Abstract
Spatial self-organization is a hallmark of surface-associated microbial communities that is governed by local environmental conditions and further modified by interspecific interactions. Here, we hypothesize that spatial patterns of microbial cell-types can stabilize the composition of cross-feeding microbial communities under fluctuating environmental conditions. We tested this hypothesis by studying the growth and spatial self-organization of microbial co-cultures consisting of two metabolically interacting strains of the bacterium Pseudomonas stutzeri. We inoculated the co-cultures onto agar surfaces and allowed them to expand (i.e. range expansion) while fluctuating environmental conditions that alter the dependency between the two strains. We alternated between anoxic conditions that induce a mutualistic interaction and oxic conditions that induce a competitive interaction. We observed co-occurrence of both strains in rare and highly localized clusters (referred to as “spatial jackpot events”) that persist during environmental fluctuations. To resolve the underlying mechanisms for the emergence of spatial jackpot events, we used a mechanistic agent-based mathematical model that resolves growth and dispersal at the scale relevant to individual cells. While co-culture composition varied with the strength of the mutualistic interaction and across environmental fluctuations, the model provides insights into the formation of spatially resolved substrate landscapes with localized niches that support the co-occurrence of the two strains and secure co-culture function. This study highlights that in addition to spatial patterns that emerge in response to environmental fluctuations, localized spatial jackpot events ensure persistence of strains across dynamic conditions.
Highlights
Microbial communities frequently experience perturbations and spatiotemporal fluctuations in their local environmental conditions [1,2,3,4,5,6]
The number of spatial jackpot events depend on pH We tested whether the number of spatial jackpot events that emerge during range expansion depend on the pH, and on the strength of the mutualistic interaction
Using a microbial co-culture consisting of two strains that cross-feed nitrite (NO2−) under anoxic conditions and compete under oxic conditions, we conducted a series of range expansion experiments and complemented experimental observations with insights gained from a mechanistic agent-based model that mimics the experimental conditions
Summary
Microbial communities frequently experience perturbations and spatiotemporal fluctuations in their local environmental conditions [1,2,3,4,5,6]. The two strains differ at only single genetic loci [46], preventing potential confounding effects that might otherwise occur if more distantly related strains were used Both strains have an intact periplasmic nitrate reductase encoded by the nap genes; this the presence of a specific cell-type at the expansion edge may result from stochastic processes that do not require beneficial mutations. Spatial selforganization during range expansion has been frequently studied under steady-state conditions (e.g., stable redox conditions), further attention is required to understand how environmental perturbations and fluctuations affect microbial interactions and spatial self-organization. We hypothesized that temporal fluctuations in environmental conditions that alter the nature of interspecific interactions can lead to irreversible transitions in spatial patterns of cell-types, affecting co-culture composition and metabolic functioning. The anoxic growth rates of the two strains with nitrate (NO3−) or nitrite (NO2−) are approximately three-fold slower when compared to their oxic
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