Erosion of functional independence early in the evolution of a microbial mutualism

Abstract

Many species have evolved to function as specialized mutualists, often to the detriment of their ability to survive independently. However, there are few, if any, well-controlled observations of the evolutionary processes underlying the genesis of new mutualisms. Here, we show that within the first 1,000 generations of initiating independent syntrophic interactions between a sulfate reducer (Desulfovibrio vulgaris) and a hydrogenotrophic methanogen (Methanococcus maripaludis), D. vulgaris frequently lost the capacity to grow by sulfate respiration, thus losing the primary physiological attribute of the genus. The loss of sulfate respiration was a consequence of mutations in one or more of three key genes in the pathway for sulfate respiration, required for sulfate activation (sat) and sulfate reduction to sulfite (apsA or apsB). Because lossof-function mutations arose rapidly and independently in replicated experiments, and because these mutations were correlated with enhanced growth rate and productivity, gene loss could be attributed to natural selection, even though these mutations should significantly restrict the independence of the evolved D. vulgaris. Together, these data present an empirical demonstration that specialization for a mutualistic interaction can evolve by natural selection shortly after its origin. They also demonstrate that a sulfatereducing bacterium can readily evolve to become a specialized syntroph, a situation that may have often occurred in nature.trade-offs | sulfate-reducing prokaryote | syntrophy | coevolution | experimental evolution F rom flowering plants and their pollinators to the microbial endosymbionts of insects, there are many examples in nature of obligate mutualists (1, 2), or species dependent upon a mutually beneficial interaction for their survival or reproduction. How these interactions evolve is a mystery because much theory predicts that cooperative interactions should be unstable (3) and because of the difficulty of inferring evolutionary events that occurred in the distant past (4). Although there are few, if any, empirical observations of evolution toward dependence on mutualism, there are now several examples of mutualisms evolving de novo in the laboratory (5-8). This advancement has provided researchers an experimental framework to study populations and ecological conditions in the early stages of evolution (5-8).Here, we describe our observations of rapid and repeated evolution of increased dependency on a mutualism through natural selection. This interaction is similar to a widespread relationship between prokaryotes that plays a pivotal role in the decomposition of carbon in many oxygen-free environments. In these syntrophic mutualisms, bacteria ferment organic acids, producing hydrogen or formate as by-products, which are then used by hydrogenconsuming species, often methanogenic archaea (9). Removal of hydrogen and formate benefits the bacteria because the free energy (ΔG) available decreases with increasing concentrations of these products (9). A variet...

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