Evolutionary diversification and succession of soil huge phages in glacier foreland

Abstract Huge phages (genome length > 200 kbp) have been found in diverse habitats worldwide, infecting a variety of prokaryotes. Yet, our understanding of their evolution and adaptation strategy in soil is limited due to the scarcity of soil-derived genomes. Here we carried out a size-fractioned (0.22µm) metagenomic survey across a 130-year chronosequence of a glacier foreland in the Tibetan plateau and discovered 597 novel huge phage populations. Their communities in glacier foreland revealed a distinct pattern between the early (≤ 40 years) and late stages (> 40 years). A significant increasing in the diversity and abundance of huge phages in the late stage following glacier retreat were illuminated, which coincided with soil development and vegetation formation. The phages within the late-stage demonstrated remarkable higher microdiversity, gene flow frequency, and stronger phylogenomic clustering, suggesting that natural selection and genetic drift are key drivers of the huge phage speciation. Alongside the shift in huge phage communities, we noted a functional transition between the early and late stages, contributing to the survival and growth of their hosts. This study unravels the hidden diversity of huge phages in soil and highlights the importance of environmental changes in shaping the composition, evolutionary trajectories and function of huge phage communities.