Evolutionary transitions between beneficial and phytopathogenic Rhodococcus challenge disease management

Abstract

Understanding how bacteria affect plant health is crucial for developing sustainable crop production systems. We coupled ecological sampling and genome sequencing to characterize the population genetic history of Rhodococcus and the distribution patterns of virulence plasmids in isolates from nurseries. Analysis of chromosome sequences shows that plants host multiple lineages of Rhodococcus, and suggested that these bacteria are transmitted due to independent introductions, reservoir populations, and point source outbreaks. We demonstrate that isolates lacking virulence genes promote beneficial plant growth, and that the acquisition of a virulence plasmid is sufficient to transition beneficial symbionts to phytopathogens. This evolutionary transition, along with the distribution patterns of plasmids, reveals 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.

Functional Genomics Insights Into the Pathogenicity, Habitat Fitness, and Mechanisms Modifying Plant Development of Rhodococcus sp. PBTS1 and PBTS2

“…Unexpectedly, the fas genes could not be detected in the assembled draft genome sequences of either of the PBTS strains (Stamler et al, 2016;Randall et al, 2018) and as a consequence the pathogenic status of PBTS1 and PBTS2 has been questioned (Savory et al, 2017). Here, we addressed this controversy and used a functional genomics approach to find clues as to how the PBTS bacteria would co-occur and modulate plant development.…”

Repeated gain and loss of a single gene modulates the evolution of vascular pathogen lifestyles

“…Conversely, the loss of cbsA , while not necessary to abolish vascular disease development, is sufficient for the development of non-vascular disease symptoms. We add to a growing body of literature that suggests that transitions between distinct bacterial ecotypes may be mediated by the recurrent gain and loss of few loci ( 5 , 8 ). Although it remains to be determined how the processes of rapid gene gain and loss impact vascular and non-vascular evolution in other pathogenic microbes, our work suggests that these evolutionary events play an important role in shaping bacterial adaptation to specific host tissues.…”

“…Especially for loci encoding ecologically relevant traits, gene gain and loss effectively act as phenotypic switches, enabling rapid shifts between what otherwise seem like complex lifestyles ( 3 ). For example, transitions between plant pathogenic and commensal Pseudomonas ( 5 ), transitions between mutualist and parasitic phenotypes in nitrogen-fixing bacteria ( 6 , 7 ) and transitions between mutualistic and plant pathogenic Rhodococcus ( 8 ) have all been shown to reproducibly occur through the gain and loss of genomic islands containing multiple genes all contributing to the same phenotype. Such rapid evolutionary dynamics have profound implications for our understanding of disease ecology and disease management strategies.…”

Convergent gain and loss of genomic islands drive lifestyle changes in plant-associated Pseudomonas

“…Many of these intimate associations are the product of millions of years of co-evolution, resulting in a complex molecular dialogue between host and bacteria 2,3 . In contrast, horizontal gene transfer (HGT) can lead to rapid lifestyle transitions in host-associated bacteria through the gain and loss of virulence genes [4][5][6] . For example, the acquisition and loss of pathogenicity islands plays a key role in the emergence of enteropathogenic E. coli strains from commensal lineages and vice versa 5 .…”

“…For example, the acquisition and loss of pathogenicity islands plays a key role in the emergence of enteropathogenic E. coli strains from commensal lineages and vice versa 5 . Similarly, a virulence plasmid transforms beneficial plant-associated Rhodococcus strains into pathogens, while strains without the plasmid revert to commensalism 4 . It is unclear if reversibility of lifestyles is common in other bacteria, or if acquisition of pathogenicity genes drives loss of genomic features associated with commensalism (or vice versa).…”