Metabolic and Demographic Feedbacks Shape the Emergent Spatial Structure and Function of Microbial Communities

Sylvie Estrela,Sam P. Brown,Stefano Allesina

doi:10.1371/journal.pcbi.1003398

Abstract

Microbes are predominantly found in surface-attached and spatially structured polymicrobial communities. Within these communities, microbial cells excrete a wide range of metabolites, setting the stage for interspecific metabolic interactions. The links, however, between metabolic and ecological interactions (functional relationships), and species spatial organization (structural relationships) are still poorly understood. Here, we use an individual-based modelling framework to simulate the growth of a two-species surface-attached community where food (resource) is traded for detoxification (service) and investigate how metabolic constraints of individual species shape the emergent structural and functional relationships of the community. We show that strong metabolic interdependence drives the emergence of mutualism, robust interspecific mixing, and increased community productivity. Specifically, we observed a striking and highly stable emergent lineage branching pattern, generating a persistent lineage mixing that was absent when the metabolic exchange was removed. These emergent community properties are driven by demographic feedbacks, such that aid from neighbouring cells directly enhances focal cell growth, which in turn feeds back to neighbour fecundity. In contrast, weak metabolic interdependence drives conflict (exploitation or competition), and in turn greater interspecific segregation. Together, these results support the idea that species structural and functional relationships represent the net balance of metabolic interdependencies.

Highlights

It is widely accepted that most polymicrobial communities living in natural environments form spatially structured and surface-attached consortia [1]
Microbial multispecies communities often show complex spatial structures and patterns of metabolic exchange, yet our understanding of how species spatial and ecological relationships emerge from the metabolic rules of species interactions is still limited
What mechanisms underlie multispecies community self-organization? In this study, we simulate the growth of a minimal—two species— community and show how the emergent properties of community spatial structure and function depend on the nature of metabolic interactions between the two species

Summary

Introduction

It is widely accepted that most polymicrobial communities living in natural environments form spatially structured and surface-attached consortia (biofilms) [1]. Empirical work in multispecies biofilms has acknowledged that species composition affects community structure and species distribution within the biofilm [4] as a result, for example, of mixing species that have distinct monoculture structures [5], or via metabolic interactions, such as cross-feeding [6,7,8,9] or detoxification of exogenous waste products [10]. The type of carbon source plays a major role in generating the diversity of spatial arrangements observed in polymicrobial communities, as varying the source of carbon likely alters the metabolic interactions between members of the community. In a two-species biofilm consisting of Burkholderia and Pseudomonas, Nielsen et al [8] observed that when the two species were competing for a common resource (non-cross-feeding medium), the biofilm consisted of separate microcolonies (high species segregation). When the two species were involved in a one-way obligate cross-feeding interaction (crossfeeding medium), the microcolonies consisted of both species (greater mixing)

Methods

Results

Discussion

Conclusion