Swimming performance of Bradyrhizobium diazoefficiens is an emergent property of its two flagellar systems

Abstract

Many bacterial species use flagella for self-propulsion in aqueous media. In the soil, which is a complex and structured environment, water is found in microscopic channels where viscosity and water potential depend on the composition of the soil solution and the degree of soil water saturation. Therefore, the motility of soil bacteria might have special requirements. An important soil bacterial genus is Bradyrhizobium, with species that possess one flagellar system and others with two different flagellar systems. Among the latter is B. diazoefficiens, which may express its subpolar and lateral flagella simultaneously in liquid medium, although its swimming behaviour was not described yet. These two flagellar systems were observed here as functionally integrated in a swimming performance that emerged as an epistatic interaction between those appendages. In addition, each flagellum seemed engaged in a particular task that might be required for swimming oriented toward chemoattractants near the soil inner surfaces at viscosities that may occur after the loss of soil gravitational water. Because the possession of two flagellar systems is not general in Bradyrhizobium or in related genera that coexist in the same environment, there may be an adaptive tradeoff between energetic costs and ecological benefits among these different species.

Transcriptional Control of the Lateral-Flagellar Genes of Bradyrhizobium diazoefficiens

“…One of these systems involves a subpolar flagellum closely related to the one in C. crescentus, while the other is characterized by lateral flagella similar to those in E. meliloti (20). The expression of each flagellar system is also different.…”

“…The expression of each flagellar system is also different. The subpolar system seems constitutive within a range of conditions; by contrast, the expression of the lateral system requires arabinose as a carbon source or viscosity in the culture medium or the presence of obstacles in the swimming path (20)(21)(22). Hence, growth in liquid medium with mannitol as the carbon source does not permit the expression of the lateral flagella.…”

“…Only the subpolar system, however, responds to chemotactic stimuli, whereas only the lateral system contributes to swimming in viscous-agar-containing medium (20). Although neither of these flagellar systems is required for the nodulation of soybean plants (30), bacterial motility might be essential for nodule occupation in competition against populations of compatible rhizobia in the soil (31).…”

“…In contrast to other species having dual flagellar systems that use one exclusively for swimming in a liquid medium and the other only for swarming on surfaces, both flagellar systems of B. diazoefficiens may be utilized together in liquid medium and interact to produce an emergent swimming performance that allows the bacterium to continually swim alongside solid surfaces (20). Only the subpolar system, however, responds to chemotactic stimuli, whereas only the lateral system contributes to swimming in viscous-agar-containing medium (20).…”

“…Bradyrhizobium diazoefficiens, the soybean N 2 -fixing symbiont, is a soil alphaproteobacterium that possesses two different flagellar systems with independent evolutionary origins (19,20). One of these systems involves a subpolar flagellum closely related to the one in C. crescentus, while the other is characterized by lateral flagella similar to those in E. meliloti (20).…”