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Predominant archaea in marine sediments degrade detrital proteins

Nature volume 496, pages 215–218 (2013)Cite this article

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Abstract

Half of the microbial cells in the Earth’s oceans are found in sediments1. Many of these cells are members of the Archaea2, single-celled prokaryotes in a domain of life separate from Bacteria and Eukaryota. However, most of these archaea lack cultured representatives, leaving their physiologies and placement on the tree of life uncertain. Here we show that the uncultured miscellaneous crenarchaeotal group (MCG) and marine benthic group-D (MBG-D) are among the most numerous archaea in the marine sub-sea floor. Single-cell genomic sequencing of one cell of MCG and three cells of MBG-D indicated that they form new branches basal to the archaeal phyla Thaumarchaeota3 and Aigarchaeota4, for MCG, and the order Thermoplasmatales, for MBG-D. All four cells encoded extracellular protein-degrading enzymes such as gingipain and clostripain that are known to be effective in environments chemically similar to marine sediments. Furthermore, we found these two types of peptidase to be abundant and active in marine sediments, indicating that uncultured archaea may have a previously undiscovered role in protein remineralization in anoxic marine sediments.

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Figure 1: Global marine occurrence of miscellaneous crenarchaeotal group (MCG) and marine benthic group D (MBG-D).
Figure 2: Evolutionary placement of SAGs.
Figure 3: Proposed protein degradation pathway for MCG_E09 (a) and MBG-D_N05 and MBG-D_F20 (b), and gene architecture for selected extracellular peptidases (c, d).

Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Data deposits

This whole-genome shotgun project has been deposited at DDBJ/EMBL/GenBank as Thaumarchaeota archaeon SCGC AB-539-E09 (accession number ALXK00000000), Thermoplasmatales archaeon SCGC AB-539-C06 (AOSH00000000), Thermoplasmatales archaeon SCGC AB-539-N05 (ALXL00000000) and Thermoplasmatales archaeon SCGC AB-540-F20 (AOSI00000000).

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Acknowledgements

The authors thank the captain and crew of the R/V Tyra for sampling; T. B. Søgaard, A. Stentebjerg and B. Poulsen for technical work; F. Löffler for laboratory space; and D. Kirchman and S. Hallam for sharing their unpublished metagenomic data sets. This work was funded by the Danish National Research Foundation, the German Max Planck Society, NSF Center for Dark Energy Biosphere Investigations NSF-157595 (K.G.L.), The Danish Council for Independent Research–Natural Sciences (D.G.P.), the Villum Kann Rasmussen Foundation, an EU Marie Curie fellowship (M.A.L.), the German Research Foundation (S.L.) and the USA National Science Foundation awards EF-826924, OCE-821374 and OCE-1019242 (R.S.).

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Author notes

  1. Karen G. Lloyd and Lars Schreiber: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Bioscience, Center for Geomicrobiology, Aarhus University, Aarhus 8000, Denmark,

    Karen G. Lloyd, Lars Schreiber, Dorthe G. Petersen, Kasper U. Kjeldsen, Mark A. Lever, Andreas Schramm & Bo Barker Jørgensen

  2. University of Tennessee, Knoxville, 37996, Tennessee, USA

    Karen G. Lloyd & Andrew D. Steen

  3. Bigelow Laboratory for Ocean Sciences, East Boothbay, 04544, Maine, USA

    Ramunas Stepanauskas

  4. Ribocon GmbH, Bremen 28359, Germany,

    Michael Richter

  5. Max Planck Institute for Marine Microbiology, Bremen 28359, Germany,

    Sara Kleindienst & Sabine Lenk

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Contributions

K.G.L., L.S., D.G.P., K.U.K., R.S., A.S. and B.B.J. worked together to design experiment and develop the method for single cell sorting from sediments. K.G.L. wrote the main paper and developed the protein degradation hypothesis. L.S. wrote the Supplementary Information, designed and performed bioinformatic analyses. K.G.L. and L.S. performed phylogenetic tests. K.G.L. and D.G.P. reconstructed metabolic pathways with SAG genes. R.S. performed cell sorting and amplification. S.K., S.L., D.G.P. and L.S. developed protocols for cell separation from sediments. K.U.K. performed and analysed 16S rRNA gene amplicon sequencing; M.A.L., L.S. and K.G.L. performed quantitative PCR; A.D.S. performed enzyme activity measurements; and M.R. gave bioinformatic support and added quality control tests. A.S. and B.B.J. obtained the major funding for this work. All co-authors commented on and provided substantial edits to the manuscript.

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Correspondence to Karen G. Lloyd.

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Supplementary Information

This file contains Supplementary Materials and Methods, Supplementary Tables 1-7 and 9-12 (see separate file for Supplementary Table 8), Supplementary Figures 1-10 and additional references. (PDF 1842 kb)

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Lloyd, K., Schreiber, L., Petersen, D. et al. Predominant archaea in marine sediments degrade detrital proteins. Nature 496, 215–218 (2013). https://doi.org/10.1038/nature12033

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