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Bacterial Colonization of Leaves: A Spectrum of Strategies

Bacteria associated with plant leaves, or phyllobacteria, probably employ a range of colonization strategies. Steps in these colonization strategies include modification of the leaf habitat, aggregation, ingression, and egression. Considerable evidence indicates that bacteria can modify their environment to enhance their colonization of plants, such as by increasing local nutrient concentrations or by producing a layer of extracellular polysaccharides. This local habitat modification may occur on the surface of leaves, as well as in the leaf interior, and may be enhanced by the formation of bacterial aggregates. The conspicuous presence of bacterial aggregates on leaves and the finding that the behavior of bacteria on plants varies in a density-dependent manner indicate the potential importance of cooperative interactions among phyllobacteria. Such cooperative interactions may occur among both homogeneous and heterogeneous populations, thus influencing the development of microbial communities. While the sites commonly colonized by most phyllobacteria have not been unambiguously identified, there is strong circumstantial evidence that a sizable proportion of cells, particularly of phytopathogenic strains, are localized within “protected sites” on plants. The likelihood that these protected sites are located in the interior of leaves indicates that phytopathogenic bacteria have access to more resources and greater protection from stresses associated with the leaf surface than bacteria that are restricted to the leaf surface. The internal and external leaf-associated populations probably form a continuum due to the processes of ingression and egression. For a specific pathogen, however, the extent of egression that occurs prior to disease induction is likely to influence the success of disease predictions based on external population size, i.e., the number of bacteria in leaf washings. In this review, we illustrate the complexity of the ecology of leaf-associated bacteria and propose a model of leaf colonization that emphasizes the common elements in bacterial colonization strategies, as well as allows for distinct behavior of different phyllobacterial species.