Spatial organization in microbial range expansion emerges from trophic dependencies and successful lineages

Benedict Borer,Dani Or,David Johnson,Davide Ciccarese

doi:10.1038/s42003-020-01409-y

Benedict Borer, Dani Or + Show 2 more

Open Access

https://doi.org/10.1038/s42003-020-01409-y

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Abstract

Evidence suggests that bacterial community spatial organization affects their ecological function, yet details of the mechanisms that promote spatial patterns remain difficult to resolve experimentally. In contrast to bacterial communities in liquid cultures, surface-attached range expansion fosters genetic segregation of the growing population with preferential access to nutrients and reduced mechanical restrictions for cells at the expanding periphery. Here we elucidate how localized conditions in cross-feeding bacterial communities shape community spatial organization. We combine experiments with an individual based mathematical model to resolve how trophic dependencies affect localized growth rates and nucleate successful cell lineages. The model tracks individual cell lineages and attributes these with trophic dependencies that promote counterintuitive reproductive advantages and result in lasting influences on the community structure, and potentially, on its functioning. We examine persistence of lucky lineages in structured habitats where expansion is interrupted by physical obstacles to gain insights into patterns in porous domains.

Highlights

Evidence suggests that bacterial community spatial organization affects their ecological function, yet details of the mechanisms that promote spatial patterns remain difficult to resolve experimentally
We hypothesize that the spatial organization of sessile, crossfeeding bacterial assemblages undergoing range expansion is shaped by highly localized and dynamic differences in cell growth rates that are reinforced by feedbacks, or self-engineered of local nutrient landscape
We use a synthetic community containing two isogenic mutants of P. stutzeri A150128,31 cross-feeding nitrite in the denitrification pathway (Fig. 1a) to systematically investigate mechanisms, that shape the spatial self-organization of trophically interacting bacterial colonies during range expansion

Summary

Introduction

Evidence suggests that bacterial community spatial organization affects their ecological function, yet details of the mechanisms that promote spatial patterns remain difficult to resolve experimentally. Cross-feeding interactions, where one species relies on nutrients or modification of its imminent surroundings provided by another species within the assemblage[23] add constraints by the need for close proximity to the interacting partner The signature of such interactions is seen in the spatial organization of cells within the assemblage[24,25,26,27] with the potential of sequential expansion if trophic interactions are unilateral[28]. Our modelling framework provides novel mechanistic insights into experimental observations of spatial selforganization during bacterial range expansion, predicting a feedback between the emerging colony pattern and selfengineered nutrient landscape at a resolution currently inaccessible to experimental quantification These insights are used to visualize the importance of the spatial dimension in shaping the community composition concerning individual “lucky” bacterial lineages and potential ramification for evolutionary mechanisms

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