title: 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 loss-of-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 sulfate-reducing bacterium can readily evolve to become a specialized syntroph, a situation that may have often occurred in nature.
authors.affiliation: Biological Sciences, University of Washington Bothell, Bothell, WA 98011; hilleskl@uw.edu.
authors.forename: Kristina L
authors.initials: KL
authors.lastname: Hillesland
authors.affiliation: Biological Sciences, University of Washington Bothell, Bothell, WA 98011;
authors.forename: Sujung
authors.initials: S
authors.lastname: Lim
authors.affiliation: Civil and Environmental Engineering, and.
authors.forename: Jason J
authors.initials: JJ
authors.lastname: Flowers
authors.affiliation: Institute for Systems Biology, Seattle, WA 98109-5234;
authors.forename: Serdar
authors.initials: S
authors.lastname: Turkarslan
authors.affiliation: Civil and Environmental Engineering, and Institute for Systems Biology, Seattle, WA 98109-5234;
authors.forename: Nicolas
authors.initials: N
authors.lastname: Pinel
authors.affiliation: Department of Biochemistry, University of Missouri, Columbia, MO 65211;
authors.forename: Grant M
authors.initials: GM
authors.lastname: Zane
authors.affiliation: Civil and Environmental Engineering, and.
authors.forename: Nicholas
authors.initials: N
authors.lastname: Elliott
authors.affiliation: Institute for Environmental Genomics and Department of Microbiology and Plant Biology, University of Oklahoma, Norman, OK 73019;
authors.forename: Yujia
authors.initials: Y
authors.lastname: Qin
authors.affiliation: Institute for Environmental Genomics and Department of Microbiology and Plant Biology, University of Oklahoma, Norman, OK 73019;
authors.forename: Liyou
authors.initials: L
authors.lastname: Wu
authors.affiliation: Institute for Systems Biology, Seattle, WA 98109-5234; Departments of Biology and Microbiology, Molecular and Cellular Biology Program, University of Washington Seattle, Seattle, WA 98195; Lawrence Berkeley National Laboratory, Berkeley, CA 94720; and.
authors.forename: Nitin S
authors.initials: NS
authors.lastname: Baliga
authors.affiliation: Institute for Environmental Genomics and Department of Microbiology and Plant Biology, University of Oklahoma, Norman, OK 73019; Earth Science Division, State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing 100084, China.
authors.forename: Jizhong
authors.initials: J
authors.lastname: Zhou
authors.affiliation: Department of Biochemistry, University of Missouri, Columbia, MO 65211;
authors.forename: Judy D
authors.initials: JD
authors.lastname: Wall
authors.affiliation: Civil and Environmental Engineering, and.
authors.forename: David A
authors.initials: DA
authors.lastname: Stahl
mesh_terms: D018920:Coculture Techniques; D016969:Desulfovibrio vulgaris / Q000235:genetics*; D019020:Directed Molecular Evolution; D017017:Methanococcus / Q000235:genetics*; D009154:Mutation / Q000235:genetics; D010084:Oxidation-Reduction; D010641:Phenotype; D013431:Sulfates / Q000378:metabolism; D013559:Symbiosis
chemical_list: D013431:Sulfates
keywords: coevolution; experimental evolution; sulfate-reducing prokaryote; syntrophy; trade-offs