Azospirillum brasilense chemotaxis depends on two signaling pathways regulating distinct motility parameters

Journal of Bacteriology

Volumn 198, Issue 12, 2016, Pages 1764-1772

  Mukherjee, Tanmoy ^a   Kumar, Dhivya ^a,c   Burriss, Nathan ^a   Xie, Zhihong ^a,b   Alexandre, Gladys ^a  

^a UNIVERSITY OF TENNESSEE   (United States)

^b YANTAI INSTITUTE OF COASTAL ZONE RESEARCH   (China)

^c UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; AZOSPIRILLUM BRASILENSE; BACTERIAL CELL; BACTERIAL COLONIZATION; BACTERIAL GENE; CELL MOTILITY; CHE1 GENE; CHE4 GENE; CHEMOTAXIS; CONTROLLED STUDY; MICROBIAL COMMUNITY; NONHUMAN; PLANT ROOT; PRIORITY JOURNAL; RHIZOSPHERE; TRITICUM AESTIVUM; CYTOLOGY; GENETICS; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; WHEAT;

BACTERIAL PROTEIN;

AZOSPIRILLUM BRASILENSE; BACTERIAL PROTEINS; CHEMOTAXIS; PLANT ROOTS; SIGNAL TRANSDUCTION; TRITICUM;

EID: 84971576405     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00020-16     Document Type: Article

References (45)

1. Wadhams GH, Armitage JP. 2004. Making sense of it all: bacterial chemotaxis. Nat Rev Mol Cell Biol 5:1024-1037. http://dx.doi.org/10.1038 /nrm1524.
2. 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. http://dx.doi.org/10.1111 /j.1462-2920.2010.02290.x.
3. Wuichet K, Zhulin IB. 2010. Origins and diversification of a complex signal transduction system in prokaryotes. Sci Signal 3:ra50. http://dx.doi.org/10.1126/scisignal.2000724.
4. Porter SL, Wadhams GH, Armitage JP. 2008. Rhodobacter sphaeroides: complexity in chemotactic signalling. Trends Microbiol 16:251-260. http: //dx.doi.org/10.1016/j.tim.2008.02.006.
5. Zhulin IB, Armitage JP. 1993. Motility, chemokinesis, and methylationindependent chemotaxis in Azospirillum brasilense. J Bacteriol 175:952-958.
6. 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. http://dx.doi.org /10.1128/JB.00310-12.
7. Cecagno R, Fritsch TE, Schrank IS. 2015. The plant growth-promoting bacteria Azospirillum amazonense: genomic versatility and phytohormone pathway. Biomed Res 2015:7. http://dx.doi.org/10.1155/2015/898592.
8. Wisniewski-Dyé F, Lozano L, Acosta-Cruz E, Borland S, Drogue B, Prigent-Combaret C, Rouy Z, Barbe V, Herrera AM, González V, Mavingui P. 2012. Genome sequence of Azospirillum brasilense CBG497 and comparative analyses of Azospirillum core and accessory genomes provide insight into niche adaptation. Genes 3:576. http://dx.doi.org/10.3390/genes3040576.
9. Rivera D, Revale S, Molina R, Gualpa J, Puente M, Maroniche G, Paris G, Baker D, Clavijo B, McLay K, Spaepen S, Perticari A, Vazquez M, Wisniewski-Dyé F, Watkins C, Martínez-Abarca F, Vanderleyden J, Cassán F. 2014. Complete genome sequence of the model rhizosphere strain Azospirillum brasilense Az39, successfully applied in agriculture. Genome Announc 2(4):e00683-14. http://dx.doi.org/10.1128/genomeA.00683-14.
10. Wisniewski-Dyé F, Borziak K, Khalsa-Moyers G, Alexandre G, Sukharnikov LO, Wuichet K, Hurst GB, McDonald WH, Robertson JS, Barbe V, Calteau A, Rouy Z, Mangenot S, Prigent-Combaret C, Normand P, Boyer M, Siguier P, Dessaux Y, Elmerich C, Condemine G, Krishnen G, Kennedy I, Paterson AH, González V, Mavingui P, Zhulin IB. 2011. Azospirillum genomes reveal transition of bacteria from aquatic to terrestrial environments. PLoS Genet 7:e1002430. http://dx.doi.org/10.1371/journal.pgen.1002430.
11. Stephens BB, Loar SN, Alexandre G. 2006. Role of CheB and CheR in the complex chemotactic and aerotactic pathway of Azospirillum brasilense. J Bacteriol 188:4759-4768. http://dx.doi.org/10.1128/JB.00267-06.
12. Bible AN, Khalsa-Moyers GK, Mukherjee T, Green CS, Mishra P, Purcell A, Aksenova A, Hurst GB, Alexandre G. 2015. Metabolic adaptations of Azospirillum brasilense to oxygen stress by cell-cell clumping and flocculation. Appl Environ Microbiol 81:8346-8357. http://dx.doi.org/10.1128/AEM.02782-15.
13. Jiang ZY, Gest H, Bauer CE. 1997. Chemosensory and photosensory perception in purple photosynthetic bacteria utilize common signal transduction components. J Bacteriol 179:5720-5727.
14. 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. http://dx.doi.org/10.1111/j.1574-6968.2002.tb11061.x.
15. Vanstockem M, Michiels K, Vanderleyden J, Van Gool AP. 1987. Transposon mutagenesis of Azospirillum brasilense and Azospirillum lipoferum: physical analysis of Tn5 and Tn5-Mob insertion mutants. Appl Environ Microbiol 53:410-415.
16. Higuchi R, Krummel B, Saiki RK. 1988. A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucleic Acids Res 16:7351-7367. http://dx.doi.org /10.1093/nar/16.15.7351.
17. Krause A, Doerfel A, Gottfert M. 2002. Mutational and transcriptional analysis of the type III secretion system of Bradyrhizobium japonicum. Mol Plant Microbe Interact 15:1228-1235. http://dx.doi.org/10.1094/MPMI.2002.15.12.1228.
18. Alexandre G, Greer SE, Zhulin IB. 2000. Energy taxis is the dominant behavior in Azospirillum brasilense. J Bacteriol 182:6042-6048. http://dx.doi.org/10.1128/JB.182.21.6042-6048.2000.
19. 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. http: //dx.doi.org/10.1111/j.1574-6968.2011.02366.x.
20. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol 215:403-410. http://dx.doi.org/10.1016 /S0022-2836(05)80360-2.
21. Mohari B, Licata NA, Kysela DT, Merritt PM, Mukhopadhay S, Brun YV, Setayeshgar S, Fuqua C. 2015. Novel pseudotaxis mechanisms improve migration of straight-swimming bacterial mutants through a porous environment. mBio 6:e00005. http://dx.doi.org/10.1128/mBio.00005-15.
22. Wolfe AJ, Berg HC. 1989. Migration of bacteria in semisolid agar. Proc Natl Acad Sci U S A 86:6973-6977. http://dx.doi.org/10.1073/pnas.86.18.6973.
23. Miller LD, Yost CK, Hynes MF, Alexandre G. 2007. The major chemotaxis gene cluster of Rhizobium leguminosarum bv. viciae is essential for competitive nodulation. Mol Microbiol 63:348-362. http://dx.doi.org/10.1111/j.1365-2958.2006.05515.x.
24. 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. http://dx.doi.org /10.1128/JB.00734-08.
25. Lauga E, DiLuzio WR, Whitesides GM, Stone HA. 2006. Swimming in circles: motion of bacteria near solid boundaries. Biophys J 90:400-412. http://dx.doi.org/10.1529/biophysj.105.069401.
26. Lemelle L, Palierne J-F, Chatre E, Place C. 2010. Counterclockwise circular motion of bacteria swimming at the air-liquid interface. J Bacteriol 192:6307-6308. http://dx.doi.org/10.1128/JB.00397-10.
27. Armitage JP, Schmitt R. 1997. Bacterial chemotaxis: Rhodobacter sphaeroides and Sinorhizobium meliloti-variations on a theme? Microbiology 143:3671-3682. http://dx.doi.org/10.1099/00221287-143-12-3671.
28. Greck M, Platzer J, Sourjik V, Schmitt R. 1995. Analysis of a chemotaxis operon in Rhizobium meliloti. Mol Microbiol 15:989-1000. http://dx.doi.org/10.1111/j.1365-2958.1995.tb02274.x.
29. Koonin EV, Makarova KS, Aravind L. 2001. Horizontal gene transfer in prokaryotes: quantification and classification. Annu Rev Microbiol 55: 709-742. http://dx.doi.org/10.1146/annurev.micro.55.1.709.
30. Porter SL, Wadhams GH, Armitage JP. 2011. Signal processing in complex chemotaxis pathways. Nat Rev Microbiol 9:153-165. http://dx.doi.org/10.1038/nrmicro2505.
31. Porter SL, Warren AV, Martin AC, Armitage JP. 2002. The third chemotaxis locus of Rhodobacter sphaeroides is essential for chemotaxis. Mol Microbiol 46:1081-1094. http://dx.doi.org/10.1046/j.1365-2958.2002.03218.x.
32. Shah DSH, Porter SL, Martin AC, Hamblin PA, Armitage JP. 2000. Fine tuning bacterial chemotaxis: analysis of Rhodobacter sphaeroides behaviour under aerobic and anaerobic conditions by mutation of the major chemotaxis operons and cheY genes. EMBO J 19:4601-4613. http://dx.doi.org/10.1093/emboj/19.17.4601.
33. Pilizota T, Brown MT, Leake MC, Branch RW, Berry RM, Armitage JP. 2009. A molecular brake, not a clutch, stops the Rhodobacter sphaeroides flagellar motor. Proc Natl Acad Sci U S A 106:11582-11587. http://dx.doi.org/10.1073/pnas.0813164106.
34. Porter SL, Wadhams GH, Martin AC, Byles ED, Lancaster DE, Armitage JP. 2006. The CheYs of Rhodobacter sphaeroides. J Biol Chem 281: 32694-32704. http://dx.doi.org/10.1074/jbc.M606016200.
35. Russell MH, Bible AN, Fang X, Gooding JR, Campagna SR, Gomelsky M, Alexandre G. 2013. Integration of the second messenger c-di-GMP into the chemotactic signaling pathway. mBio 4:e00001-13. http://dx.doi.org/10.1128/mBio.00001-13.
36. Stocker R, Seymour JR. 2012. Ecology and physics of bacterial chemotaxis in the ocean. Microbiol Mol Biol Rev 76:792-812. http://dx.doi.org/10.1128/MMBR.00029-12.
37. Carvalhais LC, Dennis PG, Fan B, Fedoseyenko D, Kierul K, Becker A, von Wiren N, Borriss R. 2013. Linking plant nutritional status to plantmicrobe interactions. PLoS One 8:e68555. http://dx.doi.org/10.1371 /journal.pone.0068555.
38. Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH. 2013. Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789-799. http://dx.doi.org/10.1038/nrmicro3109.
39. Hinsinger P, Bengough AG, Vetterlein D, Young I. 2009. Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant Soil 321:117-152. http://dx.doi.org/10.1007/s11104-008-9885-9.
40. Flessa H. 1994. Plant-induced changes in the redox potential of the rhizospheres of the submerged vascular macrophytes Myriophyllum verticillatum L. and Ranunculus circinatus L. Aquat Bot 47:119-129. http://dx.doi.org/10.1016/0304-3770(94)90009-4.
41. Greer-Phillips SE, Stephens BB, Alexandre G. 2004. An energy taxis transducer promotes root colonization by Azospirillum brasilense. J Bacteriol 186:6595- 6604. http://dx.doi.org/10.1128/JB.186.19.6595-6604.2004.
42. Simon R, Priefer U, Puhler A. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Nat Biotechnol 1:784-791. http://dx.doi.org/10.1038 /nbt1183-784.
43. Keen NT, Tamaki S, Kobayashi D, Trollinger D. 1988. Improved broadhost- range plasmids for DNA cloning in Gram-negative bacteria. Gene 70:191-197. http://dx.doi.org/10.1016/0378-1119(88)90117-5.
44. Dennis JJ, Zylstra GJ. 1998. Plasposons: modular self-cloning minitransposon derivatives for rapid genetic analysis of gram-negative bacterial genomes. Appl Environ Microbiol 64:2710-2715.
45. Töpfer R, Schell J, Steinbiss HH. 1988. Versatile cloning vectors for transient gene expression and direct gene transfer in plant cells. Nucleic Acids Res 16:8725. http://dx.doi.org/10.1093/nar/16.17.8725.