Rare and localized events stabilize microbial community composition and patterns of spatial self-organization in a fluctuating environment

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.

Environmental and ecological controls of the spatial distribution of microbial populations in aggregates

“…To explore the intrinsic influence of eco-interactions on the development of microbial communities growing in aggregates, a multispecies system was simulated using individual-based modelling (IbM). Examples in literature of empirical tests have demonstrated the ability of IbM to make accurate predictions for real biological systems that can offer mechanistic explanations of underlying biological processes [19,22,23,[25][26][27][28][29][30][31].…”

Editorial: Fluctuating Habitats: Ecological Relevance of Environmental Variability and Predictability on Species, Communities, and Ecosystems

“…For instance, fluctuating conditions can mitigate the net impact of the corresponding stressor, increasing physiological tolerance and promoting adaptation to novel environmental conditions at all biological levels (Booth et al, 2021;Fusi et al, 2021). For microorganisms, in addition to spatial patterns, environmental fluctuations can determine localized spatial jackpot events that ensure persistence of strains across environmental dynamic conditions (Ciccarese et al, 2022). At the holobiont level, desert plants stabilize the associated bacterial community (e.g., stable composition) by modulating the release of exopolysaccharides therefore insulating the bacterial community around the rhizosphere, attaining the effect of daily and seasonal fluctuations.…”

Rhythmic Spatial Self-Organization of Bacterial Colonies

“… Examples of radial colony patterns that have been previously described for various microbes are highlighted. Different mechanisms can underlie the patterning, including (A) redox metabolism in P. aeruginosa ( 7 ); (B) expansion of the biomass of two metabolically interacting Pseudomonas stutzeri strains in response to cycling oxic/anoxic conditions ( 15 ); (C) dye-binding in P. putida ( 9 ); (D) sporulation and the nitrogen stress response in B. subtilis microcolonies ( 6 ); (E) developmental switch between motility and biofilm formation in Listeria monocytogenes ( 16 ); and (F and G) swarming behavior of Proteus mirabilis ( 17 ) and K. aerogenes ( 10 ). In P. putida and K. aerogenes , the cyclic changes described have been linked to the presence of a circadian clock.…”