Viewing disease emergence through an eco-evolutionary lens: Dissecting the genetic and demographic dynamics of a beetle-vectored bacterial plant pathogen

Iowa State University, Ames IA

Investigators

Abstract

Emerging plant diseases can incur economic and environmental costs by leading to epidemics or the persistent appearance of low levels of new diseases. Identifying the risk factors favoring the emergence of plant pathogens is important to predicting, monitoring, mitigating, and managing diseases. The transmission of bacterial plant pathogens by beetles may pose an unrecognized, yet major, risk for disease emergence because beetles pick up and spread bacteria with relative ease, namely by feeding with subsequent fecal transmission. Beetles also harbor bacterial species that are well adapted to both the insect gut and plant environments, and they are prone to invasiveness, geographic range expansion, and pathogen spread among multiple plant species due to often indiscriminate feeding. The goal of this project is to understand the factors driving the adaptation, persistence, and emergence of beetle-vectored bacterial pathogens. As a study system, the project will use a bacterial wilt pathogen of commercially important cucurbit species (e.g., cucumbers, squash and muskmelons), beetles that transmit the pathogen, and bacteriophages that kill the pathogen. The project will explore mechanisms influencing the short-term evolutionary potential of the pathogen, and mechanisms driving change in present-day populations, by examining genetic bottlenecks, barriers to acquisition and spread by beetles, and genomic variation in native populations in plants and beetles. Based on the discovery of pathogen-specific bacteriophages within beetles, the project will also explore integrating bacteriophages into strategies to manage beetle-transmitted bacterial plant pathogens. Collectively, the results will provide critical data to help assess the emergence risk for such pathogens. Insects are responsible for vectoring some of the costliest bacterial diseases of crops. Although the best studied among these are the piercing-sucking hemipterans, non-hemipterans such as beetles may pose a higher risk for disease emergence due to their comparatively simple mode of pathogen acquisition and transmission. To understand the ecological and evolutionary processes impacting non-hemipteran-vectored bacterial pathogens, this study will use the wilt pathogen Erwinia tracheiphila, its cucumber beetle vectors, virulent bacteriophages, and cucurbits as a model system. The first aim is to evaluate the impact of vector–plant and plant–vector transmission events and aggregative beetle feeding on genetic variation within pathogen populations. Experiments will use neutrally barcoded pathogen libraries to track strain-level population dynamics under natural routes of transmission. The second aim is to map patterns of genomic variation in wild pathogen populations in plants and beetles in the field, including during overwintering in beetles. Experiments will use whole-population whole-genome sequencing to investigate the molecular mechanisms driving genomic changes. The final aim will interrogate bacteriophage acquisition, persistence, and predation in beetles, fitness tradeoffs that may accompany bacteriophage resistance, and the potential for beetle-mediated bacteriophage-based pathogen control. These studies will generate some of the first quantitative data characterizing bacteriophage–pathogen dynamics for a vector-transmitted phytopathogen. The societal significance of this project is its translational relevance to predicting emergence and managing insect-vectored bacterial diseases, and its educational relevance in promoting science literacy and public awareness of the importance of plant–microbe–insect interactions. This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.