17Extracellular DNA is a major macromolecule in global element cycles, and is a particularly 18 crucial phosphorus as well as nitrogen and carbon source for microorganisms in the seafloor. 19Nevertheless, the identities, ecophysiology and genetic features of key DNA-foraging 20 microorganisms in marine sediments are completely unknown. Here we combined 21 microcosm experiments, stable isotope probing and genome-centric metagenomics to study 22 microbial catabolism of DNA and its sub-components in anoxic marine sediments. 13 C-DNA 23 added to sediment microcosms was degraded within ten days and mineralised to 13 CO2. 24Stable isotope probing showed that diverse Candidatus Izemoplasma, Lutibacter, Shewanella, 25Fusibacteraceae and Nitrincolaceae incorporated DNA-derived 13 C-carbon. Genomes 26representative of the 13 C-labelled taxa were recovered and all encoded enzymatic repertoires 27 for catabolism of DNA. Comparative genomics indicated that DNA can be digested by 28 diverse members of the order Candidatus Izemoplasmatales (former Tenericutes), which 29 appear to be specialised DNA-degraders that encode multiple extracellular nucleases. 30Fusibacteraceae lacked genes for extracellular nucleases but utilised various individual 31 purine-and pyrimidine-based molecules, suggesting they 'cheated' on liberated sub-32 components of DNA. Close relatives of the DNA-degrading taxa are globally distributed in 33 marine sediments, suggesting that these poorly understood taxa contribute widely to the key 34 ecosystem function of degrading and recycling DNA in the seabed. 35 36 37 DNA compared to 12 C-DNA, from several time points, i.e., days 4, 10 and 13 (Supp. Fig. 5). 130Later time points showed no elevated 16S rRNA gene abundances in heavy fractions and 131 therefore subsequent analyses focused on the first three time points, and thus, largely on the 132 primary DNA degraders. 133