Rhizobial galactoglucan determines the predatory pattern of Myxococcus xanthus and protects Sinorhizobium meliloti from predation

Environmental Microbiology

Volumn 16, Issue 7, 2014, Pages 2341-2350

  Pérez, Juana ^a   Jiménez Zurdo, José I ^b   Martínez Abarca, Francisco ^b   Millán, Vicenta ^b   Shimkets, Lawrence J ^c   Muñoz Dorado, José ^a  

^a UNIVERSITY OF GRANADA   (Spain)

^b CSIC   (Spain)

^c UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); EUKARYOTA; MYXOCOCCUS XANTHUS; PROKARYOTA; SINORHIZOBIUM MELILOTI;

BACTERIAL POLYSACCHARIDE; BACTERIAL PROTEIN; GALACTAN; GALACTOGLUCAN; GLUCAN; TRANSACTIVATOR PROTEIN;

ADAPTATION; ANTIBIOSIS; ARTICLE; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIAL VIABILITY; MOVEMENT (PHYSIOLOGY); MUTATION; MYXOCOCCUS XANTHUS; PATHOGENICITY; QUORUM SENSING; SINORHIZOBIUM MELILOTI;

ADAPTATION, BIOLOGICAL; ANTIBIOSIS; BACTERIAL PROTEINS; GALACTANS; GENE EXPRESSION REGULATION, BACTERIAL; GLUCANS; MICROBIAL VIABILITY; MOVEMENT; MUTATION; MYXOCOCCUS XANTHUS; POLYSACCHARIDES, BACTERIAL; QUORUM SENSING; SINORHIZOBIUM MELILOTI; TRANS-ACTIVATORS;

EID: 84903785070     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12477     Document Type: Article

References (53)

1. Barnet, Y.M. (1980) The effect of rhizobiophages on populations of Rhizobium trifolii in the root zone of clover plants. Can J Microbiol 26: 572-576.
2. Beringer, J.E. (1974) R factor transfer in Rhizobium leguminosarum. J Gen Microbiol 84: 188-198.
3. Berleman, J.E., and Kirby, J.R. (2009) Deciphering the hunting strategy of a bacterial wolfpack. FEMS Microbiol Rev 33: 942-957.
4. Berleman, J.E., Chuntley, T., Cheung, P., and Kirby, J.R. (2006) Rippling is a predatory behavior in Myxococcus xanthus. J Bacteriol 188: 5888-5895.
5. Berleman, J.E., Scott, J., Chuntley, T., and Kirby, J.R. (2008) Predataxis behavior in Myxococcus xanthus. Proc Natl Acad Sci USA 105: 17127-17132.
6. Bull, C.T., Shetty, K.G., and Subbarao, K.V. (2002) Interactions between myxobacteria, plant pathogenic fungi, and biocontrol agents. Plant Dis 86: 889-896.
7. Campos, J.M., and Zusman, D. (1975) Regulation of development in Myxococcus xanthus: effect of 3':5'-cyclic AMP, ADP and nutrition. Proc Natl Acad Sci USA 72: 518-522.
8. Casadesús, J., and Olivares, J. (1979) Rough and fine linkage mapping of the Rhizobium meliloti chromosome. Mol Gen Genet 174: 203-209.
9. Casse, F., Boucher, C., Julliot, J.S., Michel, M., and Dénarié, J. (1979) Identification and characterization of large plasmids in Rhizobium meliloti using agarose-gel electrophoresis. J Gen Microbiol 113: 229-242.
10. Chesson, P. (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst 31: 342-366.
11. Curtis, P.D., Taylor, R.G., Welch, R.D., and Shimkets, L.J. (2007) Spatial organization of Myxococcus xanthus during fruiting body formation. J Bacteriol 189: 9126-9130.
12. Dawid, W. (2000) Biology and global distribution of myxobacteria in soils. FEMS Microbiol Rev 24: 403-427.
13. Gao, M., Chen, H., Eberhard, A., Gronquist, M.R., Robinson, J.B., Rolfe, B.G., etal. (2005) sinI- and expR-dependent quorum sensing in Sinorhizobium meliloti. J Bacteriol 187: 7931-7944.
14. Glazebrook, J., and Walker, G.C. (1989) Genetic techniques in Rhizobium meliloti. Methods Enzymol 204: 398-418.
15. Goldman, B.S., Nierman, W.C., Kaiser, D., Slater, S.C., Durkin, A.S., Eisen, J.A., etal. (2006) Evolution of sensory complexity recorded in a myxobacterial genome. Proc Natl Acad Sci USA 103: 15200-15205.
16. González, J.E., Gregory, M.Y., and Walker, G.C. (1996a) Rhizobium meliloti exopolysaccharides: synthesis and symbiotic function. Gene 179: 141-146.
17. González, J.E., Reuhs, B.L., and Walker, G.C. (1996b) Low molecular weight EPSII of Rhizobium meliloti allows nodule invasion in Medicago sativa. Proc Natl Acad Sci USA 93: 8636-8641.
18. Gurich, N., and González, J.E. (2009) Role of quorum sensing in Sinorhizobium meliloti-alfalfa symbiosis. J Bacteriol 191: 4372-4382.
19. Hartzell, P., and Kaiser, D. (1991) Upstream gene of the mgl operon controls the level of MglA protein in Myxococcus xanthus. J Bacteriol 173: 7625-7635.
20. Hashem, F.M., and Angle, J.S. (1988) Rhizobiophage effects on Bradyrhizobium japonicum nodulation and soybean growth. Soil Biol Biochem 20: 69-73.
21. Hoang, H.H., Becker, A., and González, J.E. (2004) The LuxR homolog ExpR, in combination with the Sin quorum sensing system, plays a central role in Sinorhizobium meliloti gene expression. J Bacteriol 186: 5460-5472.
22. Hoang, H.H., Gurich, N., and González, J.E. (2008) Regulation of motility by the ExpR/Sin quorum sensing system in Sinorhizobium meliloti. J Bacteriol 190: 861-871.
23. Hodgkin, J., and Kaiser, D. (1977) Cell-to-cell stimulation of movement in nonmotile mutants of Myxococcus. Proc Natl Acad Sci USA 74: 2938-2942.
24. Hodgkin, J., and Kaiser, D. (1979) Genetics of gliding motility in Myxococcus xanthus (Myxobacterales): two gene systems control movement. Mol Gen Genet 171: 177-191.
25. Jones, K.M., Kobayashi, H., Davies, B.W., Taga, M.E., and Walker, G.C. (2007) How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nat Rev Microbiol 5: 619-633.
26. Kaiser, D. (1979) Social gliding is correlated with the presence of pili in Myxococcus xanthus. Proc Natl Acad Sci USA 76: 5952-5956.
27. 2-dependent damage. J Bacteriol 195: 5362-5369.
28. Li, S., Lee, B.U., and Shimkets, L.J. (1992) csgA expression entrains Myxococcus xanthus development. Genes Dev 6: 401-410.
29. Lindström, K., Murwira, M., Willems, A., and Altier, N. (2010) The biodiversity of beneficial microbe-host mutualism: the case of rhizobia. Res Microbiol 161: 453-463.
30. Marketon, M.M., Gronquist, M.R., Eberhard, A., and González, J.E. (2002) Characterization of the Sinorhizobium meliloti sinR/sinI locus and the production of novel N-acyl homoserine lactones. J Bacteriol 184: 5686-5695.
31. Marketon, M.M., Glenn, S.A., Eberhard, A., and González, J.E. (2003) Quorum sensing controls exopolysaccharide production in Sinorhizobium meliloti. J Bacteriol 185: 325-331.
32. May, T.B., and Chakrabarty, A.M. (1994) Isolation and assay of Pseudomonas aeruginosa alginate. Methods Enzymol 235: 295-304.
33. Meade, H.M., and Signer, E.R. (1977) Genetic mapping of Rhizobium meliloti. Proc Natl Acad Sci USA 74: 2076-2078.
34. Mendes-Soares, H., and Velicer, G.J. (2013) Decomposing predation: testing for parameters that correlate with predatory performance by a social bacterium. Microb Ecol 65: 415-423.
35. Morgan, A.D., MacLean, R.C., Hiilesland, K.L., and Velicer, G.J. (2010) Comparative analysis of Myxococcus predation on soil bacteria. Appl Environ Microbiol 76: 6920-6927.
36. Newton, W.E. (2000) Nitrogen fixation in perspective. In Nitrogen Fixation: From Molecules to Crop Productivity. Pedrosa, F.O., Hungría, M., Yates, M.G., and Newton, W.E. (eds). Dordrecht, The Netherlands: Kluwer, pp. 3-8.
37. Nogales, J., Bernabéu-Roda, L., Cuéllar, V., and Soto, M.J. (2012) ExpR is not required for swarming but promotes sliding in Sinorhizobium meliloti. J Bacteriol 194: 2027-2035.
38. Pellock, B.J., Teplitski, M., Boinay, R.P., Bauer, W.D., and Walker, G.C. (2002) A LuxR homolog controls production of symbiotically active extracellular polysaccharide II by Sinorhizobium meliloti. J Bacteriol 184: 5067-5076.
39. Pérez, J., Muñoz-Dorado, J., Braña, A.F., Shimkets, L.J., Sevillano, L., and Santamaría, R.I. (2011) Myxococcus xanthus induces actinorhodin overproduction and aerial mycelium formation by Streptomyces coelicolor growth and development. Microb Biotechnol 4: 175-183.
40. Pham, V.D., Shebelut, C.W., Diodati, M.E., Bull, C.T., and Singer, M. (2005) Mutations affecting predation ability of the soil bacterium Myxococcus xanthus. Microbiology 151: 1865-1874.
41. Rangin, C., Brunel, B., Cleyet-Marel, J.C., Perrineau, M.M., and Béna, G. (2008) Effects of Medicago truncatula genetic diversity, rhizobial competition, and strain effectiveness on the diversity of a natural Sinorhizobium species community. Appl Environ Microbiol 74: 5653-5661.
42. Robertsen, B.K., Aiman, P., Darvill, A.G., McNeil, M., and Alberstein, P. (1981) The structure of acidic extracellular polysaccharides secreted by Rhizobium leguminosarum and Rhizobium trifolii. Plant Physiol 67: 389-400.
43. Robleto, E.A., Kmiecik, K., Oplinger, E.S., Nienhuis, J., and Triplett, E.W. (1998) Trifolitoxin production increases nodulation competitiveness of Rhizobium etli CE3 under agricultural conditions. Appl Environ Microbiol 64: 2630-2633.
44. Shimkets, L.J., and Kaiser, D. (1982) Induction of coordinated movement of Myxococcus xanthus cells. J Bacteriol 152: 451-461.
45. Toro, N. (1996) Nodulation competitiveness in the Rhizobium-legume symbiosis. World J Microbiol Biotechnol 12: 157-162.
46. Triplett, E.W., and Sadowsky, M.J. (1992) Genetics of competition for nodulation of legumes. Annu Rev Microbiol 46: 399-428.
47. Villadas, P.J., Velázquez, E., Martínez-Molina, E., and Toro, N. (1995) Identification of nodule-dominant Rhizobium meliloti strains carrying pRmeGR4b-type plasmid within indigenous soil populations by PCR using primers derived from specific DNA sequences. FEMS Microbiol Ecol 17: 161-168.
48. Volz, C., Kegler, C., and Müller, R. (2012) Enhancer binding proteins act as hetero-oligomers and link secondary metabolite production to myxococcal development, motility, and predation. Chem Biol 21: 1447-1454.
49. White, D.J., and Hartzell, P.L. (2000) AglU, a protein required for gliding motility and spore maturation of Myxococcus xanthus, is related to WD-repeat proteins. Mol Microbiol 36: 662-678.
50. Wu, S.S., and Kaiser, D. (1996) Markerless deletion of pil genes in Myxococcus xanthus generated by counterselection with the Bacillus subtilis sacB gene. J Bacteriol 178: 5817-5821.
51. Xiao, Y., Wei, X., Ebright, R., and Wall, D. (2011) Antibiotic production by myxobacteria plays a role in predation. J Bacteriol 193: 4626-4633.
52. Zahran, H.H. (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63: 968-989.
53. Zhang, H., Vaksman, Z., Litwin, D.B., Shi, P., Kaplan, H.B., and Igoshin, O.A. (2012) The mechanistic basis of Myxococcus xanthus rippling behavior and its physiological role during predation. PLoS Comput Biol 8: e1002715.