamic description of biomass yields for the chemotrophic growth of microorganisms. Biotechnol. Bioeng. 39, 833–858 (1992)

    CAS  Article  Google Scholar 

  20. 20

    Leloup, J. et al. Sulfate-reducing bacteria in marine sediment (Aarhus Bay, Denmark): abundance and diversity related to geochemical zonation. Environ. Microbiol. 11, 1278–1291 (2009)

    CAS  Article  Google Scholar 

  21. 21

    Lomstein, B., Aa, Jørgensen, B. B., Schubert, C. J. & Niggemann, J. Amino acid biogeo- and stereochemistry in coastal Chilean sediments. Geochim. Cosmochim. Acta 70, 2970–2989 (2006)

    ADS  CAS  Article  Google Scholar 

  22. 22

    Lomstein, B., Aa, Niggemann, J., Jørgensen, B. B. & Langerhuus, A. T. Accumulation of prokaryotic remains during organic matter diagenesis in surface sediments off Peru. Limnol. Oceanogr. 54, 1139–1151 (2009)

    ADS  CAS  Article  Google Scholar 

  23. 23

    Shipboard Scientific Party . Leg 201 summary Proc. ODP Init. Rep. 201, 1–81 (2003)

    Google Scholar 

  24. 24

    Lomstein, B. A. & Jøgensen, B. B. Pre column liquid chromatographic determination of dipicolinic acid from bacterial endospores. Limnol. Oceanogr. Methods (in the press)

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Acknowledgements

Bacterial cultures were provided by H. Cypionka. We thank members of the Leg 201 cruise for assistance in obtaining and processing samples. This research used samples and data provided by the Ocean Drilling Program (http://www-odp.tamu.edu/publications/201_IR/201ir.htm). The ODP was sponsored by the US National Science Foundation and participating countries under the management of Joint Oceanographic Institutions. We thank R. O. Holm and L. Poulsen for technical assistance and guidance with high-performance liquid chromatographic analyses. We thank D. L. Valentine for comments and suggestions to improve the manuscript. Financial support was provided by the Max Planck Society, the Danish National Research Foundation, the Danish National Science Research Council, the Danish Agency for Science, Technology and Innovation, the Faculty of Science and Technology at the University of Aarhus, and the US National Science Foundation.

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A.J.S. and B.Aa.L. developed ideas and performed the project planning. B.Aa.L. performed the analysis and data processing of total organic carbon, amino acid composition, dipicolinic acid and d- and l-amino acids. A.T.L. performed the muramic acid analysis and data processing. B.B.J. developed the mathematical formulation of the d:l model together with A.T.L. and B.Aa.L. Estimation of sulphate reduction rates from sulphate profiles was carried out by B.B.J and S.D. The manuscript was written by B.Aa.L., AT.L and B.B.J.. All authors participated in early stages of data interpretation and provided editorial comments on the manuscript.

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Correspondence to Bente Aa. Lomstein.

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The authors declare no competing financial interests.

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Lomstein, B., Langerhuus, A., D’Hondt, S. et al. Endospore abundance, microbial growth and necromass turnover in deep sub-seafloor sediment. Nature 484, 101–104 (2012). https://doi.org/10.1038/nature10905

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