From guest to host: parasite Cistanche deserticola shapes and dominates bacterial and fungal community structure and network complexity

Abstract

Background: Rhizosphere and plant microbiota are assumed to play an essential role in deciding the well-being of hosts, but effects of parasites on their host microbiota have been rarely studied. Also, the characteristics of the rhizosphere and root microbiota of parasites and hosts under parasitism is relatively unknown. In this study, we used Cistanche deserticola and Haloxylon ammodendron from cultivated populations as our model parasites and host plants, respectively. We collected samples from BULK soil (BULK), rhizosphere soil of H. ammodendron not parasitized (NCD) and parasitized (RHA) to study how the parasite influenced the rhizosphere microbiota of the host. We also collected samples from the rhizosphere soil and roots of C. deserticola (RCD and ECD) and Haloxylon ammodendron (RHA and EHA) to explore the difference between the microbiota of the parasite and its host under parasitism. Results: The parasite reduced the compositional and co-occurrence network complexities of bacterial and fungal microbiota of RHA. Additionally, the parasite increased the proportion of stochastic processes mainly belonging to dispersal limitation in the bacterial microbiota of RHA. Based on the PCoA ordinations and permutational multivariate analysis of variance, the dissimilarity between microbiota of C. deserticola and H. ammodendron were rarely evident (bacteria, R2 = 0.29971; fungi, R2 = 0.15631). Interestingly, four hub nodes of H. ammodendron in endosphere fungal microbiota were identified, while one hub node of C. deserticola in endosphere fungal microbiota was identified. It indicated that H. ammodendron played a predominant role in the co-occurrence network of endosphere fungal microbiota. Source model of plant microbiome suggested the potential source percentage from the parasite to the host (bacteria: 52.1%; fungi: 16.7%) was lower than host-to-parasite (bacteria: 76.5%; fungi: 34.3%), illustrating that microbial communication was bidirectional, mainly from the host to the parasite. Conclusions: Collectively, our results suggested that the parasite C. deserticola shaped the diversity, composition, co-occurrence network, and community assembly mechanisms of the rhizosphere microbiota of H. ammodendron. Additionally, the microbiota of C. deserticola and H. ammodendron were highly similar and shared. Our findings on parasite and host microbiota provided a novel line of evidence supporting the influence of parasites on the microbiota of their hosts.