Holobiomes in succession: post-glacial microbial communities are structured by hosts, time and habitat heterogeneity.

Abstract

Glacier forefields provide model ecosystems for studying primary succession, where newly exposed substrates are colonized by microbes associated with lichens, biological soil crusts (BSCs), mosses, vascular plants, and bulk soil. Collectively, these sources form an interconnected microbial holobiome, yet their roles in structuring bacterial and fungal metacommunities remain poorly understood. We investigated how source identity, moraine age, and topography shape microbial assembly across four glacier forefields in the high-altitude desert of Ladakh, India (northwestern Himalaya). Using a chronosequence approach integrating vegetation surveys, soil physicochemistry, GIS-derived topographic variables, and amplicon sequencing, we found that source identity was the primary driver of microbial diversity and composition. Lichens supported low-diversity communities, whereas mosses, bulk soil, and vascular plants harboured more diverse communities. Bacterial-fungal congruence was significant in all sources except bulk soil, indicating stronger inter-kingdom coupling in host-associated habitats than among soil environments. Source exclusion consistently altered microbial co-occurrence network structure, revealing potential ecological roles among sources, with cryptogams supporting microbial connectivity and vascular plants promoting more specialized interactions. Structural equation modelling further showed that succession indirectly shaped microbial diversity through source colonization and soil development. These findings demonstrate that complementary source-specific ecological strategies organize microbial diversity and interactions during glacier forefield succession.