UC San Diego

Quantitative studies of bacterial growth have historically focused on planktonic cells consuming dissolved substrates. In this work, we extend such studies to another important class of nutrients ubiquitous in nature: particulate substrates, not dissolvable in water. These substrates are the major nutrient sources in a variety of important natural ecosystems such as the ocean, soils, and guts, as well as synthetic ones, e.g., plastics. Understanding the interactions and growth of bacteria with such substrates is therefore vital, as it will allow to predict and manipulate the roles bacteria play in these important environments.Using chitin as a model structured substrate, we study its degradation by Vibrio sp. 1A01 and report a number of surprising findings. When culturing 1A01 with chitin flakes, we find that although chitin was the only source of nutrients in the cultures, the population had a high propensity for detachment and a majority of cells lived in the planktonic state. Despite this high detachment rate, the population was able to maintain an exponential rate of growth. Quantitative proteomic studies help elucidate how these cells manage to support high rates of dispersal while still replicating on the particles in spite of their low level of chitinase expression: secreted chitinases accumulate on particles, supporting the growth of the resident population of cells, irrespective of how many cells detached. This molecular “trick” enables the population to overcome the colonization/dispersal tradeoff often associated with growth on particles. Next, we formulated a spatiotemporal microscopic model of bacteria-chitin interactions constrained by our experimental data. Our model replicated experimental findings and provided rigorous definitions of the spatially separated subpopulations characterized above. In addition, we examined how microscopic parameters governing the local interaction of cells with particles translated to macroscopic features of the population such as growth rate and spatial extent. Finally, our model allowed us to probe regimes not accessible experimentally, particularly related to cultures starting from low-density initial conditions. We uncovered a 2-dimensional phase transition in the space of initial conditions where a critical number of both cells and enzymes is necessary for enabling growth. This allowed us to identify the mechanistic basis for the Allee effect in such systems. We discuss various mechanisms that constrain these initial conditions. Our results call for further studies of the physiology of starving cells and their transition to regrowth. Taken together our work is an experimental and theoretical attempt to tame the complexity of the various mechanisms governing growth in structured environments.