Abstract

Patterns of spatial positioning of individuals within microbial communities are often critical to community function. However, understanding patterning in natural communities is hampered by the multitude of cell-cell and cell-environment interactions as well as environmental variability. Here, through simulations and experiments on communities in defined environments, we examined how ecological interactions between two distinct partners impacted community patterning. We found that in strong cooperation with spatially localized large fitness benefits to both partners, a unique pattern is generated: partners spatially intermixed by appearing successively on top of each other, insensitive to initial conditions and interaction dynamics. Intermixing was experimentally observed in two obligatory cooperative systems: an engineered yeast community cooperating through metabolite-exchanges and a methane-producing community cooperating through redox-coupling. Even in simulated communities consisting of several species, most of the strongly-cooperating pairs appeared intermixed. Thus, when ecological interactions are the major patterning force, strong cooperation leads to partner intermixing.DOI:http://dx.doi.org/10.7554/eLife.00230.001.

Highlights

  • Biological interactions drive pattern formation at different levels of organization (Murray, 2003), ranging from developmental patterning within multicellular organisms and biofilms (Shapiro, 1998; Lewis, 2008; Vlamakis et al, 2008; Chuong and Richardson, 2009), to ecological patterning within multispecies communities (Levin, 1992; Rietkerk and van de Koppel, 2008; Momeni et al, 2011)

  • There are six possibilities:[∼ ∼], [∼ ↑], [∼ ↓], [↓ ↓], [↓ ↑], and [↑ ↑]

  • The identities of partners may be added to the notation such that A[↓ ↑]B would mean that the overall interaction inhibits A and promotes B

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Summary

Introduction

Biological interactions drive pattern formation at different levels of organization (Murray, 2003), ranging from developmental patterning within multicellular organisms and biofilms (Shapiro, 1998; Lewis, 2008; Vlamakis et al, 2008; Chuong and Richardson, 2009), to ecological patterning within multispecies communities (Levin, 1992; Rietkerk and van de Koppel, 2008; Momeni et al, 2011). Understanding the mechanistic basis of pattern formation from observations of natural communities is stymied by the multitude of cell–cell and cell–environment interactions, as well as environmental variations within and across communities. It is not uncommon to observe qualitatively different patterns in samples of essentially the same type of community (Christensen et al, 2002; Wilmes et al, 2008; Dekas et al, 2009)

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