Fitness and stability of obligate cross-feeding interactions that emerge upon gene loss in bacteria

Abstract

Cross-feeding interactions, in which bacterial cells exchange costly metabolites to the benefit of both interacting partners, are very common in the microbial world. However, it generally remains unclear what maintains this type of interaction in the presence of non-cooperating types. We investigate this problem using synthetic cross-feeding interactions: by simply deleting two metabolic genes from the genome of Escherichia coli, we generated genotypes that require amino acids to grow and release other amino acids into the environment. Surprisingly, in a vast majority of cases, cocultures of two cross-feeding strains showed an increased Darwinian fitness (that is, rate of growth) relative to prototrophic wild type cells-even in direct competition. This unexpected growth advantage was due to a division of metabolic labour: the fitness cost of overproducing amino acids was less than the benefit of not having to produce others when they were provided by their partner. Moreover, frequency-dependent selection maintained cross-feeding consortia and limited exploitation by non-cooperating competitors. Together, our synthetic study approach reveals ecological principles that can help explain the widespread occurrence of obligate metabolic cross-feeding interactions in nature.

Distinct gene expression profile of Xanthomonas retroflexus engaged in synergistic multispecies biofilm formation

“…This hypothesis is supported by the observed gene regulation in the biosynthesis of costly amino acids and suggests that the cohabitants in multispecies biofilms may share products of energyconsuming pathways. Such division of labor has been shown to result in an overall higher fitness (Schink, 2002;Poltak and Cooper, 2011;Pande et al, 2014Pande et al, , 2015.…”

Metabolic cross-feeding via intercellular nanotubes among bacteria

“…Indeed, analysing cocultures of two E. coli genotypes that both required a different amino acid to grow, yet produced increased amounts of others, revealed a significant fitness advantage of cooperative cross-feeding relative to prototrophic WT cells 56 . Especially, the tremendous fitness advantage auxotrophic bacteria gain when the required metabolite is supplied externally [56][57][58] should exert a strong selection pressure that favours cross-feeding of essential metabolites among bacterial cells.…”

“…Indeed, analysing cocultures of two E. coli genotypes that both required a different amino acid to grow, yet produced increased amounts of others, revealed a significant fitness advantage of cooperative cross-feeding relative to prototrophic WT cells 56 . Especially, the tremendous fitness advantage auxotrophic bacteria gain when the required metabolite is supplied externally [56][57][58] should exert a strong selection pressure that favours cross-feeding of essential metabolites among bacterial cells. The enormous variation in gene content that is commonly found among different genomes of E. coli 59,60 , together with the observation that often seemingly essential biosynthetic functions are lost 56 may reflect the ability of E. coli to compensate its metabolic deficiencies by connecting to other cells.…”

Beyond the Black Queen Hypothesis

“…Recent experimental tests of evolutionary dynamics have shown that it may not be genome reduction itself, but particular and individual gene loss that confers the greatest advantages (Cooper et al, 2001;Lee and Marx, 2012;D'Souza et al, 2014;Pande et al, 2014), especially if the cell's lack of metabolite production is compensated by the habitat (D'Souza et al, 2014). The fitness gained from a given gene deletion is dependent on its metabolic function (for example, which metabolite it codes for) and on the position of the deletion in the metabolic pathway.…”