Myxococcus xanthus fruiting body morphology is important for spore recovery after exposure to environmental stress

Abstract

ABSTRACTEnvironmental microorganisms have evolved a variety of strategies to survive fluctuations in environmental conditions, including production of biofilms and differentiation into spores.Myxococcus xanthusare ubiquitous soil bacteria that produce starvation-induced multicellular fruiting bodies filled with environmentally resistant spores (a specialized biofilm). Fruiting bodies are thought to facilitate theM. xanthussocial life cycle by ensuring spores can germinateen masseinto a productive feeding community. Isolated spores have been shown to be more resistant than vegetative cells to heat, ultraviolet radiation, and desiccation, but it is unknown whether assembly of spores into a fruiting body provides additional protection from environmental insults. We developed a high-throughput method to compare the recovery (outgrowth) of distinct cell types (vegetative cells, free spores, and intact fruiting bodies) after exposure to ultraviolet radiation or desiccation. Our data indicate haystack-shaped fruiting bodies protect spores from extended UV radiation but do not provide additional protection from desiccation. Perturbation of fruiting body morphology strongly impedes recovery from both UV exposure and desiccation. These results hint that the distinctive fruiting bodies produced by different myxobacterial species may have evolved to optimize their persistence in distinct ecological niches.IMPORTANCEThe myxobacteria are environmentally ubiquitous social bacteria that influence the local microbial community composition. Understanding how these bacteria are affected by environmental insults is important in predicting how microbial biogeochemical cycling is affected by climate change. When starved, myxobacteria produce multicellular fruiting bodies filled with spores. As spores are resistant to a variety of environmental insults, it has long been held that the fruiting body evolved to ensure group germination into a productive feeding community. Using the model myxobacterium,Myxococcus xanthus, we demonstrate that the haystack-shaped fruiting body morphology enables significantly more resistance to UV exposure than the free spores. In contrast, fruiting bodies are slightly detrimental to recovery from extended desiccation, an effect that is strongly exaggerated if fruiting body morphology is perturbed. These results suggest the variety of fruiting body morphologies observed in the myxobacteria may dictate their relative resistance to changing climate conditions.