Phytopathogens have evolved specialized pathogenicity determinants that enable them to colonize their specific plant hosts and cause disease, but their intimate associations with plants also predispose them to frequent encounters with herbivorous insects, providing these phytopathogens with ample opportunity to colonize and eventually evolve alternative associations with insects. Decades of research have revealed that these associations have resulted in the formation of bacterial-vector relationships, in which the insect mediates dissemination of the plant pathogen. Emerging research, however, has highlighted the ability of plant pathogenic bacteria to use insects as alternative hosts, exploiting them as they would their primary plant host. The identification of specific bacterial genetic determinants that mediate the interaction between bacterium and insect suggests that these interactions are not incidental, but have likely arisen following the repeated association of microorganisms with particular insects over evolutionary time. This review will address the biology and ecology of phytopathogenic bacteria that interact with insects, including the traditional role of insects as vectors, as well as the newly emerging paradigm of insects serving as alternative primary hosts. Also discussed is one case where an insect serves as both host and vector, which may represent a transitionary stage in the evolution of insect-phytopathogen associations.
Plant and human pathogens have evolved disease factors to successfully exploit their respective hosts. Phytopathogens utilize specific determinants that help to breach reinforced cell walls and manipulate plant physiology to facilitate the disease process, while human pathogens use determinants for exploiting mammalian physiology and overcoming highly developed adaptive immune responses. Emerging research, however, has highlighted the ability of seemingly dedicated human pathogens to cause plant disease, and specialized plant pathogens to cause human disease. Such microbes represent interesting systems for studying the evolution of cross-kingdom pathogenicity, and the benefits and tradeoffs of exploiting multiple hosts with drastically different morphologies and physiologies. This review will explore cross-kingdom pathogenicity, where plants and humans are common hosts. We illustrate that while cross-kingdom pathogenicity appears to be maintained, the directionality of host association (plant to human, or human to plant) is difficult to determine. Cross-kingdom human pathogens, and their potential plant reservoirs, have important implications for the emergence of infectious diseases.
The genus Pantoea is a highly diverse group comprising free-living, and both pathogenic and non-pathogenic host-associating species. Pathogenic isolates have been found to infect insects, plants and humans, yet it is unclear whether these isolates have similar pathogenic potential to the free-living environmental populations. Using MLSA of six housekeeping genes, we evaluated the phylogenetic relationships among 115 environmental and clinical (human) isolates representing 11 Pantoea species. An overlay of the location of isolation onto the resulting tree revealed that clinical and environmental isolates are interspersed, and do not form distinctive groups. We then conducted quantitative growth assays of our isolates using maize, onion and fruit flies as hosts. Notably, most clinical isolates were able to grow in both plant hosts often comparably or even better than the environmental isolates. There were no obvious growth or host colonization patterns that could distinguish those isolates with clinical potential. Growth of an isolate in one host could not be predicted based on its performance in another host, nor could host growth be predicted by phylogeny or source of isolation. This work demonstrates that the host-colonizing capabilities of all Pantoea species groups is unpredictable, indicating a broader host range and pathogenic potential than currently assumed.
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