Funded Grants

Life on leafs: Complex microbial cities on plant leaf surfaces

An average single plant leaf is home to about 10 million microbes living on its surface – similar to the population of New York City – so that diverse communities of hundreds of co-occurring bacterial species inhabit a single leaf. Microscopic images reveal that while some of these bacteria live as solitary cells, most live within multi-species aggregates of hundreds to thousands of cells. These aggregates can be conceptualized as the “condominiums” of the microbial city, with the valleys between epidermal cells as the main traffic arteries. A plethora of microbial interactions occur in this metropolis: Some compete for food or territory, some produce food for others, some give others a ride, and some produce toxins to attack others. These interactions, together with the microscale spatial heterogeneity of the leaf surface as a microbial habitat and the spatial constraints, are key to the organization of these “microbopoli” on the leaf surface.

A thought-provoking experiment is conducted by nature billions of times every day, when new leaves emerge and are colonized by microbes. As in human cities, leaves are first colonized by early settlers, followed by immigrants. Strikingly, in each such experiment, the community converges to a characteristic community composition with precise non-random spatial organization that is plant specific. The leaf surface’s physical, chemical, and biological properties render the robust community assembly even more puzzling. This is because leaf microbes live not in a liquid environment, but rather on a surface that is typically dry, constituting a serious limitation to transportation. How can we explain this repeatable self-organization of these complex communities? What are the underlying design principles that allow such robust self-organization?

Research in my lab centers on the phyllosphere – the above-ground parts of plants – which is dominated by plant leaves. Plant leaves offer an excellent model ecosystem for studying microbial ecology and the principles that govern complex communities’ self-organization on biotic surfaces. The phyllosphere is important, as these microbial populations are essential to plant health, growth, and function, while only a minor portion occasionally causes disease. The phyllosphere is a huge habitat: Earth’s total leaf surface area is about twice that of its land area. The total microbial phyllosphere population is vast (10^26 cells), as is its impact on global biogeochemical cycles.

My group is conducting an integrative study using systems-biology approaches combining theory, mathematical models, and computer simulations (e.g., individual-based simulations) with lab experiments and field sample analyses, while fully optimizing the latest research technologies such as single-cell genomics and advanced fluorescence microscopy. More specifically, we will:

1. Study the relationship between individual properties; the network of interactions between individuals and between species; the biological, physical, and chemical environment; and the emergent spatial organization patterns and dynamics of microbial communities on the leaf surface.
2. Lay the groundwork for a methodology for making predictions about the organization and dynamics of complex surface-related ecosystems.
3. Develop insights into emergent collective properties of complex communities such as the dramatic change in leaf wettability that is induced by microbial colonization and activity.