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

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

doi:10.1038/s41564-021-00917-9

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.

Highlights

Subsurface environments including marine sediments harbour the bulk of microbial biomass on Earth[1]
Analyses of microbial 16S ribosomal RNA genes derived from extracellular- and intracellular-DNA pools in marine sediments showed that extracellular DNA is rapidly turned over in both shallow and deeper sediments[13,14]
To identify and study the ecophysiology of DNA-degrading microorganisms, we performed a functional microbiome approach including marine sediment microcosm experiments supplemented with 13C-labelled DNA or individual unlabelled DNA subcomponents, DNA-based

Summary

Introduction

Subsurface environments including marine sediments harbour the bulk of microbial biomass on Earth[1]. The most abundant of the various classes of organic molecules available for catabolism by microorganisms in marine sediments, and in most other environments, include proteins, lipids, carbohydrates and nucleic acids—the molecules that make up most of the biomass of any cell or virus[7,8,9]. Estimates suggest ‘bioavailable’ DNA, that is, DNA available for digestion by extracellular nucleases, supplies microbial communities of coastal and deep-sea sediments with 2−4% of their carbon requirements, 7–4%. Degradation products of nucleic acids such as urea and ammonium, as well as CO2 and acetate[18], are important nutrients for other members of microbial communities. Despite the fact that nutrient-rich and ubiquitous DNA molecules are available in marine sediments, our knowledge of microorganisms that degrade and mineralize DNA remains poor[20]. To identify and study the ecophysiology of DNA-degrading microorganisms, we performed a functional microbiome approach including marine sediment microcosm experiments supplemented with 13C-labelled DNA or individual unlabelled DNA subcomponents, DNA-based

Methods

Results

Conclusion