Multiple CheY Proteins Control Surface-Associated Lifestyles of Azospirillum brasilense

Abstract

Bacterial chemotaxis is the directed movement of motile bacteria in gradients of chemoeffectors. This behavior is mediated by dedicated signal transduction pathways that couple environment sensing with changes in the direction of rotation of flagellar motors to ultimately affect the motility pattern. Azospirillum brasilense uses two distinct chemotaxis pathways, named Che1 and Che4, and four different response regulators (CheY1, CheY4, CheY6, and CheY7) to control the swimming pattern during chemotaxis. Each of the CheY homologs was shown to differentially affect the rotational bias of the polar flagellum and chemotaxis. The role, if any, of these CheY homologs in swarming, which depends on a distinct lateral flagella system or in attachment is not known. Here, we characterize CheY homologs’ roles in swimming, swarming, and attachment to abiotic and biotic (wheat roots) surfaces and biofilm formation. We show that while strains lacking CheY1 and CheY6 are still able to navigate air gradients, strains lacking CheY4 and CheY7 are chemotaxis null. Expansion of swarming colonies in the presence of gradients requires chemotaxis. The induction of swarming depends on CheY4 and CheY7, but the cells’ organization as dense clusters in productive swarms appear to depend on functional CheYs but not chemotaxis per se. Similarly, functional CheY homologs but not chemotaxis, contribute to attachment to both abiotic and root surfaces as well as to biofilm formation, although these effects are likely dependent on additional cell surface properties such as adhesiveness. Collectively, our data highlight distinct roles for multiple CheY homologs and for chemotaxis on swarming and attachment to surfaces.

Rhizobial Chemotaxis and Motility Systems at Work in the Soil

“…A. brasilense has been observed to react with reverses and pauses and to modulate speed in response to chemical gradients (Zhulin and Armitage, 1993;Mukherjee et al, 2019). Numerous studies have revealed that the Che4 system modulates reversals by changing the rotation direction of the polar flagellum, while the Che1 system modulates swimming speed (Zhulin and Armitage, 1993;Bible et al, 2012;Mukherjee et al, 2016;Ganusova et al, 2021). In addition, the Che4 system, in concert with two orphan CheY proteins (CheY6 and CheY7), also modulates the pausing behavior, aerotaxis and the induction of swarming motility (Mukherjee et al, 2019;Ganusova et al, 2021).…”

“…Numerous studies have revealed that the Che4 system modulates reversals by changing the rotation direction of the polar flagellum, while the Che1 system modulates swimming speed (Zhulin and Armitage, 1993;Bible et al, 2012;Mukherjee et al, 2016;Ganusova et al, 2021). In addition, the Che4 system, in concert with two orphan CheY proteins (CheY6 and CheY7), also modulates the pausing behavior, aerotaxis and the induction of swarming motility (Mukherjee et al, 2019;Ganusova et al, 2021). The Che2 and Che3 systems do not appear to be involved in chemotaxis.…”