Microbiology Spectrum (Dec 2023)

Rice bacterial leaf blight drives rhizosphere microbial assembly and function adaptation

  • Hubiao Jiang,
  • Jinyan Luo,
  • Quanhong Liu,
  • Solabomi Olaitan Ogunyemi,
  • Temoor Ahmed,
  • Bing Li,
  • Shanhong Yu,
  • Xiao Wang,
  • Chenqi Yan,
  • Jianping Chen,
  • Bin Li

DOI
https://doi.org/10.1128/spectrum.01059-23
Journal volume & issue
Vol. 11, no. 6

Abstract

Read online

ABSTRACT Rice bacterial leaf blight (BLB) is the most destructive phyllosphere bacterial disease caused by Xanthomonas oryzae pv. oryzae. The effect of soil-borne diseases on the rhizosphere microbiome has been extensively investigated. However, the regulatory role of the phyllosphere disease BLB on the rhizosphere microbiome remains unclear. Here, we observed that BLB significantly altered the composition of the bacterial-fungal community in the rhizosphere, decreasing bacterial diversity but not fungal diversity. The scale of inter-kingdom networks in the rhizosphere microbiome of BLB-infected plants was more complex and broader than in healthy plants, while the bacterial community was more vulnerable to BLB than the fungal community. Indeed, the relative abundance of Streptomyces, Chitinophaga, Sphingomonas, and Bacillus was higher in the BLB rhizosphere, which can be explained by their keystone hub taxa status in the rhizosphere co-occurrence network. Null model analysis showed that the deterministic assembly of bacterial communities increased while that of fungi decreased. Additionally, the assembly of bacterial and fungal communities was significantly related to variations in BLB and soil nutrients, especially pH and available phosphorus. Random forest model results showed that the bacterial community in the rhizosphere had a strong potential for predicting BLB. Metagenomic analysis revealed that BLB had a considerable impact on the functional adaptation of the rhizosphere microbiome. Interestingly, the abundance of some functional genes involved in carbon, phosphorus, and methane metabolism increased drastically. IMPORTANCE Our results suggest that rhizosphere bacteria are more sensitive to bacterial leaf blight (BLB) than fungi. BLB infection decreased the diversity of the rhizosphere bacterial community but increased the complexity and size of the rhizosphere microbial community co-occurrence networks. In addition, the relative abundance of the genera Streptomyces, Chitinophaga, Sphingomonas, and Bacillus increased significantly. Finally, these findings contribute to the understanding of plant-microbiome interactions by providing critical insight into the ecological mechanisms by which rhizosphere microbes respond to phyllosphere diseases. In addition, it also lays the foundation and provides data to support the use of plant microbes to promote plant health in sustainable agriculture, providing critical insight into ecological mechanisms.

Keywords