An Energy Taxis Transducer Promotes Root Colonization byAzospirillum brasilense

Abstract

Motility responses triggered by changes in the electron transport system are collectively known as energy taxis. In Azospirillum brasilense, energy taxis was shown to be the principal form of locomotor control. In the present study, we have identified a novel chemoreceptor-like protein, named Tlp1, which serves as an energy taxis transducer. The Tlp1 protein is predicted to have an N-terminal periplasmic region and a cytoplasmic C-terminal signaling module homologous to those of other chemoreceptors. The predicted periplasmic region of Tlp1 comprises a conserved domain that is found in two types of microbial sensory receptors: chemotaxis transducers and histidine kinases. However, the function of this domain is currently unknown. We characterized the behavior of a tlp1 mutant by a series of spatial and temporal gradient assays. The tlp1 mutant is deficient in (i) chemotaxis to several rapidly oxidizable substrates, (ii) taxis to terminal electron acceptors (oxygen and nitrate), and (iii) redox taxis. Taken together, the data strongly suggest that Tlp1 mediates energy taxis in A. brasilense. Using qualitative and quantitative assays, we have also demonstrated that the tlp1 mutant is impaired in colonization of plant roots. This finding supports the hypothesis that energy taxis and therefore bacterial metabolism might be key factors in determining host specificity in Azospirillum-grass associations.Azospirillum brasilense, a free-living diazotroph that belongs to the alpha-subdivision of proteobacteria, associates with the roots of many agriculturally important crops, including wheat, corn, and rice. Azospirilla colonize the root surface and may significantly promote plant growth and crop yield, properties that make them attractive candidates for the development of biological fertilizers for these crops (26-28). The ability of Azospirillum to attain significant populations on the root surfaces of the host is essential for its beneficial effect on plant growth and requires that the bacteria come in close contact with the roots (9,27,28,35). The abilities of sensing chemicals released by the host plant and navigating toward the root system are likely to be important for the establishment of bacteria, including Azospirillum (9, 10, 42), in the rhizosphere. Experimental evidence supporting this hypothesis was obtained by demonstrating that nonchemotactic and nonmotile mutants of A. brasilense are severely impaired in surface colonization of wheat roots (41). Although there is no strict host specificity in Azospirillum-plant associations, a strain-specific chemotaxis was reported: strains isolated from the rhizosphere of a particular grass demonstrated preferential chemotaxis toward chemicals found in root exudates of that grass (31). These results suggested that chemotaxis may contribute to host-plant specificity and could largely be determined by metabolism (31).Most motility responses in A. brasilense are a particular form of metabolism-dependent taxis called energy taxis (1). In energy taxis, a flow of reducing equ...

PAS domain containing chemoreceptor couples dynamic changes in metabolism with chemotaxis

“…Given the ecological advantage provided by energy taxis (24), energy taxis transducers are expected to be widespread in bacteria; however, only a few have been identified thus far (7,8,10,14,15). Here we characterize an energy taxis chemoreceptor, AerC, in the nitrogen-fixing bacterium, A. brasilense.…”

“…In A. brasilense, a transmembrane chemoreceptor Tlp1 modulates many energy taxis responses (10). The sensory domain of Tlp1 is located in the periplasm and lacks a recognizable motif for redox or energy sensing, and thus the energy-related parameter sensed by Tlp1 is unknown (10).…”

“…In E. coli, two of the five chemoreceptors have been implicated in mediating energy taxis: Aer, which senses the redox status via an FAD cofactor (7,8) and Tsr, which likely monitors the proton motive force (8,9). In A. brasilense, a transmembrane chemoreceptor Tlp1 modulates many energy taxis responses (10). The sensory domain of Tlp1 is located in the periplasm and lacks a recognizable motif for redox or energy sensing, and thus the energy-related parameter sensed by Tlp1 is unknown (10).…”

Cyclic di-GMP: the First 25 Years of a Universal Bacterial Second Messenger

“…In the alphaproteobacterium Azospirillum brasilense, the MCP Tlp1 plays a key role in energy taxis and colonization of plant roots (218). Tlp1 contains a C-terminal PilZ domain (48) that binds c-di-GMP with low-micromolar affinity (218a).…”

Chemotaxis Is Required for Virulence and Competitive Fitness of the Bacterial Wilt Pathogen Ralstonia solanacearum

“…Bacterial taxis is directly involved in interactions with both animal and plant hosts (16,17,21,38,53). Taxis, especially chemotaxis, together with its mechanism of signal transduction and response regulation, has been well studied in Escherichia coli (32,48).…”