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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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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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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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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DOI: https://doi.org/10.1038/s41396-023-01538-2