Networking the desert plant microbiome, bacterial and fungal symbionts structure and assortativity in co-occurrence networks.

Abstract

In nature, microbes do not thrive in seclusion but are involved in complex interactions within- and between-microbial kingdoms. Among these, symbiotic associations with mycorrhizal fungi and nitrogen-fixing bacteria are namely known to improve plant health, while providing resources to benefit other microbial members. Yet, it is not clear how these microbial symbionts interact with each other or how they impact the microbiota network architecture. We used an extensive co-occurrence network analysis, including rhizosphere and roots samples from six plant species in a natural desert in AlUla region (Kingdom of Saudi Arabia) and described how these symbionts were structured within the plant microbiota network. We found that the plant species was a significant driver of its microbiota composition and also of the specificity of its interactions in networks at the microbial taxa level. Despite this specificity, a motif was conserved across all networks, i.e., mycorrhizal fungi highly covaried with other mycorrhizal fungi, especially in plant roots-this pattern is known as assortativity. This structural property might reflect their ecological niche preference or their ability to opportunistically colonize roots of plant species considered non symbiotic e.g., H. salicornicum, an Amaranthaceae. Furthermore, these results are consistent with previous findings regarding the architecture of the gut microbiome network, where a high level of assortativity at the level of bacterial and fungal orders was also identified, suggesting the existence of general rules of microbiome assembly. Otherwise, the bacterial symbionts Rhizobiales and Frankiales covaried with other bacterial and fungal members, and were highly structural to the intra- and inter-kingdom networks. Our extensive co-occurrence network analysis of plant microbiota and study of symbiont assortativity, provided further evidence on the importance of bacterial and fungal symbionts in structuring the global plant microbiota network.