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

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.

Keystone Genes from Extracellular DNA Facilitate Microbial Adaptation in Organochlorine Pesticide-Contaminated Soil

“…Extracellular and intracellular DNA (e-iDNA) were extracted according to the method in Wasmund and Liang et al with some modi cations (Fig. S2) [37,57]. Brie y, soil samples were mixed with sterile phosphate buffer and polyvinyl polypyrrolidone.…”

“…S11). According to the previous studies [45][46][47][48], especially in oligotrophic and pollutedstress, microorganisms could passively or actively release eDNA through plasmid and chromosome DNA sections of living cells, phage infection, or pyrolysis of dead cells.Meanwhile, natural competent microorganisms could integrate and express free or bonded eDNA fragments through natural transformation, which was a parasexual mechanism of microbes forsurviving environmental stress andfor generating diversity and adaptation [37,[45][46]48].Therefore, gene exchanges within e-iDNA factions could enhance the process of natural transformation, and play a vital role in microorganism responses to environmental stress [46,48]. Furthermore, in this study, the proportion of copresence gene interactions in the co-occurrence networks of low-and high-OCP-induced soil groups was signi cantly higher than that in the clean soil (Fig.…”

“…5C-5E). Therefore, both in simpli ed and complicated microenvironments, gene exchanges between e-iDNA fractions might be an important strategy for KGs to respond to environmental stress [1,4,37]. Moreover, previous studies havedocumented that the ecosystem might shift from one stable state to an alternative stable state once the disturbance exceedsa threshold,and that this new state is hard to recover from [4,[52][53].This shift might be accelerated by gene ow and gene selection, and in uenced or driven by KGs [4,54].…”

Shifts in DNA yield and biological community composition in stored sediment: implications for paleogenomic studies

“…Additionally, cell lysate also contains cellular nucleases that may contribute to DNA degradation before some molecules become sediment bound. Bacteria surviving in chilled sediments can also produce or take advantage of nucleases in the sediment matrix, allowing them to feed on depurinated DNA and subsequent degradation products (Wasmund et al 2021). Proteobacteria, which increased in abundance during the experi-ment (see discussion below) are known to have genes that enable consumption of DNA (Finkle and Kolter 2001) and this could be another possible mechanism for reduction in DNA of lysate-spiked samples.…”

“…Bacteria can degrade and recycle extracellular DNA in marine sediments via extracellular nucleases (Wasmund et al 2021), indicating there is potential for decreased DNA yields if sediment bacteria survive during longterm storage. Furthermore, some microbes can survive in low energy conditions, such as subsurface sediments (Ciobanu et al 2014) and they may influence the community composition by consuming or outcompeting other microbes.…”