Abstract
Metabolic exchange is widespread in natural microbial communities and an important driver of ecosystem structure and diversity, yet it remains unclear what determines whether microbes evolve division of labor or maintain metabolic autonomy. Here we use a mechanistic model to study how metabolic strategies evolve in a constant, one resource environment, when metabolic networks are allowed to freely evolve. We find that initially identical ancestral communities of digital organisms follow different evolutionary trajectories, as some communities become dominated by a single, autonomous lineage, while others are formed by stably coexisting lineages that cross-feed on essential building blocks. Our results show how without presupposed cellular trade-offs or external drivers such as temporal niches, diverse metabolic strategies spontaneously emerge from the interplay between ecology, spatial structure, and metabolic constraints that arise during the evolution of metabolic networks. Thus, in the long term, whether microbes remain autonomous or evolve metabolic division of labour is an evolutionary contingency.
Highlights
Metabolic exchange is widespread in natural microbial communities and an important driver of ecosystem structure and diversity, yet it remains unclear what determines whether microbes evolve division of labor or maintain metabolic autonomy
Experimental evolution has shown how initially clonal populations can adaptively diversify into stably coexisting ecotypes, each specialised on pre-existing niches defined by available nutrients[1], spatial structure[2,11], temporal variability such as the feast and famine cycles in serial transfer[3,4,5,6,7,8,9], or combinations thereof[10]
Initially clonal Escherichia coli populations grown in a glucose-limited chemostat genetically diversify into a lineage that rapidly but inefficiently grows on the provided resource, and lineages that specialise in using the overflow acetate produced by the first lineage[4,13,15]
Summary
Metabolic exchange is widespread in natural microbial communities and an important driver of ecosystem structure and diversity, yet it remains unclear what determines whether microbes evolve division of labor or maintain metabolic autonomy. Natural microbial communities are typically complex, composed of many different taxonomic groups that stably coexist The complexity of these communities might partly reflect the complexity of their environment, which can generate and maintain diversity by allowing specialisation on different niches[1,2,3,4,5,6,7,8,9,10]. Cross-feeding might be caused by a gene loss ratchet in a community of initially autonomous microbes that, driven by escaping the burden of biosynthesis genes, evolve complementary metabolic networks and become dependent[30,31]
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