Novel Transcriptome Patterns Accompany Evolutionary Restoration of Defective Social Development in the Bacterium Myxococcus xanthus

Abstract

Evolutionary trait losses can be restored by direct reversion or by compensatory pathways. Upon starvation, the bacterium Myxococcus xanthus develops into spore-bearing fruiting bodies, but this ability can be rapidly lost during evolution. Some developmentally defective strains of M. xanthus "cheat" on proficient strains during development by superior sporulation in mixed cultures. Here, we examine transcriptomic patterns accompanying the evolution of a cheater (obligate cheater [OC]) to a developmentally competent strain (PX) by a single mutation. Using quantitative real-time-polymerase chain reaction analysis of 5 genes essential for development, we initially show that restoration of development in strain PX was associated with increased expression of 4 of these genes, not only relative to OC but also relative to the developmentally proficient ancestor of both OC and PX (wild type [WT]). Global transcriptome analyses showed further that developmental expression of well more than 100 genes differ significantly between PX and the proficient WT ancestor. Moreover, the expression profile of PX was found to differ from that of WT more than does that of the defective intermediate strain OC. These results show that the restoration of a complex trait is accompanied by novel expression patterns across a large number and wide variety of genes, rather than by a large-scale return to ancestral expression patterns.