Carbohydrate-active enzymes of soil prophages enhance global carbon cycling potential

Hanpeng Liao, Chaofan Ai, Chen Liu, Hongbo Zhang, Dong Zhang, Pengfa Li, Xiang Tang, Xiaolong Liang, Ville‐Petri Friman, Manuel Delgado‐Baquerizo, Shungui Zhou

Recent work suggests that soil-borne viruses play an important role in controlling carbon (C) cycling and stocks. However, the contribution of individual prophage (i.e., temperate phages residing within bacterial hosts during lysogenic cycle) to C degradation remains largely undocumented at global scale. Here, we generated a global gene catalog of prophage-encoded carbohydrate-active enzyme (pCAZymes), including 20,131 soil bacterial genomes, 3548 metagenomes, and 951 metatranscriptomes derived from pre-existing databases. The catalog includes 4708 pCAZymes associated with the degradation of lignocellulose, lignin, and pectin, with 21 lytic polysaccharide monooxygenase genes newly identified in phages. Our findings reveal that prophages have potential to accelerate labile soil C degradation by encoding pCAZymes that cooperate with their bacterial hosts. Using machine learning models, we predict a 13 ± 0.7% increase in the C metabolic potential driven by soil prophages by 2100 under a high-emission scenario (SSP585). In vitro experiments demonstrated that the transcriptional activity of pCAZyme genes is regulated by environmental temperature. Soil microcosm experiments further confirmed that pCAZymes can enhance host-mediated organic C mineralization by increasing degradative enzyme activity. This study reveals previously overlooked ecological functions of prophages in global soil C transformation, with important implications for the global climate and C cycling. While it has been known that viruses contribute to biogeochemical cycles, it was unclear how prophages, of which reside within their bacterial hosts, contribute to soil carbon cycling. Zhou et al. present a global gene catalog of prophage-encoded carbohydrate-active enzyme (pCAZymes) and model the influence of these phages under a high-emission scenario.