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An energy taxis transducer promotes root colonization by Azospirillum 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.

SUBMITTER: Greer-Phillips SE

PROVIDER: S-EPMC516605 | biostudies-literature | 2004 Oct

REPOSITORIES: biostudies-literature

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An energy taxis transducer promotes root colonization by Azospirillum brasilense.

Greer-Phillips Suzanne E SE Stephens Bonnie B BB Alexandre Gladys G

Journal of bacteriology 20041001 19

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 chemorecep ...[more]

PMID: 15375141

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Project description:Azospirillum is a plant growth promoting rhizobacteria (PGPR) with ability to produce several phytohormones such as auxins, mainly indole-3-acetic acid (IAA). The positive interaction of Azospirillum with plants has been simplified and explained through the bacterial capacity to produce IAA. Typical changes on root architecture by promoting the number of lateral roots and hair formation, and reducing the primary root length were established in inoculated plants. These changes increase the root surface improving the water and nutrients acquisition, and thus the growth of the whole plant. The mechanisms by which Azospirillum induces such changes fails to be explained only by the bacterial capacity to produce IAA. In this work, we have evaluated the root architecture and gene expression changes occurred in Arabidopsis thaliana inoculated with A. brasilense Az39 and the IAA-deficient mutant (Az39 ipdC-), or treated with exogenous IAA solution to confirm both, the IAA-dependent and IAA-independent Azospirillum´s pathways to promote the root growth. Our results demonstrate the ability of Az39 to modify the primary root development through IAA biosynthesis, while other IAA-independent mechanisms were related to an increase in the lateral roots development and the root hairs number. Jasmonates, ethylene and salicylic acid were increased in the IAA-deficient bacterial treatments, as the ipdC mutant significantly up-regulated transcription of genes enriched of these phytohormones signaling after 7 days. Further, the physical presence of the inactive bacteria (Az39φ) seems to mediate the development of root hairs, a mechanism common to other non-PGPR as E. coli DH5α. Our results suggest that Az39 inoculation induces morphological changes in root architecture through both IAA-dependent and independent mechanism. The IAA biosynthesis by Az39 reduces the primary root length; while the cells contact with the roots increases the root hairs production. Both the synthesis of active IAA and the presence of metabolically active Az39 cells increase the growth and development of lateral roots.

Project description:Plant roots shape the rhizosphere community by secreting compounds that recruit diverse bacteria. Colonization of various plant roots by the motile alphaproteobacterium Azospirillum brasilens e causes increased plant growth, root volume, and crop yield. Bacterial chemotaxis in this and other motile soil bacteria is critical for competitive colonization of the root surfaces. The role of chemotaxis in root surface colonization has previously been established by endpoint analyses of bacterial colonization levels detected a few hours to days after inoculation. More recently, microfluidic devices have been used to study plant-microbe interactions, but these devices are size limited. Here, we use a novel slide-in chamber that allows real-time monitoring of plant-microbe interactions using agriculturally relevant seedlings to characterize how bacterial chemotaxis mediates plant root surface colonization during the association of A. brasilens e with Triticum aestivum (wheat) and Medicago sativa (alfalfa) seedlings. We track A. brasilense accumulation in the rhizosphere and on the root surfaces of wheat and alfalfa. A. brasilense motile cells display distinct chemotaxis behaviors in different regions of the roots, including attractant and repellent responses that ultimately drive surface colonization patterns. We also combine these observations with real-time analyses of behaviors of wild-type and mutant strains to link chemotaxis responses to distinct chemicals identified in root exudates to specific chemoreceptors that together explain the chemotactic response of motile cells in different regions of the roots. Furthermore, the bacterial second messenger c-di-GMP modulates these chemotaxis responses. Together, these findings illustrate dynamic bacterial chemotaxis responses to rhizosphere gradients that guide root surface colonization.IMPORTANCE Plant root exudates play critical roles in shaping rhizosphere microbial communities, and the ability of motile bacteria to respond to these gradients mediates competitive colonization of root surfaces. Root exudates are complex chemical mixtures that are spatially and temporally dynamic. Identifying the exact chemical(s) that mediates the recruitment of soil bacteria to specific regions of the roots is thus challenging. Here, we connect patterns of bacterial chemotaxis responses and sensing by chemoreceptors to chemicals found in root exudate gradients and identify key chemical signals that shape root surface colonization in different plants and regions of the roots.

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An energy taxis transducer promotes root colonization by Azospirillum brasilense.

Publications

An energy taxis transducer promotes root colonization by Azospirillum brasilense.

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