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

Abstract

O_LIGlacier forefields in the high-desert region of Ladakh (northwestern Himalaya) are colonized by a variety of interdependent organisms, including lichens, prokaryotes, fungi, mosses, and vascular plants, along a successional gradient. Together with bulk soil, these hosts and their associated microorganisms form a broader microbial metacommunity (holobiome) whose structure, interactions and functions remain poorly underexplored in one of the Earths most extreme and climate-sensitive environments. C_LIO_LIUsing a multidisciplinary approach combining glacial chronosequence transects, GIS-derived topographic variables, soil properties, and plot cover measurements, we assessed the abiotic and biotic factors influencing bacterial and fungal communities sequenced from different hosts and bulk soil (hereafter sources). Microbial composition was primarily shaped by source identity, though certain sources, such as biological soil crusts (BSCs), mosses, and plant rhizospheres, also showed relationships with moraine age in either bacterial or fungal communities. C_LIO_LIBacterial and fungal community congruence was tested using Procrustes analyses, revealing that mosses maintained tightly coupled inter-kingdom relationships throughout the glacier forefields. However, the degree of congruence in plant rhizospheres and bulk soils was influenced by topographic variation and moraine age, respectively. C_LIO_LICo-occurrence network analyses revealed that early successional microbial communities were assembled more stochastically, with bacteria being more interconnected than fungi. In contrast, late successional stages were more compartmentalized, being more structurally stabile, likely driven by increased plant cover and functional redundancy among microbial taxa. C_LIO_LIKeystone bacterial and fungal taxa were identified in plant rhizospheres and bulk soil using a dual-criteria approach related to inter-kingdom congruence and network node eigenvalues. Furthermore, some of these taxa were associated with environmental factors, suggesting topographic heterogeneity and successional age can promote or deter the influence of keystone taxa. C_LIO_LISynthesis: This study reveals the impact of both macroorganism colonization (i.e. plants, mosses, and lichens) and microcommunity establishment (BSCs and bulk soil), as abiotic and biotic sources, on microbial metacommunity assembly in glacier forefields. By adopting a broader approach across different spatial scales, we demonstrate that while plant colonization plays a central role in shaping microbial metacommunities, its effects are modulated by topographic variation along the chronosequence. C_LI