A β‐lactamase gene of Fusarium oxysporum alters the rhizosphere microbiota of soybean

Summary The rhizosphere is a multitrophic environment, and for soilborne pathogens such as Fusarium oxysporum, microbial competition in the rhizosphere is inevitable before reaching and infecting roots. This study established a tritrophic interaction among the plant growth‐promoting rhizobacterium Burkholderia ambifaria, F. oxysporum and Glycine max (soybean) to study the effects of F. oxysporum genes on shaping the soybean microbiota. Although B. ambifaria inhibited mycelial growth and increased bacterial propagation in the presence of F. oxysporum, F. oxysporum still managed to infect soybean in the presence of B. ambifaria. RNA‐Seq identified a putative F. oxysporum secretory β‐lactamase‐coding gene, FOXG_18438 (abbreviated as Fo18438), that is upregulated during soybean infection in the presence of B. ambifaria. The ∆Fo18438 mutants displayed reduced mycelial growth towards B. ambifaria, and the complementation of full Fo18438 and the Fo18438 β‐lactamase domain restored mycelial growth. Using the F. oxysporum wild type, ∆Fo18438 mutants and complemented strains with full Fo18438, Fo18438 β‐lactamase domain or Fo18438 RTA1‐like domain for soil inoculation, 16S rRNA amplicon sequencing revealed that the abundance of a Burkholderia operational taxonomic unit (OTU) was increased in the rhizosphere microbiota infested by the strains with Fo18438 β‐lactamase domain. Non‐metric multidimensional scaling and PICRUSt2 functional analysis revealed differential abundance for the bacterial β‐lactam‐related functions when contrasting the genotypes of F. oxysporum. These results indicated that the Fo18438 β‐lactamase domain provides F. oxysporum with the advantage of growing into the soybean rhizosphere, where β‐lactam antibiosis is involved in microbial competition. Accordingly, this study highlights the capability of an F. oxysporum gene for altering the soybean rhizosphere and taproot microbiota. Significance Statement The integration of RNA‐Seq transcriptomics, fungal knockout approach and microbiome analyses revealed that β‐lactam antibiosis occurs between Fusarium oxysporum and the rhizosphere microbiota of soybean.