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Identification and cultivation of anaerobic bacterial scavengers of dead cells

The ISME Journal volume 17, pages 2279–2289 (2023)Cite this article

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Abstract

The cycle of life and death and Earth’s carbon cycle(s) are intimately linked, yet how bacterial cells, one of the largest pools of biomass on Earth, are recycled back into the carbon cycle remains enigmatic. In particular, no bacteria capable of scavenging dead cells in oxygen-depleted environments have been reported thus far. In this study, we discover the first anaerobes that scavenge dead cells and the two isolated strains use distinct strategies. Based on live-cell imaging, transmission electron microscopy, and hydrolytic enzyme assays, one strain (designated CYCD) relied on cell-to-cell contact and cell invagination for degrading dead food bacteria where as the other strain (MGCD) degraded dead food bacteria via excretion of lytic extracellular enzymes. Both strains could degrade dead cells of differing taxonomy (bacteria and archaea) and differing extents of cell damage, including those without artificially inflicted physical damage. In addition, both depended on symbiotic metabolic interactions for maximizing cell degradation, representing the first cultured syntrophic Bacteroidota. We collectively revealed multiple symbiotic bacterial decomposition routes of dead prokaryotic cells, providing novel insight into the last step of the carbon cycle.

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Fig. 1: Plaque formation by anaerobic dead cell scavengers.
Fig. 2: Degradation of dead bacterial cells by strains CYCD and MGCD.
Fig. 3: Growth of strains CYCD and MGCD on autoclaved E. coli cells.
Fig. 4: Transmission electron microscopy (TEM) and scanning electron microscopy (SEM) images of degrader of dead cells.
Fig. 5: Degradation of protein by strains CYCD with M. hungatei.

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Data availability

The genome sequences and annotation data of strain CYCD are available in National Center for Biotechnology Information (NCBI) BioProject under accession number PRJDB15250.

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Acknowledgements

This research was supported financially by Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science 18H03367 to MKN and 22K18046 to YH. We thank Dr. Bernhard Schink and Dr. Aharon Oren for their help with the nomenclature of the species.

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Authors and Affiliations

  1. Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, 305-8566, Japan

    Yuga Hirakata, Ran Mei, Kana Morinaga, Hideyuki Tamaki, Xian-ying Meng & Masaru K. Nobu

  2. Geomicrobiology Research Group, Research Institute for Geo-Resources and Environment, Geological Survey of Japan (GSJ), National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, 305-8567, Japan

    Taiki Katayama

  3. Department of Civil and Environmental Engineering, Nagaoka University of Technology, Nagaoka, 940-2188, Japan

    Takahiro Watari, Takashi Yamaguchi & Masashi Hatamoto

  4. Department of Science of Technology Innovation, Nagaoka University of Technology, Nagaoka, 940-2188, Japan

    Takashi Yamaguchi

  5. Institute for Extra-Cutting-Edge Science and Technology Avant-Garde Research (X-star), Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, 237-0061, Japan

    Masaru K. Nobu

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  1. Yuga Hirakata
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Conceptualization: YH, MKN; Methodology: YH, RM, MKN; Investigation: YH, KM, XM; Resources: YH, MH, TW, TY, TK, MKN; Visualization: YH, MKN; Writing – original draft: YH, MKN; Writing – review & editing: YH, RM, KM, TK, HT, XM, TW, TY, MH, MKN. All authors have read and approved the manuscript submission.

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Correspondence to Yuga Hirakata or Masaru K. Nobu.

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Hirakata, Y., Mei, R., Morinaga, K. et al. Identification and cultivation of anaerobic bacterial scavengers of dead cells. ISME J 17, 2279–2289 (2023). https://doi.org/10.1038/s41396-023-01538-2

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