Rhizobial Chemotaxis and Motility Systems at Work in the Soil

Abstract

Bacteria navigate their way often as individual cells through their chemical and biological environment in aqueous medium or across solid surfaces. They swim when starved or in response to physical and chemical stimuli. Flagella-driven chemotaxis in bacteria has emerged as a paradigm for both signal transduction and cellular decision-making. By altering motility, bacteria swim toward nutrient-rich environments, movement modulated by their chemotaxis systems with the addition of pili for surface movement. The numbers and types of chemoreceptors reflect the bacterial niche and lifestyle, with those adapted to complex environments having diverse metabolic capabilities, encoding far more chemoreceptors in their genomes. The Alpha-proteobacteria typify the latter case, with soil bacteria such as rhizobia, endosymbionts of legume plants, where motility and chemotaxis are essential for competitive symbiosis initiation, among other processes. This review describes the current knowledge of motility and chemotaxis in six model soil bacteria: Sinorhizobium meliloti, Agrobacterium fabacearum, Rhizobium leguminosarum, Azorhizobium caulinodans, Azospirillum brasilense, and Bradyrhizobium diazoefficiens. Although motility and chemotaxis systems have a conserved core, rhizobia possess several modifications that optimize their movements in soil and root surface environments. The soil provides a unique challenge for microbial mobility, since water pathways through particles are not always continuous, especially in drier conditions. The effectiveness of symbiont inoculants in a field context relies on their mobility and dispersal through the soil, often assisted by water percolation or macroorganism movement or networks. Thus, this review summarizes the factors that make it essential to consider and test rhizobial motility and chemotaxis for any potential inoculant.

Keywords: Azospirillum brasilense; Bradyrhizobium diazoefficiens; Rhizobium leguminosarum; Sinorhizobium meliloti; chemotaxis; motility; rhizobia; soil.

Figure 1

Escherichia coli and rhizobial motility models. (A) The E. coli peritrichous flagella provides thrust through counterclockwise rotation and tumbles through clockwise rotation causing the flagella bundle to dissociate. (B) The Sinorhizobium meliloti and Agrobacterium fabacearum peritrichous flagella provide thrust through clockwise rotation and tumbles through speed modulation causing the flagella bundle to dissociate. This speed modulation is controlled by MotC, stabilized by MotE. The reversed direction is due to the heterogeneous filament proteins producing a right-handed striated filament. (C) The Rhizobium leguminosarum subpolar flagella also provide thrust through clockwise rotation and tumbles through speed modulation, although they do not form a flagella bundle. The R. leguminosarum flagella also have heterogeneous filaments, although they are not visibly striated. (D) The Azorhizobium caulinodans flagella are not well-studied but may match either (B) or (C), having the MotC and MotE accessory proteins. (E) Azospirillum brasilense produces two flagella types: a polar flagellum covered by a polysaccharide sheath that provides thrust through counterclockwise rotation, reverses through clockwise rotation and can pause by stopping the motor; and lateral flagella matching (A). (F) Bradyrhizobium diazoefficiens produces two flagella types: a subpolar flagellum that provides thrust through counterclockwise rotation and reverses through clockwise rotation; and lateral flagella matching (C) that can cause tumbles.

Figure 2

Escherichia coli and rhizobial chemotaxis systems. (A) Typical MCP (methyl-accepting chemotaxis protein) chemoreceptor domain structure including transmembrane domains flanking a periplasmic sensor domain. In the cytoplasm, the receptors form a coiled coil of alpha helices down to the CheA binding domain and returning to the plasma membrane to complete the coiled coil. Methylation and demethylation occur at sites along the coiled coil. The number of helix repeats varies, with some MCPs containing 34, 36, 38 or 40 repeats (classes 34H, 36H, 38H, and 40H, respectively). (B) The chemotaxis clusters of Escherichia coli and various rhizobia. Most clusters consist of the che genes A, Y, W, R, and B. E. coli K12 substr. MG1655 has one cluster of class F7 containing an extra cheZ gene and two MCP genes. Sinorhizobium meliloti RU11 has two clusters: one of class F7 containing extra che genes Y, S, D, and T and one MCP gene; and one of class ACF containing the standard genes except an altered cheA-REC, missing cheY and one MCP gene. Rhizobium leguminosarum biovar viciae 3841 has two clusters: one of class F7 containing extra che genes Y, S, D, and T and one MCP gene; and one of class F8 containing an extra cheW and three MCP genes. Agrobacterium fabacearum H13-3 has two clusters: one of class F7 containing extra che genes Y, S, D, and T and one MCP gene but missing cheW; and one of class F8 containing an extra cheW and one MCP gene. Azorhizobium caulinodans ORS571 has one cluster of class F5 containing the standard genes and one MCP gene; and 37 kb upstream the che genes Y and Z. Azospirillum brasilense Sp7 has four clusters: one of class F5 containing the standard genes; and one of class F7 containing the standard genes, cheD and two MCP genes. The two clusters not shown have not been linked to chemotaxis. Bradyrhizobium diazoefficiens USDA110 has three clusters: one of class F5 containing two extra cheY genes and one operon reading frame but missing cheB; one of class F5 containing the standard genes; and one of class F8 containing an extra cheW gene and three MCP genes.

Figure 3

Bacterial mobility methods and challenges in soil. Microbial passage through the soil is dependent on sufficient moisture content to produce continuous pathways through water. Without rain or irrigation, air pockets form within the soil and prevent microbial passage. To combat this, microbes can exploit macroorganisms through methods including traversal along plant roots, navigation of fungal hyphae or hitching a ride on or in mobile macroorganisms. These mobility methods and challenges in soil are important for symbiont inoculation of crop plants. The two main inoculation techniques are on-seed, which although economical does not provide much dispersal, and in-furrow, which requires large amounts of inoculated soil but provides extensive dispersal.