Niche engineering demonstrates a latent capacity for fungal-algal mutualism

Abstract

Mutualistic symbioses shape the evolution of species and ecosystems and catalyze the emergence of biological complexity, yet how such symbioses first form is unclear. We show that an obligate mutualism between the yeast Saccharomyces cerevisiae and the alga Chlamydomonas reinhardtii—two model eukaryotes with very different life histories—can arise spontaneously in an environment requiring reciprocal carbon and nitrogen exchange. This capacity for mutualism is phylogenetically broad, extending to other Chlamydomonas and fungal species. Furthermore, we witnessed the spontaneous association of Chlamydomonas algal cells physically interacting with filamentous fungi. These observations demonstrate that under specific conditions, environmental change induces free-living species to become obligate mutualists and establishes a set of experimentally tractable, phylogenetically related, synthetic systems for studying the evolution of symbiosis.

Microbial mutualism dynamics governed by dose-dependent toxicity of cross-fed nutrients

“…Overall, these data demonstrate that the external supply of NH 4 + breaks the reciprocal dependency of this syntrophy and allows E. coli to rapidly overtake the coculture due to its lower intrinsic generation time relative to that of R. palustris (2.5 h versus 9.9 h), and ultimately prevent R. palustris growth. These results, in combination with the acetate results discussed above, also corroborate the notion that stable coexistence relies on the metabolic dependence of the faster-growing species on its slower-growing partner and not the converse (Hom and Murray, 2014).…”

“…High cross-feeding levels can be detrimental to a mutualism Cross-feeding levels are inherently difficult to measure and yet are hypothesized to be a major determinant of mutualism dynamics and stability (Shou et al, 2007;Kim et al, 2008;Estrela et al, 2012;Hom and Murray, 2014). We therefore used our model to address the effect of NH 4 + -cross-feeding levels on mutualism dynamics.…”

“…As an alternative, synthetic microbial communities (cocultures) have been developed in which two or more species are cultivated together under laboratory conditions. Cocultures preserve core aspects of natural systems while offering greater practical experimental control (Shou et al, 2007;Hillesland and Stahl, 2010;Summers et al, 2010;Harcombe, 2010;Momeni et al, 2011;Hom and Murray, 2014;Mee et al, 2014). They are also more amenable to modeling than are natural systems and facilitate the development, experimental testing and refining of models for predicting community behavior (Zomorrodi and Segrè, 2015;Johns et al, 2016;Lindemann et al, 2016;Widder et al, 2016).…”

“…One factor that can promote cross-feeding in natural ecosystems is nutrient limitation, as crossfeeding can be a means by which to acquire scarce key nutrients (Shou et al, 2007;Klitgord and Segrè, 2010;Hom and Murray, 2014;Zelezniak et al, 2015). Limitation of bacterial growth is most commonly considered to result from nutrient deficiency; however, growth can also be influenced by diverse compounds that are inhibitory when abundant but serve as nutrients at lower concentrations (Abbott, 1973;Kunz et al, 1992;Alvarez et al, 2009;Barnhill et al, 2010).…”

Oscillatory dynamics in a bacterial cross-protection mutualism

“…So far, the majority of studies of microbial mutualisms have focused on cross-feeding, the mutually beneficial exchange of metabolites (10)(11)(12)(13)(14)(15)). Studies involving cross-feeding amino acid auxotrophs (10)(11)(12) found that the division of labor within the mutualism can increase the fitness of cross-feeding cocultures compared with a self-sufficient strain (10).…”