Predominant archaea in marine sediments degrade detrital proteins

Journal name:
Nature
Volume:
496,
Pages:
215–218
Date published:
DOI:
doi:10.1038/nature12033
Received
Accepted
Published online

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.

At a glance

Figures

  1. Global marine occurrence of miscellaneous crenarchaeotal group (MCG) and marine benthic group D (MBG-D).
    Figure 1: Global marine occurrence of miscellaneous crenarchaeotal group (MCG) and marine benthic group D (MBG-D).

    Relative abundance of 16S rRNA gene sequences in clone libraries from marine sediments for MCG (red) and MBG-D (blue). For some (crosses), sequence abundance information was unavailable.

  2. Evolutionary placement of SAGs.
    Figure 2: Evolutionary placement of SAGs.

    Consensus of maximum likelihood (RAxML) trees of concatenated core archaeal conserved single-copy genes (individual trees shown in Supplementary Fig. 7). Phyla (bold) and orders are labelled. Numbers of genomes in collapsed clades are written on the boxes.

  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).
    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).

    Substrates and products are in black italic font, energetic molecules are red, enzymes are in black bold font, and blue lines indicate the cell membrane. ACS, acetyl-CoA synthetase; SCS, succinyl-CoA synthetase. Other acronyms are defined in the text. c, d, Gene architecture for gingipain and clostripain in MBG-D_N05 (c), and clostripain in MCG_E09 (d). MBG-D_C06 had a partial representation of the pathways present in b.

Accession codes

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Author information

  1. These authors contributed equally to this work.

    • Karen G. Lloyd &
    • Lars Schreiber

Affiliations

  1. Center for Geomicrobiology, Department of Bioscience, 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, Tennessee 37996, USA

    • Karen G. Lloyd &
    • Andrew D. Steen
  3. Bigelow Laboratory for Ocean Sciences, East Boothbay, Maine 04544, 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

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.

Competing financial interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to:

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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Supplementary information

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  1. Supplementary Information (1.7 MB)

    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.

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  1. Supplementary Tables (44 KB)

    This file contains Supplementary Table 8.

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