Advertisement

Plant Molecular Biology

, Volume 90, Issue 6, pp 549–559 | Cite as

Chemotaxis signaling systems in model beneficial plant–bacteria associations

  • Birgit E. Scharf
  • Michael F. Hynes
  • Gladys M. AlexandreEmail author
Article

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.

Keywords

Flagella Motility Nitrogen fixation Rhizosphere Signal transduction Symbiosis 

Notes

Acknowledgments

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.

Author’s contribution

BES, MFH and GMA wrote and revised the manuscript and designed the figures and tables.

References

  1. Alexandre G, Greer SE, Zhulin IB (2000) Energy taxis is the dominant behavior in Azospirillum brasilense. J Bacteriol 182:6042–6048CrossRefPubMedPubMedCentralGoogle Scholar
  2. Ames P, Bergman K (1981) Competitive advantage provided by bacterial motility in the formation of nodules by Rhizobium meliloti. J Bacteriol 148:728–908PubMedPubMedCentralGoogle Scholar
  3. Armitage JP, Gallagher A, Johnston AW (1988) Comparison of the chemotactic behaviour of Rhizobium leguminosarum with and without the nodulation plasmid. Mol Microbiol 2:743–748CrossRefPubMedGoogle Scholar
  4. Attmannspacher U, Scharf B, Schmitt R (2005) Control of speed modulation (chemokinesis) in the unidirectional rotary motor of Sinorhizobium meliloti. Mol Microbiol 56:708–718CrossRefPubMedGoogle Scholar
  5. Badri DV, Weir TL, van der Lelie D, Vivanco JM (2009) Rhizosphere chemical dialogues: plant–microbe interactions. Curr Opin Biotechnol 20:642–650CrossRefPubMedGoogle Scholar
  6. Bahlawane C, McIntosh M, Krol E, Becker A (2008) Sinorhizobium meliloti regulator MucR couples exopolysaccharide synthesis and motility. Mol Plant Microbe Interact 21:1498–1509CrossRefPubMedGoogle Scholar
  7. Bais HP, Park SW, Weir TL, Callaway RM, Vivanco JM (2004) How plants communicate using the underground information superhighway. Trends Plant Sci 9:26–32CrossRefPubMedGoogle Scholar
  8. 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 57:233–266CrossRefGoogle Scholar
  9. Barbour WM, Hattermann DR, Stacey G (1991) Chemotaxis of Bradyrhizobium japonicum to soybean exudates. Appl Env Microbiol 57:2635–2639Google Scholar
  10. Barnett MJ et al (2001) Nucleotide sequence and predicted functions of the entire Sinorhizobium meliloti pSymA megaplasmid. Proc Natl Acad Sci USA 98:9883–9888CrossRefPubMedPubMedCentralGoogle Scholar
  11. Bauer WD, Caetano-Anollés G (1990) Chemotaxis, induced gene expression and competitiveness in the rhizosphere. Plant Soil 129:45–52CrossRefGoogle Scholar
  12. Becker A et al (2004) Global changes in gene expression in Sinorhizobium meliloti 1021 under microoxic and symbiotic conditions. Molec Plant-Microbe Interact 17:292–303CrossRefGoogle Scholar
  13. Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486CrossRefPubMedGoogle Scholar
  14. Berleman JE, Bauer CE (2005) Involvement of a Che-like signal transduction cascade in regulating cyst cell development in Rhodospirillum centenum. Mol Microbiol 56:1457–1466CrossRefPubMedGoogle Scholar
  15. 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 190:6365–6375CrossRefPubMedPubMedCentralGoogle Scholar
  16. 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 194:3343–3355CrossRefPubMedPubMedCentralGoogle Scholar
  17. Bowra BJ, Dilworth MJ (1981) Motility and chemotaxis towards sugars in Rhizobium leguminosarum. J Gen Microbiol 126:231–235Google Scholar
  18. Bringhurst RM, Gage DJ (2002) Control of inducer accumulation plays a key role in succinate-mediated catabolite repression in Sinorhizobium meliloti. J Bacteriol 184:5385–5392CrossRefPubMedPubMedCentralGoogle Scholar
  19. Buchan A, Crombie B, Alexandre GM (2010) Temporal dynamics and genetic diversity of chemotactic-competent microbial populations in the rhizosphere. Environ Microbiol 12:3171–3184CrossRefPubMedGoogle Scholar
  20. Burg D, Guillaume J, Tailliez R (1982) Chemotaxis by Rhizobium meliloti. Arch Microbiol 133:162–163CrossRefGoogle Scholar
  21. Caetano-Anollés G, Crist-Estes DK, Bauer WD (1988a) Chemotaxis of Rhizobium meliloti to the plant flavone luteolin requires functional nodulation genes. J Bacteriol 170:3164–3169PubMedPubMedCentralGoogle Scholar
  22. 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 86:1228–1235CrossRefPubMedPubMedCentralGoogle Scholar
  23. 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 98:1181–1189CrossRefPubMedPubMedCentralGoogle Scholar
  24. 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 19:363–372CrossRefGoogle Scholar
  25. Charoenpanich P, Meyer S, Becker A, McIntosh M (2013) Temporal expression program of quorum sensing-based transcription regulation in Sinorhizobium meliloti. J Bacteriol 195:3224–3236CrossRefPubMedPubMedCentralGoogle Scholar
  26. 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 72:313–327CrossRefPubMedGoogle Scholar
  27. Dharmatilake AJ, Bauer WD (1992) Chemotaxis of Rhizobium meliloti towards nodulation gene-inducing compounds from alfalfa roots. Appl Environ Microbiol 58:1153–1158PubMedPubMedCentralGoogle Scholar
  28. Dogra G et al (2012) Sinorhizobium meliloti CheA complexed with CheS exhibits enhanced binding to CheY1, resulting in accelerated CheY1 dephosphorylation. J Bacteriol 194:1075–1087CrossRefPubMedPubMedCentralGoogle Scholar
  29. Galibert F et al (2001) The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293:668–672CrossRefPubMedGoogle Scholar
  30. 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 189:3591–3602CrossRefPubMedPubMedCentralGoogle Scholar
  31. Götz R, Limmer N, Ober K, Schmitt R (1982) Motility and chemotaxis in two strains of Rhizobium with complex flagella. J General Microbiol 128:789–798Google Scholar
  32. Greer-Phillips SE, Stephens BB, Alexandre G (2004) An energy taxis transducer promotes root colonization by Azospirillum brasilense. J Bacteriol 186:6595–6604CrossRefPubMedPubMedCentralGoogle Scholar
  33. Gulash M, Ames P, Larosiliere RC, Bergman K (1984) Rhizobia are attracted to localized sites on legume roots. Appl Environ Microbiol 48:149–152PubMedPubMedCentralGoogle Scholar
  34. 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 208:61–67PubMedGoogle Scholar
  35. Hazelbauer GL (2012) Bacterial chemotaxis: the early years of molecular studies. Ann Rev Microbiol 66:285–303. doi: 10.1146/annurev-micro-092611-150120 CrossRefGoogle Scholar
  36. Hazelbauer GL, Lai WC (2010) Bacterial chemoreceptors: providing enhanced features to two-component signaling. Curr Opin Microbiol 13:124–132CrossRefPubMedPubMedCentralGoogle Scholar
  37. Hazelbauer GL, Falke JJ, Parkinson JS (2008) Bacterial chemoreceptors: high-performance signaling in networked arrays. Trends Biochem Sci 33:9–19CrossRefPubMedPubMedCentralGoogle Scholar
  38. Heinrich D, Hess D (1985) Chemotactic attraction of Azospirillum lipoferum by wheat roots and characterization of some attractants. Can J Microbiol 31:26–31CrossRefGoogle Scholar
  39. Hoang HH, Gurich N, González JE (2008) Regulation of motility by the ExpR/Sin quorum-sensing system in Sinorhizobium meliloti. J Bacteriol 190:861–871CrossRefPubMedPubMedCentralGoogle Scholar
  40. Janczarek M (2011) Environmental signals and regulatory pathways that influence exopolysaccharide production in rhizobia. Int J Molec Sci 12:7898–7933CrossRefGoogle Scholar
  41. Karunakaran R et al (2009) Transcriptomic analysis of Rhizobium leguminosarum biovar viciae in symbiosis with host plants Pisum sativum and Vicia cracca. J Bacteriol 191:4002–4014CrossRefPubMedPubMedCentralGoogle Scholar
  42. Kirby JR, Zusman DR (2003) Chemosensory regulation of developmental gene expression in Myxococcus xanthus. Proc Natl Acad Sci USA 100:2008–2013CrossRefPubMedPubMedCentralGoogle Scholar
  43. Kristich CJ, Ordal GW (2002) Bacillus subtilis CheD is a chemoreceptor modification enzyme required for chemotaxis. J Biol Chem 277:25356–25362CrossRefPubMedGoogle Scholar
  44. Lakshmanan V, Selvaraj G, Bais HP (2014) Functional soil microbiome: belowground solutions to an aboveground problem. Plant Physiol 166:689–700CrossRefPubMedPubMedCentralGoogle Scholar
  45. Mandal SM, Chakraborty D, Dey S (2010) Phenolic acids act as signaling molecules in plant–microbe symbioses. Plant Signal Behav 5:359–368CrossRefPubMedPubMedCentralGoogle Scholar
  46. Mandimba G, Heulin T, Bally R, Guckert A, Balandreau J (1986) Chemotaxis of free-living nitrogen-fixing bacteria towards maize mucilage. Plant Soil 90:129–139CrossRefGoogle Scholar
  47. McDougall BM, Rovira AD (1970) Sites of exudation of 14C-labelled compounds from wheat roots. New Phytol 69:999–1003CrossRefGoogle Scholar
  48. McIntosh M, Krol E, Becker A (2008) Competitive and cooperative effects in quorum-sensing-regulated galactoglucan biosynthesis in Sinorhizobium meliloti. J Bacteriol 190:5308–5317CrossRefPubMedPubMedCentralGoogle Scholar
  49. McIntosh M, Meyer S, Becker A (2009) Novel Sinorhizobium meliloti quorum sensing positive and negative regulatory feedback mechanisms respond to phosphate availability. Mol Microbiol 74:1238–1256CrossRefPubMedGoogle Scholar
  50. Meier VM, Scharf BE (2009) Cellular localization of predicted transmembrane and soluble chemoreceptors in Sinorhizobium meliloti. J Bacteriol 191:5724–5733CrossRefPubMedPubMedCentralGoogle Scholar
  51. Meier VM, Muschler P, Scharf BE (2007) Functional analysis of nine putative chemoreceptor proteins in Sinorhizobium meliloti. J Bacteriol 189:1816–1826CrossRefPubMedPubMedCentralGoogle Scholar
  52. 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 63:348–362CrossRefGoogle Scholar
  53. 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 177:5419–5426PubMedPubMedCentralGoogle Scholar
  54. 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 178:5017–5019PubMedPubMedCentralGoogle Scholar
  55. Morris J, González JE (2009) The novel genes emmABC are associated with exopolysaccharide production, motility, stress adaptation, and symbiosis in Sinorhizobium meliloti. J Bacteriol 191:5890–5900CrossRefPubMedPubMedCentralGoogle Scholar
  56. Mukherjee A, Ghosh S (1987) Regulation of fructose uptake and catabolism by succinate in Azospirillum brasilense. J Bacteriol 169:4361–4367PubMedPubMedCentralGoogle Scholar
  57. Neumann S, Grosse K, Sourjik V (2012) Chemotactic signaling via carbohydrate phosphotransferase systems in Escherichia coli. Proc Natl Acad Sci USA 109:12159–12164CrossRefPubMedPubMedCentralGoogle Scholar
  58. Parkinson JS, Hazelbauer GL, Falke JJ (2015) Signaling and sensory adaptation in Escherichia coli chemoreceptors: 2015 update. Trends Microbiol 23:257–266CrossRefPubMedGoogle Scholar
  59. 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 179:6391–6399PubMedPubMedCentralGoogle Scholar
  60. Poole PS, Blyth A, Reid CJ, Walters K (1994) myo-Inositol catabolism and catabolite regulation in Rhizobium leguminosarum bv. viciae. Microbiology 140:2787–2795CrossRefGoogle Scholar
  61. Reinhold B, Hurek T, Fendrik I (1985) Strain-specific chemotaxis of Azospirillum spp. J Bacteriol 162:190–195PubMedPubMedCentralGoogle Scholar
  62. Robinson JB, Bauer WD (1993) Relationships between C4 dicarboxylic acid transport and chemotaxis in Rhizobium meliloti. J Bacteriol 175:2284–2291PubMedPubMedCentralGoogle Scholar
  63. 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 34:3823–3831CrossRefPubMedGoogle Scholar
  64. 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 188:6932–6942CrossRefPubMedPubMedCentralGoogle Scholar
  65. Sadasivan L, Neyra CA (1985) Flocculation in Azospirillum brasilense and Azospirillum lipoferum: exopolysaccharides and cyst formation. J Bacteriol 163:716–723PubMedPubMedCentralGoogle Scholar
  66. Sampedro I, Parales RE, Krell T, Hill JE (2015) Pseudomonas chemotaxis. FEMS Microbiol Rev 39:17–46PubMedGoogle Scholar
  67. Scharf B (2002) Real-time imaging of fluorescent flagellar filaments of Rhizobium lupini H13-3: flagellar rotation and pH-induced polymorphic transitions. J Bacteriol 184:5979–5986CrossRefPubMedPubMedCentralGoogle Scholar
  68. 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 323:105–112CrossRefPubMedGoogle Scholar
  69. Sourjik V, Schmitt R (1996) Different roles of CheY1 and CheY2 in the chemotaxis of Rhizobium meliloti. Mol Microbiol 22:427–436CrossRefPubMedGoogle Scholar
  70. Sourjik V, Schmitt R (1998) Phosphotransfer between CheA, CheY1, and CheY2 in the chemotaxis signal transduction chain of Rhizobium meliloti. Biochemistry 37:2327–2335CrossRefPubMedGoogle Scholar
  71. 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 223:283–290CrossRefPubMedGoogle Scholar
  72. 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 182:782–788CrossRefPubMedPubMedCentralGoogle Scholar
  73. Steenhoudt O, Vanderleyden J (2000) Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol Rev 24:487–506CrossRefPubMedGoogle Scholar
  74. 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 156:1673–1685CrossRefPubMedGoogle Scholar
  75. Ulrich LE, Zhulin IB (2009) The MiST2 database: a comprehensive genomics resource on microbial signal transduction. Nucleic Acids Res 38:D401–407CrossRefPubMedPubMedCentralGoogle Scholar
  76. 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 19–20Google Scholar
  77. 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 32:703–714CrossRefGoogle Scholar
  78. Vande Broek A, Lambrecht M, Vanderleyden J (1998) Bacterial chemotactic motility is important for the initiation of wheat root colonization by Azospirillum brasilense. Microbiology 144:2599–2606CrossRefPubMedGoogle Scholar
  79. Wadhams GH, Armitage JP (2004) Making sense of it all: bacterial chemotaxis. Nature Rev Mol Cell Biol 5:1024–1037CrossRefGoogle Scholar
  80. Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51CrossRefPubMedPubMedCentralGoogle Scholar
  81. 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 80:3404–3415CrossRefPubMedPubMedCentralGoogle Scholar
  82. Wisniewski-Dyé F et al (2011) Azospirillum genomes reveal transition of bacteria from aquatic to terrestrial environments. PLoS Genet 7:e1002430CrossRefPubMedPubMedCentralGoogle Scholar
  83. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  84. 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 107:2235–2240CrossRefPubMedPubMedCentralGoogle Scholar
  85. Yao SY et al (2004) Sinorhizobium meliloti ExoR and ExoS proteins regulate both succinoglycan and flagellum production. J Bacteriol 186:6042–6049CrossRefPubMedPubMedCentralGoogle Scholar
  86. Yost CK, Rochepeau P, Hynes MF (1998) Rhizobium leguminosarum contains a group of genes that appear to code for methyl-accepting chemotaxis proteins. Microbiology 144:1945–1956CrossRefPubMedGoogle Scholar
  87. Yost CK, Clark KT, Del Bel KL, Hynes MF (2003) Characterization of the nodulation plasmid encoded chemoreceptor gene mcpG from Rhizobium leguminosarum. BMC Microbiol 3:1CrossRefPubMedPubMedCentralGoogle Scholar
  88. 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 182:505–513CrossRefPubMedGoogle Scholar
  89. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  90. 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 80:2429–2439CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Birgit E. Scharf
    • 1
  • Michael F. Hynes
    • 2
  • Gladys M. Alexandre
    • 3
    Email author
  1. 1.Department of Biological Sciences, Life Sciences IVirginia Polytechnic Institute and State UniversityBlacksburgUSA
  2. 2.Department of Biological SciencesUniversity of CalgaryCalgaryCanada
  3. 3.Department of Biochemistry, Cellular and Molecular BiologyUniversity of TennesseeKnoxvilleUSA

Personalised recommendations