Flagellation of Shewanella oneidensis Impacts Bacterial Fitness in Different Environments

Abstract

Flagella occur on many prokaryotes, which primarily propel cells to move from detrimental to favorable environments. A variety of species-specific flagellation patterns have been identified. Although it is presumed that for each of these flagellated microorganisms, an evolutionarily fixed flagellation pattern is favored under the normal living conditions, direct evidence is lacking. Here, we use Shewanella oneidensis, a rod-shaped Gram-negative bacterium with a monotrichous polar flagellum (MR-1, the wild-type), as a research model. The investigation has been enabled by multiple mutants with diverse flagellation patterns that had been generated by removing FlhF and FlhG proteins that control flagellar location and number, respectively. Growth assays, as a measure of fitness, revealed that the wild-type strain predominated in spreading on swim plates and in pellicles which form at the air–liquid interface. However, under the pellicles where oxygen is limited, both aflagellated and monotrichous lateral strains showed similar increase in fitness, whereas strains with multiple flagella were less competitive. Moreover, under shaking culturing conditions, the aflagellated strain outcompeted all other strains, including the wild-type, suggesting that cells devoid of flagella would be more likely enriched upon agitation. Overall, these data support the presumption that the monotrichous polar flagellum, as evolutionarily fixed in the wild-type strain, is optimal for the growth fitness of S. oneidensis over any other mutants under most test conditions. However, upon specific changes of environmental conditions, another form could come to predominate. These findings provide insight into the impacts of flagellation patterns and function on bacterial adaptation to differing environments.