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

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.