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Transient Surface Hydration Impacts Biogeography and Intercellular Interactions of Nonmotile Bacteria

Understanding the dynamics within microbiome communities is a challenge. Knowledge of phylogeny and spatial arrangement has led to increased understanding of numerous polymicrobial communities, yet these snapshots do not convey the dynamics of populations over time. ABSTRACT There are many hydrated surface niches that are neither static nor continuously flowing that are colonized by microbes such as bacteria. Such periodic hydrodynamic regimes are distinct from aquatic systems where microbial dissemination is reasonably predicted by assuming continuous flow or static systems where motile microbes largely control their own fate. Here, we show how nonmotile bacteria exhibit rapid, dispersive bursts of movement over surfaces using transient confluent hydration from the environment, which we term “surface hydrodispersion,” in which cells traverse thousands of cell lengths within minutes. The fraction of the population disseminated by surface hydrodispersion is small—on the order of 1 cell per million. Thus, surface hydrodispersion can promote isolated distribution of single cells, which is unlike other characterized active and passive surface motilities. We describe this translocation using a continuous-time random-walk modeling approach and found in computational simulations that transient fluid accumulation, dilution, and gravitational pull are the contributing factors. Surface hydrodispersion, consistent with advection, is unlike simple colony expansion, as it dramatically alters spatial relationships, shown in this study with Staphylococcus aureus, which becomes increasingly virulent when isolated from Corynebacterium striatum. Surface hydrodispersion of nonmotile bacteria exploiting transient fluid availability and gravity is a mechanism that can result in sporadic and sudden shifts in microbial community behavior. To better understand how this movement can impact biogeography on the millimeter scale, this work describes a system for study of primary factors behind this movement as well as a stochastic model describing this dispersal. IMPORTANCE Understanding the dynamics within microbiome communities is a challenge. Knowledge of phylogeny and spatial arrangement has led to increased understanding of numerous polymicrobial communities, yet these snapshots do not convey the dynamics of populations over time. The actual biogeography of any microbiome controls the potential interactions, governing any possible antagonistic or synergistic behavior. Accordingly, a shift in biogeography can enable new behavior. Little is known about the movement mechanisms of “nonmotile” microbes. Here, we characterize a universal means of movement we term hydrodispersion in which nonmotile bacteria are transported thousands of cell lengths in minutes. We show that only a small fraction of the population is translocated by hydrodispersion and describe this movement further using a random-walk mathematical model approach in silico. We demonstrate the importance of hydrodispersion by showing that Staphylococcus aureus can separate from a coculture inoculation with Corynebacterium striatum, thus permitting transition to a more virulent state.