Abstract
Beneficial plant–microbe associations play critical roles in plant health. Bacterial chemotaxis provides a competitive advantage to motile flagellated bacteria in colonization of plant root surfaces, which is a prerequisite for the establishment of beneficial associations. Chemotaxis signaling enables motile soil bacteria to sense and respond to gradients of chemical compounds released by plant roots. This process allows bacteria to actively swim towards plant roots and is thus critical for competitive root surface colonization. The complete genome sequences of several plant-associated bacterial species indicate the presence of multiple chemotaxis systems and a large number of chemoreceptors. Further, most soil bacteria are motile and capable of chemotaxis, and chemotaxis-encoding genes are enriched in the bacteria found in the rhizosphere compared to the bulk soil. This review compares the architecture and diversity of chemotaxis signaling systems in model beneficial plant-associated bacteria and discusses their relevance to the rhizosphere lifestyle. While it is unclear how controlling chemotaxis via multiple parallel chemotaxis systems provides a competitive advantage to certain bacterial species, the presence of a larger number of chemoreceptors is likely to contribute to the ability of motile bacteria to survive in the soil and to compete for root surface colonization.
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References
Alexandre G, Greer SE, Zhulin IB (2000) Energy taxis is the dominant behavior in Azospirillum brasilense. J Bacteriol 182:6042–6048
Ames P, Bergman K (1981) Competitive advantage provided by bacterial motility in the formation of nodules by Rhizobium meliloti. J Bacteriol 148:728–908
Armitage JP, Gallagher A, Johnston AW (1988) Comparison of the chemotactic behaviour of Rhizobium leguminosarum with and without the nodulation plasmid. Mol Microbiol 2:743–748
Attmannspacher U, Scharf B, Schmitt R (2005) Control of speed modulation (chemokinesis) in the unidirectional rotary motor of Sinorhizobium meliloti. Mol Microbiol 56:708–718
Badri DV, Weir TL, van der Lelie D, Vivanco JM (2009) Rhizosphere chemical dialogues: plant–microbe interactions. Curr Opin Biotechnol 20:642–650
Bahlawane C, McIntosh M, Krol E, Becker A (2008) Sinorhizobium meliloti regulator MucR couples exopolysaccharide synthesis and motility. Mol Plant Microbe Interact 21:1498–1509
Bais HP, Park SW, Weir TL, Callaway RM, Vivanco JM (2004) How plants communicate using the underground information superhighway. Trends Plant Sci 9:26–32
Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Ann Rev Plant Biol 57:233–266
Barbour WM, Hattermann DR, Stacey G (1991) Chemotaxis of Bradyrhizobium japonicum to soybean exudates. Appl Env Microbiol 57:2635–2639
Barnett MJ et al (2001) Nucleotide sequence and predicted functions of the entire Sinorhizobium meliloti pSymA megaplasmid. Proc Natl Acad Sci USA 98:9883–9888
Bauer WD, Caetano-Anollés G (1990) Chemotaxis, induced gene expression and competitiveness in the rhizosphere. Plant Soil 129:45–52
Becker A et al (2004) Global changes in gene expression in Sinorhizobium meliloti 1021 under microoxic and symbiotic conditions. Molec Plant-Microbe Interact 17:292–303
Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486
Berleman JE, Bauer CE (2005) Involvement of a Che-like signal transduction cascade in regulating cyst cell development in Rhodospirillum centenum. Mol Microbiol 56:1457–1466
Bible AN, Stephens BB, Ortega DR, Xie Z, Alexandre G (2008) Function of a chemotaxis-like signal transduction pathway in modulating motility, cell clumping, and cell length in the alphaproteobacterium Azospirillum brasilense. J Bacteriol 190:6365–6375
Bible A, Russell MH, Alexandre G (2012) The Azospirillum brasilense Che1 chemotaxis pathway controls swimming velocity, which affects transient cell-to-cell clumping. J Bacteriol 194:3343–3355
Bowra BJ, Dilworth MJ (1981) Motility and chemotaxis towards sugars in Rhizobium leguminosarum. J Gen Microbiol 126:231–235
Bringhurst RM, Gage DJ (2002) Control of inducer accumulation plays a key role in succinate-mediated catabolite repression in Sinorhizobium meliloti. J Bacteriol 184:5385–5392
Buchan A, Crombie B, Alexandre GM (2010) Temporal dynamics and genetic diversity of chemotactic-competent microbial populations in the rhizosphere. Environ Microbiol 12:3171–3184
Burg D, Guillaume J, Tailliez R (1982) Chemotaxis by Rhizobium meliloti. Arch Microbiol 133:162–163
Caetano-Anollés G, Crist-Estes DK, Bauer WD (1988a) Chemotaxis of Rhizobium meliloti to the plant flavone luteolin requires functional nodulation genes. J Bacteriol 170:3164–3169
Caetano-Anollés G, Wall LG, De Micheli AT, Macchi EM, Bauer WD, Favelukes G (1988b) Role of motility and chemotaxis in efficiency of nodulation by Rhizobium meliloti. Plant Physiol 86:1228–1235
Caetano-Anollés G, Wrobel-Boerner E, Bauer WD (1992) Growth and movement of spot inoculated Rhizobium meliloti on the root surface of alfalfa. Plant Physiol 98:1181–1189
Capela D, Filipe C, Bobik C, Batut J, Bruand C (2006) Sinorhizobium meliloti differentiation during symbiosis with alfalfa: a transcriptomic dissection. Molec Plant-Microbe Interact 19:363–372
Charoenpanich P, Meyer S, Becker A, McIntosh M (2013) Temporal expression program of quorum sensing-based transcription regulation in Sinorhizobium meliloti. J Bacteriol 195:3224–3236
Dennis PG, Miller AJ, Hirsch PR (2010) Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiol Ecol 72:313–327
Dharmatilake AJ, Bauer WD (1992) Chemotaxis of Rhizobium meliloti towards nodulation gene-inducing compounds from alfalfa roots. Appl Environ Microbiol 58:1153–1158
Dogra G et al (2012) Sinorhizobium meliloti CheA complexed with CheS exhibits enhanced binding to CheY1, resulting in accelerated CheY1 dephosphorylation. J Bacteriol 194:1075–1087
Galibert F et al (2001) The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293:668–672
Gibson KE, Barnett MJ, Toman CJ, Long SR, Walker GC (2007) The symbiosis regulator CbrA modulates a complex regulatory network affecting the flagellar apparatus and cell envelope proteins. J Bacteriol 189:3591–3602
Götz R, Limmer N, Ober K, Schmitt R (1982) Motility and chemotaxis in two strains of Rhizobium with complex flagella. J General Microbiol 128:789–798
Greer-Phillips SE, Stephens BB, Alexandre G (2004) An energy taxis transducer promotes root colonization by Azospirillum brasilense. J Bacteriol 186:6595–6604
Gulash M, Ames P, Larosiliere RC, Bergman K (1984) Rhizobia are attracted to localized sites on legume roots. Appl Environ Microbiol 48:149–152
Hauwaerts D, Alexandre G, Das SK, Vanderleyden J, Zhulin IB (2002) A major chemotaxis gene cluster in Azospirillum brasilense and relationships between chemotaxis operons in α-proteobacteria. FEMS Microbiol Lett 208:61–67
Hazelbauer GL (2012) Bacterial chemotaxis: the early years of molecular studies. Ann Rev Microbiol 66:285–303. doi:10.1146/annurev-micro-092611-150120
Hazelbauer GL, Lai WC (2010) Bacterial chemoreceptors: providing enhanced features to two-component signaling. Curr Opin Microbiol 13:124–132
Hazelbauer GL, Falke JJ, Parkinson JS (2008) Bacterial chemoreceptors: high-performance signaling in networked arrays. Trends Biochem Sci 33:9–19
Heinrich D, Hess D (1985) Chemotactic attraction of Azospirillum lipoferum by wheat roots and characterization of some attractants. Can J Microbiol 31:26–31
Hoang HH, Gurich N, González JE (2008) Regulation of motility by the ExpR/Sin quorum-sensing system in Sinorhizobium meliloti. J Bacteriol 190:861–871
Janczarek M (2011) Environmental signals and regulatory pathways that influence exopolysaccharide production in rhizobia. Int J Molec Sci 12:7898–7933
Karunakaran R et al (2009) Transcriptomic analysis of Rhizobium leguminosarum biovar viciae in symbiosis with host plants Pisum sativum and Vicia cracca. J Bacteriol 191:4002–4014
Kirby JR, Zusman DR (2003) Chemosensory regulation of developmental gene expression in Myxococcus xanthus. Proc Natl Acad Sci USA 100:2008–2013
Kristich CJ, Ordal GW (2002) Bacillus subtilis CheD is a chemoreceptor modification enzyme required for chemotaxis. J Biol Chem 277:25356–25362
Lakshmanan V, Selvaraj G, Bais HP (2014) Functional soil microbiome: belowground solutions to an aboveground problem. Plant Physiol 166:689–700
Mandal SM, Chakraborty D, Dey S (2010) Phenolic acids act as signaling molecules in plant–microbe symbioses. Plant Signal Behav 5:359–368
Mandimba G, Heulin T, Bally R, Guckert A, Balandreau J (1986) Chemotaxis of free-living nitrogen-fixing bacteria towards maize mucilage. Plant Soil 90:129–139
McDougall BM, Rovira AD (1970) Sites of exudation of 14C-labelled compounds from wheat roots. New Phytol 69:999–1003
McIntosh M, Krol E, Becker A (2008) Competitive and cooperative effects in quorum-sensing-regulated galactoglucan biosynthesis in Sinorhizobium meliloti. J Bacteriol 190:5308–5317
McIntosh M, Meyer S, Becker A (2009) Novel Sinorhizobium meliloti quorum sensing positive and negative regulatory feedback mechanisms respond to phosphate availability. Mol Microbiol 74:1238–1256
Meier VM, Scharf BE (2009) Cellular localization of predicted transmembrane and soluble chemoreceptors in Sinorhizobium meliloti. J Bacteriol 191:5724–5733
Meier VM, Muschler P, Scharf BE (2007) Functional analysis of nine putative chemoreceptor proteins in Sinorhizobium meliloti. J Bacteriol 189:1816–1826
Miller LD, Yost CK, Hynes MF, Alexandre G (2007) The major chemotaxis gene cluster of Rhizobium leguminosarum bv. viciae is essential for competitive nodulation. Molec Microbiol 63:348–362
Moens S, Michiels K, Keijers V, Van Leuven F, Vanderleyden J (1995) Cloning, sequencing, and phenotypic analysis of laf1, encoding the flagellin of the lateral flagella of Azospirillum brasilense Sp7. J Bacteriol 177:5419–5426
Moens S, Schloter M, Vanderleyden J (1996) Expression of the structural gene, laf1, encoding the flagellin of the lateral flagella in Azospirillum brasilense Sp7. J Bacteriol 178:5017–5019
Morris J, González JE (2009) The novel genes emmABC are associated with exopolysaccharide production, motility, stress adaptation, and symbiosis in Sinorhizobium meliloti. J Bacteriol 191:5890–5900
Mukherjee A, Ghosh S (1987) Regulation of fructose uptake and catabolism by succinate in Azospirillum brasilense. J Bacteriol 169:4361–4367
Neumann S, Grosse K, Sourjik V (2012) Chemotactic signaling via carbohydrate phosphotransferase systems in Escherichia coli. Proc Natl Acad Sci USA 109:12159–12164
Parkinson JS, Hazelbauer GL, Falke JJ (2015) Signaling and sensory adaptation in Escherichia coli chemoreceptors: 2015 update. Trends Microbiol 23:257–266
Platzer J, Sterr W, Hausmann M, Schmitt R (1997) Three genes of a motility operon and their role in flagellar rotary speed variation in Rhizobium meliloti. J Bacteriol 179:6391–6399
Poole PS, Blyth A, Reid CJ, Walters K (1994) myo-Inositol catabolism and catabolite regulation in Rhizobium leguminosarum bv. viciae. Microbiology 140:2787–2795
Reinhold B, Hurek T, Fendrik I (1985) Strain-specific chemotaxis of Azospirillum spp. J Bacteriol 162:190–195
Robinson JB, Bauer WD (1993) Relationships between C4 dicarboxylic acid transport and chemotaxis in Rhizobium meliloti. J Bacteriol 175:2284–2291
Rosario MM, Kirby JR, Bochar DA, Ordal GW (1995) Chemotactic methylation and behavior in Bacillus subtilis: role of two unique proteins, CheC and CheD. Biochemistry 34:3823–3831
Rotter C, Mühlbacher S, Salamon D, Schmitt R, Scharf B (2006) Rem, a new transcriptional activator of motility and chemotaxis in Sinorhizobium meliloti. J Bacteriol 188:6932–6942
Sadasivan L, Neyra CA (1985) Flocculation in Azospirillum brasilense and Azospirillum lipoferum: exopolysaccharides and cyst formation. J Bacteriol 163:716–723
Sampedro I, Parales RE, Krell T, Hill JE (2015) Pseudomonas chemotaxis. FEMS Microbiol Rev 39:17–46
Scharf B (2002) Real-time imaging of fluorescent flagellar filaments of Rhizobium lupini H13-3: flagellar rotation and pH-induced polymorphic transitions. J Bacteriol 184:5979–5986
Siuti P, Green C, Edwards AN, Doktycz MJ, Alexandre G (2011) The chemotaxis-like Che1 pathway has an indirect role in adhesive cell properties of Azospirillum brasilense. FEMS Microbiol Lett 323:105–112
Sourjik V, Schmitt R (1996) Different roles of CheY1 and CheY2 in the chemotaxis of Rhizobium meliloti. Mol Microbiol 22:427–436
Sourjik V, Schmitt R (1998) Phosphotransfer between CheA, CheY1, and CheY2 in the chemotaxis signal transduction chain of Rhizobium meliloti. Biochemistry 37:2327–2335
Sourjik V, Sterr W, Platzer J, Bos I, Haslbeck M, Schmitt R (1998) Mapping of 41 chemotaxis, flagellar and motility genes to a single region of the Sinorhizobium meliloti chromosome. Gene 223:283–290
Sourjik V, Muschler P, Scharf B, Schmitt R (2000) VisN and VisR are global regulators of chemotaxis, flagellar, and motility genes in Sinorhizobium (Rhizobium) meliloti. J Bacteriol 182:782–788
Steenhoudt O, Vanderleyden J (2000) Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol Rev 24:487–506
Tambalo DD, Del Bel KL, Bustard DE, Greenwood PR, Steedman AE, Hynes MF (2010) Regulation of flagellar, motility and chemotaxis genes in Rhizobium leguminosarum by the VisN/R-Rem cascade. Microbiology 156:1673–1685
Ulrich LE, Zhulin IB (2009) The MiST2 database: a comprehensive genomics resource on microbial signal transduction. Nucleic Acids Res 38:D401–407
Uren NC (2000) Types, amounts and possible functions of compounds released into the rhizosphere by soil-grown plants. In: Pinton R, Varanini Z, Nannipiero P (eds) The rhizosphere: Biochemistry and organic substances at the soil–plant interface. Marcel Dekker, New York, pp 19–20
Van Bastelaere E, Lambrecht M, Vermeiren H, Van Dommelen A, Keijers V, Proost P, Vanderleyden J (1999) Characterization of a sugar-binding protein from Azospirillum brasilense mediating chemotaxis to and uptake of sugars. Molec Microbiol 32:703–714
Vande Broek A, Lambrecht M, Vanderleyden J (1998) Bacterial chemotactic motility is important for the initiation of wheat root colonization by Azospirillum brasilense. Microbiology 144:2599–2606
Wadhams GH, Armitage JP (2004) Making sense of it all: bacterial chemotaxis. Nature Rev Mol Cell Biol 5:1024–1037
Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51
Webb BA, Hildreth S, Helm RF, Scharf BE (2014) Sinorhizobium meliloti Chemoreceptor McpU mediates chemotaxis toward host plant exudates through direct proline sensing. Appl Environ Microbiol 80:3404–3415
Wisniewski-Dyé F et al (2011) Azospirillum genomes reveal transition of bacteria from aquatic to terrestrial environments. PLoS Genet 7:e1002430
Wuichet K, Zhulin IB (2010) Origins and diversification of a complex signal transduction system in prokaryotes. Sci Signal 3:ra50. doi:10.1126/scisignal.2000724
Xie Z, Ulrich LE, Zhulin IB, Alexandre G (2010) PAS domain containing chemoreceptor couples dynamic changes in metabolism with chemotaxis. Proc Natl Acad Sci USA 107:2235–2240
Yao SY et al (2004) Sinorhizobium meliloti ExoR and ExoS proteins regulate both succinoglycan and flagellum production. J Bacteriol 186:6042–6049
Yost CK, Rochepeau P, Hynes MF (1998) Rhizobium leguminosarum contains a group of genes that appear to code for methyl-accepting chemotaxis proteins. Microbiology 144:1945–1956
Yost CK, Clark KT, Del Bel KL, Hynes MF (2003) Characterization of the nodulation plasmid encoded chemoreceptor gene mcpG from Rhizobium leguminosarum. BMC Microbiol 3:1
Yost CK, Del Bel KL, Quandt J, Hynes MF (2004) Rhizobium leguminosarum methyl-accepting chemotaxis protein genes are down-regulated in the pea nodule. Arch Microbiol 182:505–513
Young JPW et al (2006) The genome of Rhizobium leguminosarum has recognizable core and accessory components. Genome Biol 7:R34. doi:10.1186/gb-2006-7-4-r34
Zatakia HM, Nelson CE, Syed UJ, Scharf BE (2014) ExpR coordinates the expression of symbiotically important, bundle-forming Flp pili with quorum sensing in Sinorhizobium meliloti. Appl Environ Microbiol 80:2429–2439
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Research in our laboratories is funded by NSF-330344 (GMA), NSF-1253234 (BES) and NSERC Canada RGPIN 2015-03926 (MFH). Any opinion, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the National Science Foundation.
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BES, MFH and GMA wrote and revised the manuscript and designed the figures and tables.
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Scharf, B.E., Hynes, M.F. & Alexandre, G.M. Chemotaxis signaling systems in model beneficial plant–bacteria associations. Plant Mol Biol 90, 549–559 (2016). https://doi.org/10.1007/s11103-016-0432-4
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DOI: https://doi.org/10.1007/s11103-016-0432-4