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.

细胞外DNA是全球元素循环中的主要大分子，是海底微生物特别重要的磷、氮和碳源。然而，海洋沉积物中 DNA 觅食微生物的身份、生态生理学和遗传特征在很大程度上是未知的。在这里，我们结合微观实验、DNA 稳定同位素探测 (SIP)、使用纳米级次级同位素质谱 (NanoSIMS) 的单细胞 SIP 和以基因组为中心的宏基因组学来研究海洋沉积物中 DNA 及其亚组分的微生物分解代谢。添加到沉积物微观世界中的^{13 C-DNA 在 10 d 内大量降解并矿化为13} CO ₂。DNA 的 SIP 探测揭示了多种“ Candidatus Izemoplasma”，Lutibacter、Shewanella和 Fusibacteraceae 结合了 DNA 衍生的¹³ C-碳。NanoSIMS 证实将¹³ C 掺入到从微观世界中分选出来的梭杆菌科的单个细菌细胞中。¹³ C 标记的分类群的基因组都编码用于 DNA 或 DNA 亚组分分解代谢的酶库。比较基因组学表明，不同的候选者Izemoplasmatales（以前的 Tenericutes）是特殊的，因为它们编码多个（最多五个）预测的细胞外核酸酶，并且可能是专门的 DNA 降解剂。对其他沉积物宏基因组的分析表明，细胞外核酸酶基因在拟杆菌门的不同部位普遍存在。总之，我们的结果揭示了微生物的特性和功能特性，这些特性可能有助于在海底降解和回收 DNA 的关键生态系统功能。