Evolutionary transitions between beneficial and phytopathogenic Rhodococcus challenge disease management

Authors: SAVORY, ELIZABETH - Oregon State University; FULLER, SKYLAR - Oregon State University; WEISBERG, ALEXANDRA - Oregon State University; THOMAS, WILLIAM - Oregon State University; GORDON, MICHAEL - Oregon State University; STEVENS, DANIELLE - Oregon State University; CREASON, ALLISON - Oregon State University; BELCHER, MICHAEL - Oregon State University; SERDANI, MARYNA - Oregon State University; WISEMAN, MICHELE - Oregon State University; PUTNAM, MELODIE - Oregon State University; Grunwald, Niklaus - Nik; CHANG, JEFF - Oregon State University

Submitted to: eLife
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/3/2017
Publication Date: 12/12/2017
Citation: Savory, E., Fuller, S., Weisberg, A., Thomas, W., Gordon, M., Stevens, D., Creason, A., Belcher, M., Serdani, M., Wiseman, M., Putnam, M., Grunwald, N.J., Chang, J. 2017. Evolutionary transitions between beneficial and phytopathogenic Rhodococcus challenge disease management. eLife. 6:e30925. https://doi.org/10.7554/eLife.30925.
DOI: https://doi.org/10.7554/eLife.30925

Interpretive Summary: Understanding how bacteria affect plant health is crucial for developing sustainable crop production systems. We coupled ecological sampling and whole genome sequencing to characterize the population genetic history of the gall forming bacterium Rhodococcus. Analysis of chromosome sequences show plants host multiple evolutionary lineages of Rhodococcus. We demonstrate that isolates lacking virulence genes promote beneficial plant growth. Furthermore, acquisition of a virulence plasmid is sufficient to transition beneficial bacteria in this genus from symbionts to phytopathogens. This rarely described evolutionary transition, along with the distribution patterns of plasmids, reveal the impact of horizontal gene transfer in rapidly generating new pathogenic lineages and provides an alternative explanation for pathogen transmission patterns. This work has implications for managing epidemics of Rhodococcus where beneficial and pathogenic strains need to be differentiated.

Technical Abstract: Understanding how bacteria affect plant health is crucial for developing sustainable crop production systems. We coupled ecological sampling and whole genome sequencing to characterize the population genetic history of Rhodococcus and distribution of virulence plasmids in managed systems. Analysis of chromosome sequences show plants host multiple lineages of Rhodococcus , and suggested that transmissions are due to independent introductions, reservoir populations, and point source outbreaks. We demonstrate that isolates lacking virulence genes promote beneficial plant growth, and that acquisition of a virulence plasmid is sufficient to transition beneficial symbionts to phytopathogens. This rarely described evolutionary transition, along with the distribution patterns of plasmids, reveal the impact of horizontal gene transfer in rapidly generating new pathogenic lineages and provides an alternative explanation for pathogen transmission patterns. Results also uncovered a misdiagnosed epidemic that implicated beneficial Rhodococcus bacteria as pathogens of pistachio. The misdiagnosis perpetuated the unnecessary removal of trees and exacerbated economic losses.