DNA-foraging bacteria in the seafloor

Abstract

Extracellular DNA is a major macromolecule in global element cycles, and is a particularly crucial phosphorus as well as nitrogen and carbon source for microorganisms in the seafloor. Nevertheless, the identities, ecophysiology and genetic features of key DNA-foraging microorganisms in marine sediments are completely unknown. Here we combined microcosm experiments, stable isotope probing and genome-centric metagenomics to study microbial catabolism of DNA and its sub-components in anoxic marine sediments. 13C-DNA added to sediment microcosms was degraded within ten days and mineralised to 13CO2. Stable isotope probing showed that diverse Candidatus Izemoplasma, Lutibacter, Shewanella, Fusibacteraceae and Nitrincolaceae incorporated DNA-derived 13C-carbon. Genomes representative of the 13C-labelled taxa were recovered and all encoded enzymatic repertoires for catabolism of DNA. Comparative genomics indicated that DNA can be digested by diverse members of the order Candidatus Izemoplasmatales (former Tenericutes), which appear to be specialised DNA-degraders that encode multiple extracellular nucleases. Fusibacteraceae lacked genes for extracellular nucleases but utilised various individual purine- and pyrimidine-based molecules, suggesting they cheated on liberated sub-components of DNA. Close relatives of the DNA-degrading taxa are globally distributed in marine sediments, suggesting that these poorly understood taxa contribute widely to the key ecosystem function of degrading and recycling DNA in the seabed.