The microbial exometabolome: ecological resource and architect of microbial communities

Abstract

All microorganisms release many metabolites, collectively known as the exometabolome. The resultant multi-way cross-feeding of metabolites among microorganisms distributes resources, thereby increasing total biomass of the microbial community, and promotes the recruitment and persistence of phylogenetically and functionally diverse taxa in microbial communities. Metabolite transfer can also select for evolutionary diversification, yielding multiple closely related but functionally distinct strains. Depending on starting conditions, the evolved strains may be auxotrophs requiring metabolic outputs from producer cells or, alternatively, display loss of complementary reactions in metabolic pathways, with increased metabolic efficiency. Metabolite cross-feeding is widespread in many microbial communities associated with animals and plants, including the animal gut microbiome, and these metabolic interactions can yield products valuable to the host. However, metabolite exchange between pairs of intracellular microbial taxa that share the same host cell or organ can be very limited compared to pairs of free-living microorganisms, perhaps as a consequence of host controls over the metabolic function of intracellular microorganisms. Priorities for future research include the development of tools for improved quantification of metabolite exchange in complex communities and greater integration of the roles of metabolic cross-feeding and other ecological processes, including priority effects and antagonistic interactions, in shaping microbial communities. This article is part of the theme issue 'Conceptual challenges in microbial community ecology'.

Keywords: facilitation; metabolite cross-feeding; microbiome; reciprocity; syntrophy.

Figure 1.

Modes of metabolite exchange between pairs of microorganisms. (a) Facilitation, (b) syntrophy and (c) reciprocity. (Online version in colour.)

Figure 2.

Metabolic interactions in a three-member microbial community supported by butyrate as carbon source and inorganic ammonium as nitrogen source under anoxic conditions. (a) Syntrophic cross-feeding of waste products of butyrate degradation by Syntrophomonas to the hydrogenotrophic methanogen Methanoculleus and Desulfovibrio. (although Desulfovibrio is potentially able to reduce sulphate with concomitant consumption of hydrogen, sulphate reduction was not observed in this system.). (b) Reciprocal exchange of amino acids among the community members, inferred from their genetic capacity to synthesize the 20 amino acids, indicated by one-letter abbreviations (D, E, N, Q and G, which are synthesized by all three taxa, are not shown). (Drawn from data in figs 2 and 3 of [32]). (Online version in colour.)

Figure 3.

Metabolic cross-feeding between intracellular bacterial symbionts of insects. (a) Number of metabolites exchanged between bacteria (solid lines) and derived from host (dashed lines) in three species of xylem-feeding insects, as predicted from genome-scale metabolic models. (b) Genetic capacity of two bacterial symbionts (Tremblaya and Moranella) in the mealybug Planococcus citri for enzymes in the tryptophan biosynthesis pathway (cross, absent). (c) Genetic capacity of two genotypes of the bacterium Hodgkinia (I and II) in the cicada Tettigades undata for reactions in histidine biosynthesis. (Drawn from data in [64], fig. 2 of [65] and fig. 2 of [66]). (Online version in colour.)