As a microbial biome, the phyllosphere, or plant leaf surface, represents a highly heterogeneous landscape. We have a limited quantitative understanding of this heterogeneity, especially as it pertains to the structural and functional connectivity at micrometer dimensions and how this connectivity impacts the actions and interactions of microorganisms that colonize plant foliage at that scale. Newly developed tools, including bacterial bioreporters and topomimetic leaf surfaces, allow the interrogation of individual microbes for their experiences of the phyllosphere under highly controlled and reproducible experimental conditions. Here, we report on the use of such tools to ask basic questions about the role of the leaf waterscape (which we refer to as the phyllotelma), how this waterscape is a function of leaf surface topography, how it impacts the survival of microorganisms, facilitates dispersal, and affects the ability of microorganisms to sense their environment over short and long distances.
Results/Conclusions
Using a casting process, we generated artificial (polydimethylsiloxane-based) leaf surfaces to demonstrate that different leaf topographies differ in their ability to retain and shape waterscapes. By doing so, these topographies also variably impact the retention and distribution of bacteria along leaf surfaces. Leaf veins, for example, were found to interact with water to create corridors along which individual bacteria may be moved over distances that exceed their body length by many orders of magnitude. We showed that the ability of bacteria to sense chemicals on the leaf surface is predicted less well by the shortest path between the bacteria and the source of those chemicals, than by the often longer path that water follows as a function of local leaf topography. Our data greatly support efforts toward the formulation of spatially explicit models that predict patterns of leaf surface colonization by microorganisms and that have as a long-term goal the development of management strategies that interfere with the foliar establishment of unwanted microorganisms such as plant and human pathogens.