Ecological and evolutionary dynamics of a model facultative pathogen: Agrobacterium and crown gall disease of plants

Abstract

Many important pathogens maintain significant populations in highly disparate disease and non-disease environments. The consequences of this environmental heterogeneity in shaping the ecological and evolutionary dynamics of these facultative pathogens are incompletely understood. Agrobacterium tumefaciens, the causative agent for crown gall disease of plants has proven a productive model for many aspects of interactions between pathogens and their hosts and with other microbes. In this review, we highlight how this past work provides valuable context for the use of this system to examine how heterogeneity and transitions between disease and non-disease environments influence the ecology and evolution of facultative pathogens. We focus on several features common among facultative pathogens, such as the physiological remodelling required to colonize hosts from environmental reservoirs and the consequences of competition with host and non-host associated microbiota. In addition, we discuss how the life history of facultative pathogens likely often results in ecological tradeoffs associated with performance in disease and non-disease environments. These pathogens may therefore have different competitive dynamics in disease and non-disease environments and are subject to shifting selective pressures that can result in pathoadaptation or the within-host spread of avirulent phenotypes.

Figure 1

Facultative pathogens experience disparate ecological factors and evolutionary pressures associated with disease and non-disease environments. Transitions between these environments (double-headed curved arrows) are critically important to the ecological and evolutionary dynamics of these pathogens. In the case of Agrobacterium tumefaciens (white ovals), non-disease environments include soil reservoirs and uninfected host rhizospheres, both of which vary dramatically from the environment of diseased plant rhizospheres or actively infected galls (light brown mass in upper root system). Each environment is associated with a unique microbiome (multicolored ovals) allowing for key differences in the positive and negative microbial interactions that A. tumefaciens experiences in these environments. In addition, the need to colonize plant surfaces (e.g. via the unipolar polysaccharide or UPP, red in inset) and antagonism from plant defenses are key features of host plant environments. Within host environments, important host-microbe interactions also include the utilization of rhizosphere exudates, including those (filled yellow circles) whose catabolism (curved blue arrow pointing to split yellow circles that represent catabolized rhizosphere exudates) is conferred by the At plasmid (blue open circle), and pathogenesis conferred by the Ti plasmid (open circle with purple, orange, and gray regions). The T-DNA (purple region) found on the Ti plasmid is delivered via a type IV secretion system (gray cylinder) encoded by the vir-region (gray region) of the Ti plasmid into the host plant cell (arrow through gray cylinder). This allows for T-DNA insertion into the plant genome stimulating tumorigenesis via expression of oncogene products (filled yellow triangles) and opine (filled purple circles) production (curved arrows originating at integrated T-DNA). Opine uptake and catabolism functions (curved orange arrow pointing to split purple circles that represent catabolized opines) are conferred by the opine catabolic region (orange) of the Ti plasmid. Within the disease environment, the pathogen also faces potential exploitative competition over opines and other plant exudates from other microbes able to use these resources (e.g. arrow representing opine uptake by blue genotype) as well as potential interference competition (dashed, blunt line between white and blue genotypes).

Figure 2

Facultative pathogens often infect hosts from environmental populations or reservoirs (leftmost curved arrow). As a consequence, pathogenesis results in a dramatic shift in the pathogen’s biotic and abiotic environment. In this highly simplified schematic, each color represents a different microbial genotype. These may be resident microbiota, microbes that subsequently colonize the host, or novel genetic variants arising via genetic changes (e.g. mutation or horizontal gene transfer). The space defined by the solid curvy lines represents the within-host environment, while the space outside this represents the pathogen’s environmental reservoir. Dynamic selective pressures stemming from changes in the competitive environment, environmental conditions, and host responses can result in shifts within host-associated microbial populations and communities as the disease progresses (arrows exclusively inside the within-host environment). At any point over the course of the infection there is potential for shedding of the host-associated microbiota into the environmental reservoir (curved arrows exiting the within-host environment).