Rapid evolution of stability and productivity at the origin of a microbial mutualism

Abstract

Mutualistic interactions are taxonomically and functionally diverse. Despite their ubiquity, however, the basic ecological and evolutionary processes underlying their origin and maintenance are poorly understood. A major reason for this is the lack of an experimentally tractable model system. We examine the evolution of an experimentally imposed obligate mutualism between sulfate-reducing and methanogenic microorganisms that have no known history of previous interaction. Twenty-four independent pairings (cocultures) of the bacterium Desulfovibrio vulgaris and the archaeon Methanococcus maripaludis were established and followed for 300 community doublings in two environments, one allowing for the development of a heterogeneous distribution of resources and the other not. Evolved cocultures grew up to 80% faster and were up to 30% more productive (biomass yield per mole of substrate) than the ancestors. The evolutionary process was marked by periods of significant instability leading to extinction of two of the cocultures, but it resulted in more stable, efficient, and productive mutualisms for most replicated pairings. Comparisons of evolved cocultures with those assembled from one evolved mutualist and one ancestral mutualist showed that evolution of both species contributed to improved productivity. Surprisingly, however, overall improvements in growth rate and yield were less than the sum of the individual contributions, suggesting antagonistic interactions between mutations from the coevolved populations. Physical constraints on the transfer of metabolites in the evolution environment affected the evolution of M. maripaludis, but not of D. vulgaris. Together, these results demonstrate that challenges can imperil nascent obligate mutualisms and demonstrate the evolutionary responses that enable their persistence and future evolution.

Fig. 1.

Coculture density at each transfer during the evolution experiment.

Fig. 2.

Improvements in growth rate and yield of cocultures after 300 generations of evolution. The growth rate (A) and yield (B) of uniform (solid bars) or heterogeneous (open bars) evolved cocultures and their ancestors was measured in both evolution environments. Bars indicate least squares means from the ANOVA results reported in Table S1, and error bars indicate SE.

Fig. 3.

Improvements in growth rate of each coculture caused by both evolved species together (open triangles), evolved D. vulgaris only (open circles), or evolved M. maripaludis only (white stars on solid squares). The average of four replicate measures for cocultures from the uniform environment and the heterogeneous environment are plotted separately in A and B, respectively. Error bars indicate 95% CIs.

Fig. 4.

Improvements in yield of each coculture caused by both evolved species together. Symbols and error bars are the same as in Fig. 3. The average of four replicate measures for cocultures from the uniform environment and the heterogeneous environment are plotted separately in A and B, respectively.