Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Predicted microbial secretomes and their target substrates in marine sediment

Nature Microbiology volume 3, pages 32–37 (2018)Cite this article

Subjects

Abstract

Scientific drilling has identified a biosphere in marine sediments1, which contain many uncultivated microbial groups known only by their DNA sequences2,3,4. Recycling of organic matter in sediments is an important component of biogeochemical cycles because marine sediments are critical for long-term carbon storage5. Turnover of carbon is hypothesized to be driven by the secretion of enzymes by microbial organisms5,6,7, which act to break down macromolecules into constitutive monomers that can be transported into cells. As such, the nature of the microbial secretome often influences the function of a community6. However, the microbial groups involved in this process and the biochemistry they encode is poorly understood. Here, we show that expressed genes from 5 to 159 meters below the seafloor8 (mbsf) encode numerous candidate peptidases and carbohydrate-active enzymes (‘CAZymes’)9 targeted for secretion. The majority (90–99%) were assigned to Bacteria, of which 12% shared the highest sequence similarity with candidate phyla10,11. The remaining putatively secreted proteins shared highest sequence similarity with archaeal and fungal enzymes, which peak in two redox transition zones12. In the shallower redox zone at 30 mbsf, 20% of the transcripts encoding putative secreted peptidases were assigned to lineages7,13,14 of uncultivated Archaea. The target compounds of the predicted secreted proteome show a preference for necromass in the form of microbial cell envelopes as well as plankton and algal detritus. The predicted fungal secreted proteome encodes CAZymes not present in the predicted bacterial or archaeal secreted proteomes, indicating that fungi putatively play a minimal but specialized role in subseafloor carbohydrate recycling.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Classes of expressed ORFs encoding putatively secreted enzymes in subseafloor metatranscriptomes across the tree of life19.
Fig. 2: Relative abundance of expressed ORFs encoding putatively secreted proteins.
Fig. 3: Distributions of expressed ABC transporters for sugars and amino acids/peptides.
Fig. 4: Distribution of CAZy protein classes with sequence similarity to putatively secreted enzymes.

Similar content being viewed by others

References

  1. Kallmeyer, J., Pockalny, R., Adhikari, R., Smith, D. C. & D’Hondt, S. Global distribution of microbial abundance and biomass in subseafloor sediment. Proc. Natl Acad. Sci. USA 109, 16213–16216 (2012).

    Article  CAS  Google Scholar 

  2. Fry, J. C., Parkes, R. J., Cragg, B. A., Weightman, A. J. & Webster, G. Prokaryotic biodiversity and activity in the deep subseafloor biosphere. FEMS Microb. Ecol. 66, 181–196 (2008).

    Article  CAS  Google Scholar 

  3. 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).

    Article  CAS  Google Scholar 

  4. Inagaki, F. et al. Biogeographical distribution and diversity of microbes in methane hydrate-bearing deep marine sediments, on the Pacific Ocean Margin. Proc. Natl Acad. Sci. USA 103, 2815–2820 (2006).

    Article  CAS  Google Scholar 

  5. Arndt, S. et al. Quantifying the degradation of organic matter in marine sediments: a review and synthesis. Earth Sci. Rev. 123, 53–86 (2013).

    Article  CAS  Google Scholar 

  6. Arnosti, C. Microbial extracellular enzymes and the marine carbon cycle. Ann. Rev. Mar. Sci. 3, 401–425 (2011).

    Article  Google Scholar 

  7. Lloyd, K. G. et al. Predominant archaea in marine sediments degrade detrital proteins. Nature 496, 215–218 (2013).

    Article  CAS  Google Scholar 

  8. Orsi, W. D., Edgcomb, V. P., Christman, G. D. & Biddle, J. F. Gene expression in the deep biosphere. Nature 499, 205–208 (2013).

    Article  CAS  Google Scholar 

  9. Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P. M. & Henrissat, B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42, D490–D495 (2014).

    Article  CAS  Google Scholar 

  10. Brown, C. T. et al. Unusual biology across a group comprising more than 15% of domain Bacteria. Nature 523, 208–211 (2015).

  11. Rinke, C. et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature 499, 431–437 (2013).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  13. Evans, P. N. et al. Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics. Science 350, 434–438 (2015).

    Article  CAS  Google Scholar 

  14. Baker, B. J. et al. Genomic inference of the metabolism of cosmopolitan subsurface Archaea, Hadesarchaea. Nat. Microbiol. 1, 16002 (2016).

    Article  CAS  Google Scholar 

  15. Petersen, T. N., Brunak, S., von Heijne, G. & Nielsen, H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8, 785–786 (2011).

    Article  CAS  Google Scholar 

  16. Overbeek, R. et al. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids. Res. 42, D206–D214 (2014).

    Article  CAS  Google Scholar 

  17. Wrighton, K. C. et al. Fermentation, hydrogen, and sulfur metabolism in multiple uncultivated bacterial phyla. Science 337, 1661–1665 (2012).

    Article  CAS  Google Scholar 

  18. Nobu, M. K. et al. Phylogeny and physiology of candidate phylum ‘Atribacteria’ (OP9/JS1) inferred from cultivation-independent genomics. ISME J. 10, 273–286 (2016).

    Article  CAS  Google Scholar 

  19. Hug, L. A. et al. A new view of the tree of life. Nat. Microbiol. 1, 16048 (2016).

    Article  CAS  Google Scholar 

  20. Lomstein, B. A., Langerhuus, A. T., D’Hondt, S., Jorgensen, B. B. & Spivack, A. J. Endospore abundance, microbial growth and necromass turnover in deep sub-seafloor sediment. Nature 484, 101–104 (2012).

    Article  CAS  Google Scholar 

  21. Canfield, D. E. Factors influencing organic carbon preservation in marine sediments. Chem. Geol. 114, 315–329 (1994).

    Article  CAS  Google Scholar 

  22. Ferry, J. G. & Wolfe, R. S. Anaerobic degradation of benzoate to methane by a microbial consortium. Arch. Microbiol. 107, 33–40 (1976).

    Article  CAS  Google Scholar 

  23. Vollmer, W., Blanot, D. & de Pedro, M. A. Peptidoglycan structure and architecture. FEMS Microbiol. Rev. 32, 149–167 (2008).

    Article  CAS  Google Scholar 

  24. Lazar, C. S. et al. Genomic evidence for distinct carbon substrate preferences and ecological niches of Bathyarchaeota in estuarine sediments. Environ Microbiol. 18, 1200–1211 (2016).

    Article  CAS  Google Scholar 

  25. Artzi, L., Bayer, E. A. & Morais, S. Cellulosomes: bacterial nanomachines for dismantling plant polysaccharides. Nat. Rev. Microbiol. 15, 83–95 (2017).

    Article  CAS  Google Scholar 

  26. Orsi, W., Biddle, J. F. & Edgcomb, V. Deep sequencing of subseafloor eukaryotic rRNA reveals active Fungi across marine subsurface provinces. PloS ONE 8, e56335 (2013).

    Article  CAS  Google Scholar 

  27. Visweswaran, G. R., Dijkstra, B. W. & Kok, J. Murein and pseudomurein cell wall binding domains of bacteria and archaea-a comparative view. Appl. Microbiol. Biotechnol. 92, 921–928 (2011).

    Article  CAS  Google Scholar 

  28. Hasegawa, S. & Nordin, J. H. Enzymes that hydrolyze fungal cell wall polysaccharides. I. Purification and properties of an endo-α-d-(1–3)-glucanase from Trichoderma. J Biol. Chem. 244, 5460–5470 (1969).

    CAS  PubMed  Google Scholar 

  29. Rho, M., Tang, H. & Ye, Y. FragGeneScan: predicting genes in short and error-prone reads. Nucleic Acids Res. 38, e191 (2010).

    Article  Google Scholar 

  30. Hansen, G. & Hilgenfeld, R. Architechture and regulation of HtrA-family proteins involved in protein quality control and stress response. Cell. Mol. Life Sci. 70, 761–765 (2012).

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the Deutsche Forschungsgemeinschaft (DFG) through Project OR 417/1-1 (W.D.O.), and also by Ludwig-Maximilians Universität München Junior Researcher Fund (W.D.O.). T.A.R. is supported by a Royal Society University Research Fellowship. We thank O. Voigt (LMU Munich) for his help in installing the stand-alone (command line) implementation of SignalP.

Author information

Author notes

  1. Warren R. Francis

    Present address: Department of Biology, University of Southern Denmark, DK-5230, Odense, Denmark

Authors and Affiliations

  1. Department of Earth and Environmental Sciences, Paleontology & Geobiology, Ludwig-Maximilians-Universität München, 80333, Munich, Germany

    William D. Orsi & Warren R. Francis

  2. GeoBio-CenterLMU, Ludwig-Maximilians-Universität München, 80333, Munich, Germany

    William D. Orsi

  3. Biosciences, College of Life and Environmental Sciences, University of Exeter, Exeter, EX4 4QD, UK

    Thomas A. Richards

Authors
  1. William D. Orsi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Thomas A. Richards
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Warren R. Francis
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

W.D.O. and T.A.R. conceived the idea for the study, W.D.O. wrote the paper; W.D.O. and W.R.F. analysed data, W.R.F. developed analytical tools. All authors participated in data interpretation and provided editorial comments on the manuscript.

Corresponding author

Correspondence to William D. Orsi.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Supplementary Information

Supplementary Tables 1 and 2, Supplementary Figure 1.

Life Sciences Reporting Summary

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Orsi, W.D., Richards, T.A. & Francis, W.R. Predicted microbial secretomes and their target substrates in marine sediment. Nat Microbiol 3, 32–37 (2018). https://doi.org/10.1038/s41564-017-0047-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41564-017-0047-9

This article is cited by

Search

Advanced search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Microbiology