Root endophytic bacterial and fungal communities in a natural hot desert are differentially regulated in dry and wet seasons by stochastic processes and functional traits

Abstract

Dryland ecosystems experience seasonal cycles of severe drought and moderate precipitation. Desert plants may develop symbiotic relationships with root endophytic microbes to survive under the repeated wet and extremely dry conditions. Although community coalescence has been found in many systems, the colonization by functional microbes and its relationship to seasonal transitions in arid regions are not well understood. Here we examined root endophytic microbial taxa, and their traits in relation to their root colonization, during the dry and wet seasons in a hot desert of the southwestern United States. We used high-throughput DNA sequencing of 16S rRNA and internal transcribed spacer gene profiling of five desert shrubs, and analyzed the seasonal change in endophytic microbial lineages. Goodness of fit to the neutral community model in relationship to microbial traits was evaluated. In summer, Actinobacteria and Bacteroidia increased, although this was not genus-specific. For fungi, Glomeraceae selectively increased in summer. In winter, Gram-negative bacterial genera, including those capable of nitrogen fixation and plant growth promotion, increased. Neutral model analysis revealed a strong stochastic influence on endophytic bacteria but a weak effect for fungi, especially in summer. The taxa with higher frequency than that predicted by neutral model shared environmental adaptability and symbiotic traits, whereas the frequency of pathogenic fungi was at or under the predicted value. These results suggest that community assembly of bacteria and fungi is regulated differently. The bacterial community was affected by stochastic and deterministic processes via bacterial response to drought (response trait), beneficial effect on plants (effect trait), and likely stable mutualistic interactions with plants suggested by the frequency of nodule bacteria. For fungi, mycorrhizal fungi were selected by plants in summer. The regulation of beneficial microbes by plants in both dry and wet seasons suggests the presence of plant-soil positive feedback in this natural desert ecosystem.

Keywords: Arbuscular mycorrhizal fungi; Desert; Dryland; Endophytic bacteria; Endophytic fungi; Neutral community model.