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Predicted microbial secretomes and their target substrates in marine sediment

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

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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.

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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.

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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.

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  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

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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.

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Correspondence to William D. Orsi.

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Supplementary Tables 1 and 2, Supplementary Figure 1.

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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

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