A Bacterial–Fungal Metaproteomic Analysis Enlightens an Intriguing Multicomponent Interaction in the Rhizosphere of Lactuca sativa

Fusarium oxysporum MSA 35 [wild-type (WT) strain] is an antagonistic isolate that protects plants against pathogenic Fusaria. This strain lives in association with ectosymbiotic bacteria. When cured of the prokaryotic symbionts [cured (CU) form], the fungus is pathogenic, causing wilt symptoms similar to those of F. oxysporum f.sp. lactucae. The aim of this study was to understand if and how the host plant Lactuca sativa contributes to the expression of the antagonistic/pathogenic behaviors of MSA 35 strains. A time-course comparative analysis of the proteomic profiles of WT and CU strains was performed. Fungal proteins expressed during the early stages of plant-fungus interaction were involved in stress defense, energy metabolism, and virulence and were equally induced in both strains. In the late phase of the interkingdom interaction, only CU strain continued the production of virulence- and energy-related proteins. The expression analysis of lettuce genes coding for proteins involved in resistance-related processes corroborated proteomic data by showing that, at the beginning of the interaction, both fungi are perceived by the plant as pathogen. On the contrary, after 8 days, only the CU strain is able to induce plant gene expression. For the first time, it was demonstrated that an antagonistic F. oxysporum behaves initially as pathogen, showing an interesting similarity with other beneficial organisms such as mychorrizae.