Biogeographic patterns and adaptive strategies of microbial carbon metabolic profiles in paddy soils in the Chinese Mollisol region

• Microbial C metabolic profiles display significant distance-decay relationships. • LCS harbors lower soil C contents but higher abundance of C cycle-related genes. • 211 MAGs and 133 novel vMAGs were reconstructed in the Mollisols. • Distinct microbial carbon metabolic strategies response to soil C heterogeneity. Microbial adaptive evolution and regulation strategies response to carbon (C) heterogeneity in paddy fields at large spatial scales remain poorly understood. Here, we employed gene- and genomic-centric metagenomic approaches to explore soil microbial biogeographic patterns and functional traits regulating C metabolisms across 120 soils derived from 30 paddy fields in Chinese Mollisols. Our findings revealed that significant distance-decay relationships (DDRs) were observed at both microbial C functional and genomic taxonomic levels. Microbial C cycling profiles were clustered into two groups. HCS (including sites R1-R10) represented soils with high total carbon (TC) at relatively high latitudes, whereas LCS (including sites R11-R30) had low soil C content distributed at low latitudes. Compared with HCS, LCS presented higher abundances of C cycling pathways involving aerobic respiration, C fixation, and methanogenesis pathways, as well as higher levels of carbohydrate esterase (CE) and glycosyl transferase (GT) classes. 211 metagenome-assembled genomes (MAGs) with diverse C metabolic functions were constructed. Among these, high-quality MAG292, assigned to the Nanopelagicales order, had a significantly positive correlation with TC and was more abundant in HCS. Contrarily, MAG153, assigned to the Chitinophagales order, exhibited an opposite trend. Additionally, 133 novel vMAGs were retrieved, and the abundances of phage11, phage16, phage26, and phage120 were higher in LCS than in HCS, containing chiA and GH19 that involved in chitin degradation. HCS had a relatively high abundance of phage89, containing slt and GH23 genes that regulate peptidoglycan lysis. These results indicated that soil viruses potentially lyse bacteria by encoding peptidoglycan lyase, releasing nutrients, and increasing the amount of dead microbial debris that facilitates soil C accumulation at relatively high latitudes. In contrast, at low latitudes, the phages together with microbes may indirectly decrease the soil TC by potentially expressing auxiliary metabolic genes (AMGs) involved in chitin degradation. Our findings indicate the divergent microbial adaptive evolution and soil C regulation strategies response to soil C heterogeneity in paddy soils of Chinese Mollisols.