Ralstonia pseudosolanacearum LOV domain protein regulates environmental stress tolerance, iron homeostasis, and bacterial wilt virulence
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Bacteria use diverse sensors to integrate environmental stimuli into physiological responses that ensure fitness and survival. Ralstonia pseudosolanacearum ( Rps ), a soil-borne plant pathogen that causes bacterial wilt disease, encodes a conserved LOV (light-oxygen-voltage) protein that mediates photoreception across the tree of life. However, Rps had a minimal LOV-dependent transcriptional response to light in culture. Clues from functional domains, the lov genomic neighborhood, and transcriptional analyses suggest that LOV shapes Rps biology in response to stress. Loss of LOV did not affect Rps biofilm or motility in vitro , but did influence expression of genes encoding for these phenotypes in planta . The Δlov mutant had reduced heat tolerance and broad metabolic dysregulation, leading to growth defects on several carbon sources but a growth advantage in ex vivo tomato xylem sap and in high-iron medium. In vitro , the Δlov mutant was more tolerant than wild type of redox stress and the antimicrobial phenolic caffeate, but Rps required lov for full virulence on tomato. LOV mediated attachment to the root surface, stem colonization, and overall symptom development. Together these findings reveal that LOV, which is highly conserved among plant pathogenic Ralstonia , modulates Rps stress response and virulence independently of light cues, but in a plant-dependent fashion.
Importance
Like other plant-associated microbes, the destructive crop pathogen Ralstonia pseudosolanacearum ( Rps ) must integrate a complex array of biotic and abiotic signals to successfully infect and colonize the roots and xylem vessels of its plant hosts. Rps encodes a large LOV domain protein. LOV proteins sense blue light in leaf colonizing microbes, but Rps inhabits soil, plant roots, and xylem where there is little blue light. Although deleting lov had only minor effects when the bacterium grew in culture, many genes were dysregulated when the Δlov mutant infected tomato plants. Functional experiments showed LOV has diverse light-independent roles in Rps , including modulating environmental stress tolerance and cellular iron and redox status. Most importantly, Rps needs LOV to grow normally in plants and cause bacterial wilt disease. Thus, LOV is a key sensor-regulator that controls Rps adaptation to the plant environment and virulence.
