<i>Sinorhizobium meliloti</i> Chemotaxis to Multiple Amino Acids Is Mediated by the Chemoreceptor McpU

Webb, Benjamin A.; Compton, K. Karl; Campo, Julia S. Martín del; Taylor, Doris Mia; Sobrado, Pablo; Scharf, Birgit E.

doi:10.1094/mpmi-04-17-0096-r

Cited by 42 publications

(33 citation statements)

References 43 publications

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“…For example, malic acid that is present both in the root exudates of Arabidopsis thaliana and tomato, is a chemoattractant for B. subtilis (Rudrappa et al, ), R. pseudosolanacearum (Hida et al, ) and P. fluorescens (de Weert et al, ; Gupta Sood, ) and contributes to root colonization. Further examples illustrate that several of the other key attractants (fumaric and gluconic acids, Lys, Ser and Ala) that were identified in exudates of Cicer arietinum L., tomato and alfalfa, were also important attractants for rhizospheric microorganisms (Gitte et al, ; de Weert et al, ; Gupta Sood, ; Glekas et al, ; Webb et al, ). It appears that organic acids (especially the tricarboxylic acid cycle intermediates) and amino acids serve frequently as chemoattractants for various rhizobacteria (Bardy et al, ).…”

Section: Discussionmentioning

confidence: 99%

Recognition of dominant attractants by key chemoreceptors mediates recruitment of plant growth‐promoting rhizobacteria

Feng

Zhang

et al. 2019

Environmental Microbiology

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Summary Chemotaxis to plant root exudates is supposed to be a prerequisite for efficient root colonization by rhizobacteria. This is a highly multifactorial process since root exudates are complex compound mixtures of which components are recognized by different chemoreceptors. Little information is available as to the key components in root exudates and their receptors that drive colonization related chemotaxis. We present here the first global assessment of this issue using the plant growth‐promoting rhizobacterium (PGPR) Bacillus velezensis SQR9 (formerly B. amyloliquefaciens). This strain efficiently colonizes cucumber roots, and here, we show that chemotaxis to cucumber root exudates was essential in this process. We conducted chemotaxis assays using cucumber root exudates at different concentrations, individual exudate components as well as recomposed exudates, taking into account their concentrations detected in root exudates. Results indicated that two key chemoreceptors, McpA and McpC, were essential for root exudate chemotaxis and root colonization. Both receptors possess a broad ligand range and recognize most of the exudate key components identified (malic, fumaric, gluconic and glyceric acids, Lys, Ser, Ala and mannose). The remaining six chemoreceptors did not contribute to exudate chemotaxis. This study provides novel insight into the evolution of the chemotaxis system in rhizobacteria.

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Section: Discussionmentioning

confidence: 99%

Recognition of dominant attractants by key chemoreceptors mediates recruitment of plant growth‐promoting rhizobacteria

Feng

Zhang

et al. 2019

Environmental Microbiology

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“…The size of the ligand-binding domains of S. meliloti chemoreceptors varies greatly between 160 and 390 amino acid (aa) residues (30). Our group has shown that McpU and McpX play a role in host interaction by sensing plant-derived amino acids and quaternary ammonium compounds, respectively (31)(32)(33)(34). However, the function of the remaining six chemoreceptors is not known.…”

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confidence: 99%

Cellular Stoichiometry of Methyl-Accepting Chemotaxis Proteins in Sinorhizobium meliloti

et al. 2018

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The chemosensory system in has several important deviations from the widely studied enterobacterial paradigm. To better understand the differences between the two systems and how they are optimally tuned, we determined the cellular stoichiometry of the methyl-accepting chemotaxis proteins (MCPs) and the histidine kinase CheA in Quantitative immunoblotting was used to determine the total amount of MCPs and CheA per cell in The MCPs are present in the cell in high abundance (McpV), low abundance (IcpA, McpU, McpX, and McpW), and very low abundance (McpY and McpZ), whereas McpT was below the detection limit. The approximate cellular ratio of these three receptor groups is 300:30:1. The chemoreceptor-to-CheA ratio is 23.5:1, highly similar to that seen in (23:1) and about 10 times higher than that in (3.4:1). Different from, the high-abundance receptors in are lacking the carboxy-terminal NWETF pentapeptide that binds the CheR methyltransferase and CheB methylesterase. Using transcriptional fusions, we showed that chemoreceptors are positively controlled by the master regulators of motility, VisNR and Rem. In addition, FlbT, a class IIA transcriptional regulator of flagellins, also positively regulates the expression of most chemoreceptors except for McpT and McpY, identifying chemoreceptors as class III genes. Taken together, these results demonstrate that the chemosensory complex and the adaptation system in deviates significantly from the established enterobacterial paradigm but shares some similarities with The symbiotic soil bacterium is of great agricultural importance because of its nitrogen-fixing properties, which enhances growth of its plant symbiont, alfalfa. Chemotaxis provides a competitive advantage for bacteria to sense their environment and interact with their eukaryotic hosts. For a better understanding of the role of chemotaxis in these processes, detailed knowledge on the regulation and composition of the chemosensory machinery is essential. Here, we show that chemoreceptor gene expression in is controlled through the main transcriptional regulators of motility. Chemoreceptor abundance is much lower in than in and Moreover, the chemoreceptor-to-kinase CheA ratio is different from that of but similar to that of .

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“…Chemotaxis has been thoroughly established as a critical facet of nodule occupancy and competition in symbiotic rhizobacteria (15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)35). Plants exude a plethora of compounds, such as amino acids, sugars, organic acids, flavonoids, lipids, and ions (20,21,(36)(37)(38).…”

Section: Discussionmentioning

confidence: 99%

“…The functions of two of the eight chemoreceptors involved in S. meliloti chemotaxis have been elucidated. McpU is a general amino acid receptor, sensing all nonacidic proteogenic amino acids, as well as several nonproteogenic amino acids (16,25). McpX senses quaternary ammonium compounds (QACs), such as glycine betaine, trigonelline, and choline, through direct binding, and it is the first QAC chemoreceptor described in bacteria (17).…”

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confidence: 99%

Sinorhizobium meliloti Chemoreceptor McpV Senses Short-Chain Carboxylates via Direct Binding

et al. 2018

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is a soil-dwelling endosymbiont of alfalfa that has eight chemoreceptors to sense environmental stimuli during its free-living state. The functions of two receptors have been characterized, with McpU and McpX serving as general amino acid and quaternary ammonium compound sensors, respectively. Both receptors use a dual Cache (lcium channels and motaxis receptors) domain for ligand binding. We identified that the ligand-binding periplasmic region (PR) of McpV contains a single Cache domain. Homology modeling revealed that McpV is structurally similar to a sensor domain of a chemoreceptor with unknown function from , which crystallized with acetate in its binding pocket. We therefore assayed McpV for carboxylate binding and for carboxylate sensing. Differential scanning fluorimetry identified 10 potential ligands for McpV Nine of these are monocarboxylates with chain lengths between two and four carbons. We selected seven compounds for capillary assay analysis, which established positive chemotaxis of the wild type, with concentrations of peak attraction at 1 mM for acetate, propionate, pyruvate, and glycolate, and at 100 mM for formate and acetoacetate. Deletion of or mutation of residues essential for ligand coordination abolished positive chemotaxis to carboxylates. Using microcalorimetry, we determined that dissociation constants of the seven ligands with McpV were in the micromolar range. An McpV variant with a mutation in the ligand coordination site displayed no binding to isobutyrate or propionate. Of all the carboxylates tested as attractants, only glycolate was detected in alfalfa seed exudates. This work examines the relevance of carboxylates and their sensor to the rhizobium-legume interaction. Legumes share a unique association with certain soil-dwelling bacteria known broadly as rhizobia. Through concerted interorganismal communication, a legume allows intracellular infection by its cognate rhizobial species. The plant then forms an organ, the root nodule, dedicated to housing and supplying fixed carbon and nutrients to the bacteria. In return, the engulfed rhizobia, differentiated into bacteroids, fix atmospheric N into ammonium for the plant host. This interplay is of great benefit to the cultivation of legumes, such as alfalfa and soybeans, and is initiated by chemotaxis to the host plant. This study on carboxylate chemotaxis contributes to the understanding of rhizobial survival and competition in the rhizosphere and aids the development of commercial inoculants.

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Sinorhizobium meliloti Chemotaxis to Multiple Amino Acids Is Mediated by the Chemoreceptor McpU

Cited by 42 publications

References 43 publications

Recognition of dominant attractants by key chemoreceptors mediates recruitment of plant growth‐promoting rhizobacteria

Recognition of dominant attractants by key chemoreceptors mediates recruitment of plant growth‐promoting rhizobacteria

Cellular Stoichiometry of Methyl-Accepting Chemotaxis Proteins in Sinorhizobium meliloti

Sinorhizobium meliloti Chemoreceptor McpV Senses Short-Chain Carboxylates via Direct Binding

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