Genomic insights into diverse bacterial taxa that degrade extracellular DNA in marine sediments

Kenneth Wasmund*, Claus Pelikan, Arno Schintlmeister, Michael Wagner, Margarete Watzka, Andreas Richter, Srijak Bhatnagar, Amy Noel, Casey R.J. Hubert, Thomas Rattei, Thilo Hofmann, Bela Hausmann, Craig W. Herbold, Alexander Loy

*Corresponding author for this work

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    Abstract

    Extracellular DNA is a major macromolecule in global element cycles, and is a particularly crucial phosphorus, nitrogen and carbon source for microorganisms in the seafloor. Nevertheless, the identities, ecophysiology and genetic features of DNA-foraging microorganisms in marine sediments are largely unknown. Here, we combined microcosm experiments, DNA stable isotope probing (SIP), single-cell SIP using nano-scale secondary isotope mass spectrometry (NanoSIMS) and genome-centric metagenomics to study microbial catabolism of DNA and its subcomponents in marine sediments. 13C-DNA added to sediment microcosms was largely degraded within 10 d and mineralized to 13CO2. SIP probing of DNA revealed diverse ‘Candidatus Izemoplasma’, Lutibacter, Shewanella and Fusibacteraceae incorporated DNA-derived 13C-carbon. NanoSIMS confirmed incorporation of 13C into individual bacterial cells of Fusibacteraceae sorted from microcosms. Genomes of the 13C-labelled taxa all encoded enzymatic repertoires for catabolism of DNA or subcomponents of DNA. Comparative genomics indicated that diverse ‘Candidatus Izemoplasmatales’ (former Tenericutes) are exceptional because they encode multiple (up to five) predicted extracellular nucleases and are probably specialized DNA-degraders. Analyses of additional sediment metagenomes revealed extracellular nuclease genes are prevalent among Bacteroidota at diverse sites. Together, our results reveal the identities and functional properties of microorganisms that may contribute to the key ecosystem function of degrading and recycling DNA in the seabed.

    Original languageEnglish
    Pages (from-to)885-898
    Number of pages14
    JournalNature Microbiology
    Volume6
    Issue number7
    Early online date14 Jun 2021
    DOIs
    Publication statusPublished - 1 Jul 2021

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