Hydration dynamics promote bacterial coexistence on rough surfaces

Abstract

Identification of mechanisms that promote and maintain the immense microbial diversity found in soil is a central challenge for contemporary microbial ecology. Quantitative tools for systematic integration of complex biophysical and trophic processes at spatial scales, relevant for individual cell interactions, are essential for making progress. We report a modeling study of competing bacterial populations cohabiting soil surfaces subjected to highly dynamic hydration conditions. The model explicitly tracks growth, motion and life histories of individual bacterial cells on surfaces spanning dynamic aqueous networks that shape heterogeneous nutrient fields. The range of hydration conditions that confer physical advantages for rapidly growing species and support competitive exclusion is surprisingly narrow. The rapid fragmentation of soil aqueous phase under most natural conditions suppresses bacterial growth and cell dispersion, thereby balancing conditions experienced by competing populations with diverse physiological traits. In addition, hydration fluctuations intensify localized interactions that promote coexistence through disproportional effects within densely populated regions during dry periods. Consequently, bacterial population dynamics is affected well beyond responses predicted from equivalent and uniform hydration conditions. New insights on hydration dynamics could be considered in future designs of soil bioremediation activities, affect longevity of dry food products, and advance basic understanding of bacterial diversity dynamics and its role in global biogeochemical cycles.

Microbial community response to hydration-desiccation cycles in desert soil

“…The recovery of diversity reflects the role of aqueous habitat fragmentation. As the degree of connectivity in the aqueous phase decreased, microbial interactions are spatially limited31. Essentially, the observed dynamics of community composition and diversity are the outcome of simultaneous effects of the competition over dissolved substrates and the temporary dominance of anaerobic taxa due the transition from oxic to anoxic conditions in some parts of the wet soil.…”

“…The model focuses on the putative role of aqueous phase connectivity. Following soil wetting, the increased connectivity of habitats facilitates higher rates of substrate diffusion and larger ranges of cell dispersion as key mechanisms for the observed loss of diversity during wetting3134. Furthermore, the detailed account of water configuration dynamics in the soil profile and associated oxygen diffusion suggest the possibility of establishing anoxic conditions following wetting that may last a day or two within the soil volume.…”

Trophic interactions induce spatial self-organization of microbial consortia on rough surfaces

“…Soil microorganisms are constrained to life in a fragmented and highly dynamic aqueous network in complex pore spaces that limit nutrient diffusion pathways, control cell dispersion rates, and shape interactions among microbial populations123456. The wide range of trophic interactions and the inherent variability of nutrient fluxes in soil give rise to the formation of microbial consortia that are considered important for maintaining stable ecological interactions within a complex and dynamic soil environment789.…”

Modeling microbial growth and dynamics

“…Other spatial soil or pore space models were directed at studying basic processes in microbial ecology (Dechesne et al 2010;Gharasoo et al 2012;Resat et al 2012;Wang and Or 2013;Wang and Or 2014). These models gave important insights into the microbial life in soils, for example showing how multiple strategies of resource utilization may reduce stochasticity in biofilm dynamics (Resat et al 2012), or how spatial segregation of cells is achieved either by temporal habitat fragmentation by varying hydration conditions (Wang and Or 2013) or simply by limits in chemotaxis that define a trophic interaction distance (Wang and Or 2014).…”

“…These models gave important insights into the microbial life in soils, for example showing how multiple strategies of resource utilization may reduce stochasticity in biofilm dynamics (Resat et al 2012), or how spatial segregation of cells is achieved either by temporal habitat fragmentation by varying hydration conditions (Wang and Or 2013) or simply by limits in chemotaxis that define a trophic interaction distance (Wang and Or 2014). Models from spatial statistics have been used to reveal such interaction distances between bacteria on the leaf surface and between bacteria and leaf surface structures (Esser et al 2015).…”