Deterministic Selection Dominates Microbial Community Assembly in Termite Mounds Across a Large Spatial Area

Abstract

Background: Termites are ubiquitous insects in tropical and subtropical habitats, where they construct massive mounds from soil, their saliva and excreta. Termite mounds harbor an enormous amount of microbial inhabitants, which regulate multiple ecosystem functions such as mitigating methane emissions and increasing ecosystem resistance to climate change. However, we lack a mechanistic understanding about the role of termite mounds in modulating the microbial community assembly processes, which are essential to unravel the biological interactions of soil fauna and microorganisms, the major components of soil food webs. We conducted a large-scale survey across a >1500 km transect in northern Australia to investigate biogeographical patterns of bacterial and fungal community in 134 termite mounds and the relative importance of deterministic versus stochastic processes in microbial community assembly. Results: Microbial alpha (number of phylotypes) and beta (changes in bacterial and fungal community composition) significantly differed between termite mounds and surrounding soils. Microbial communities in termite mounds exhibited a significant distance-decay pattern, and fungal communities had a stronger distance-decay relationship (slope = -1.91) than bacteria (slope = -0.21). Based on the neutral community model (fitness < 0.7) and normalized stochasticity ratio index (NST) with a value below the 50% boundary point, deterministic selection, rather than stochastic forces, predominated the microbial community assembly in termite mounds. Deterministic processes exhibited significantly weaker impacts on bacteria (NST = 45.23%) than on fungi (NST = 33.72%), probably due to the wider habitat niche breadth and higher potential migration rate of bacteria. The abundance of antibiotic resistance genes (ARGs) was negatively correlated with bacterial/fungal biomass ratios, indicating that ARG content might be an important biotic factor that drove the biogeographic pattern of microbial communities in termite mounds. Conclusions: Deterministic processes play a more important role than stochastic processes in shaping the microbial community assembly in termite mounds, an unique habitat ubiquitously distributed in tropical and subtropical ecosystems. An improved understanding of the biogeographic patterns of microorganisms in termite mounds is crucial to decipher the role of soil faunal activities in shaping microbial community assembly, with implications for their mediated ecosystems functions and services.