Novel mechanisms for phosphate acquisition in abundant rhizosphere-dwelling Bacteroidetes

Global food production is reliant on the application of finite phosphorus (P) fertilisers. Numerous negative consequences associated with intensive P fertilisation have resulted in a high demand to find alternative sustainable methods that will enhance crop P uptake. Bacteroidetes, primarily from the genus Flavobacterium, have recently been shown to be abundant members of the plant microbiome, but their general ecological role and potential to mobilise P in the rhizosphere remains very poorly characterised. Here, we sought to determine the P mobilisation potential of Flavobacterium strains isolated from the rhizosphere of oilseed rape (Brassica napus L.). In contrast to other abundant rhizosphere bacteria, such as Pseudomonas, all Flavobacterium strains exhibited constitutive phosphatase activity independent of external phosphate (Pi) concentrations. Interestingly, a combination of exoproteomic analysis and molecular microbiology techniques revealed that Flavobacterium have a complex and largely unique repertoire of proteins to mobilise and acquire Pi. This includes the expression of novel, as yet unidentified, phosphatases, and numerous proteins of unknown function. We also discovered that Flavobacterium expresses certain SusCD-like transporters, whose role is typically associated with specialised carbon acquisition, in response to Pi-starvation. Furthermore, the genes encoding these unusual Pi-responsive proteins were enriched in plant-associated Flavobacterium strains suggesting that this machinery represents niche-adaptive strategies for overcoming P scarcity in this genus. We propose that abundant rhizosphere-dwelling Flavobacterium spp. have evolved unique mechanisms for coping with Pi-stress which may provide novel solutions for future sustainable agricultural practices.