1887

Abstract

genetic mutants with characterized phenotypes were analysed for the ability to prey on susceptible bacteria. Quantification of predatory ability was scored by a newly developed method under conditions in which prey bacteria provided the only source of nutrients. These results were corroborated by data derived using a previously published protocol that measures predation in the presence of limited external nutrients. First, early developmental regulatory mutants were examined, because their likely functions in assessing the local nutrient status were predicted to be also important for predation. The results showed that predation efficiency is reduced by 64–80 % for mutants of three A-signalling components, AsgA, AsgC and AsgE, but not for AsgB. This suggests that an Asg regulon function that is separate from A-signal production is needed for predation. Besides the Asg components, mutations in the early developmental genes and were also consistently observed to reduce predatory efficacy by 36 and 33 %, respectively. In contrast, later developmental components, such as DevRS, 4406 and PhoP4, did not appear to play significant roles in predation. The predatory abilities of mutants defective for motility were also tested. The data showed that adventurous, but not social, motility is required for predation in the assay. Also, mutants for components in the chemotaxis-like Frz system were found to be reduced in predation efficiency by between 62 and 85 %. In sum, it was demonstrated here that defects in development and development-related processes affect the ability of to prey on other bacteria.

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2005-06-01
2024-03-29
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References

  1. Alexander M. 1981; Why microbial parasites and predators do not eliminate their prey and hosts. Annu Rev Microbiol 35:113–133 [CrossRef]
    [Google Scholar]
  2. Blackhart B. D., Zusman D. R. 1985; “Frizzy” genes of Myxococcus xanthus are involved in control of frequency of reversal of gliding motility. Proc Natl Acad Sci U S A 82:8767–8770 [CrossRef]
    [Google Scholar]
  3. Blackhart B. D., Zusman D. R. 1986; Analysis of the products of the Myxococcus xanthus frz genes. J Bacteriol 166:673–678
    [Google Scholar]
  4. Bull C. T., Ishimaru C. A., Loper J. E. 1994; Two genomic regions involved in catechol siderophore production by Erwinia carotovora . Appl Environ Microbiol 60:662–669
    [Google Scholar]
  5. Bull C. T., Shetty K. G., Subbarao K. V. 2002; Interactions between myxobacteria, plant pathogenic fungi, and biocontrol agents. Plant Dis 86:889–896 [CrossRef]
    [Google Scholar]
  6. Bustamante V. H., Martinez-Flores I., Vlamakis H. C., Zusman D. R. 2004; Analysis of the Frz signal transduction system of Myxococcus xanthus shows the importance of the conserved C-terminal region of the cytoplasmic chemoreceptor FrzCD in sensing signals. Mol Microbiol 53:1501–1513 [CrossRef]
    [Google Scholar]
  7. Bycroft B. W., Maslen C., Box S. J., Brown A., Tyler J. W. 1987; The isolation and characterization of (3R,5R)- and (3S,5R)-carbapenem-3-carboxylic acid from Serratia and Erwinia species and their putative biosynthetic role. Chem Soc Chem Commun 21:1623–1625
    [Google Scholar]
  8. Campos J. M., Zusman D. R. 1975; Regulation of development in Myxococcus xanthus: effect of 3′: 5′-cyclic AMP, ADP, and nutrition. Proc Natl Acad Sci U S A 72:518–522 [CrossRef]
    [Google Scholar]
  9. Casida L. E. J. 1980; Bacterial predators of Micrococcus luteus in soil. Appl Environ Microbiol 39:1035–1041
    [Google Scholar]
  10. Casida L. E. J. 1988; Minireview: nonobligate bacterial predation of bacteria in soil. Microb Ecol 15:1–8 [CrossRef]
    [Google Scholar]
  11. Cintas N. A., Koike S. T., Bull C. T. 2002; A new pathovar, Pseudomonas syringae pv.alisalensis pv. nov., proposed for the causal agent of bacterial blight of broccoli and broccoli raab. Plant Dis 86:992–998 [CrossRef]
    [Google Scholar]
  12. Daft M. J., Stewart W. D. P. 1973; Light and electron microscope observations on algal lysis by bacterium CP-1. New Phytol 72:799–808 [CrossRef]
    [Google Scholar]
  13. Davis J. M., Mayor J., Plamann L. 1995; A missense mutation in rpoD results in an A-signalling defect in Myxococcus xanthus. Mol Microbiol 18:943–952 [CrossRef]
    [Google Scholar]
  14. Dawid W. 2000; Biology and global distribution of myxobacteria in soils. FEMS Microbiol Rev 24:403–427 [CrossRef]
    [Google Scholar]
  15. Dworkin M. 1983; Tactic behavior of Myxococcus xanthus. J Bacteriol 154:452–459
    [Google Scholar]
  16. Dworkin M. 1996; Recent advances in the social and developmental biology of the myxobacteria. Microbiol Rev 60:70–102
    [Google Scholar]
  17. Dworkin M., Eide D. 1983; Myxococcus xanthus does not respond chemotactically to moderate concentration gradients. J Bacteriol 154:437–442
    [Google Scholar]
  18. Garza A. G., Pollack J. S., Harris B. Z., Lee A., Keseler I. M., Licking E. F., Singer M. 1998; SdeK is required for early fruiting body development in Myxococcus xanthus . J Bacteriol 180:4628–4637
    [Google Scholar]
  19. Garza A. G., Harris B. Z., Pollack J. S., Singer M. 2000; The asgE locus is required for cell-cell signalling duringMyxococcus xanthus development. Mol Microbiol 35:812–824 [CrossRef]
    [Google Scholar]
  20. Goldman P. H., Koike S. T., Ryder E., Bull C. T. 2003; Influence of bacterial populations on leaf spot development in resistant and susceptible lettuce cultivars. Presentation at the American Phytopathological Society Annual Meeting August 2003 Charlotte, NC: http://www.apsnet.org/meetings/2003/abstracts/a03ma214.htm
    [Google Scholar]
  21. Hagen T. J., Shimkets L. J. 1990; Nucleotide sequence and transcriptional products of the csg locus of Myxococcus xanthus . J Bacteriol 172:15–23
    [Google Scholar]
  22. Hagen D. C., Bretscher A. P., Kaiser D. 1978; Synergism between morphogenetic mutants of Myxococcus xanthus. Dev Biol 64:284–296 [CrossRef]
    [Google Scholar]
  23. Hahn M. W, Höfle M. G. 2001; Grazing of protozoa and its effect on populations of aquatic bacteria. FEMS Microbiol Ecol 35:113–121 [CrossRef]
    [Google Scholar]
  24. Hanahan D. 1983; Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557–580 [CrossRef]
    [Google Scholar]
  25. Hejazi A., Falkiner F. R. 1997; Serratia marcescens. J Med Microbiol 46:903–912 [CrossRef]
    [Google Scholar]
  26. Hernandez V. J., Cashel M. 1995; Changes in conserved region 3 of Escherichia coli sigma 70 mediate ppGpp-dependent functions in vivo . J Mol Biol 252:536–549 [CrossRef]
    [Google Scholar]
  27. Hodgkin J., Kaiser D. 1977; Cell-to-cell stimulation of movement in nonmotile mutants of Myxococcus. Proc Natl Acad Sci U S A 74:2938–2942 [CrossRef]
    [Google Scholar]
  28. Hodgkin J., Kaiser D. 1979a; Genetics of gliding motility in Myxococcus xanthus (Myxobacterales): two gene systems control movement. Mol Gen Genet 171:177–191 [CrossRef]
    [Google Scholar]
  29. Hodgkin J., Kaiser D. 1979b; Genetics of gliding motility in Myxococcus xanthus (Myxobacterales): genes controlling movement of single cells. Mol Gen Genet 171:167–176 [CrossRef]
    [Google Scholar]
  30. Kaiser D. 1979; Social gliding is correlated with the presence of pili in Myxococcus xanthus. Proc Natl Acad Sci U S A 76:5952–5956 [CrossRef]
    [Google Scholar]
  31. Kaiser D. 2003; Coupling cell movement to multicellular development in myxobacteria. Nat Rev Microbiol 1:45–54 [CrossRef]
    [Google Scholar]
  32. Kearns D. B., Shimkets L. J. 1998; Chemotaxis in a gliding bacterium. Proc Natl Acad Sci U S A 95:11957–11962 [CrossRef]
    [Google Scholar]
  33. Kearns D. B., Venot A., Bonner P. J., Stevens B., Boons G. J., Shimkets L. J. 2001; Identification of a developmental chemoattractant in Myxococcus xanthus through metabolic engineering. Proc Natl Acad Sci U S A 98:13990–13994 [CrossRef]
    [Google Scholar]
  34. Kim S. K., Kaiser D. 1990; C-factor: a cell-cell signaling protein required for fruiting body morphogenesis of M. xanthus . Cell 61:19–26 [CrossRef]
    [Google Scholar]
  35. Kroos L., Kaiser D. 1987; Expression of many developmentally regulated genes in Myxococcus depends on a sequence of cell interactions. Genes Dev 1:840–854 [CrossRef]
    [Google Scholar]
  36. Kroos L., Kuspa A., Kaiser D. 1986; A global analysis of developmentally regulated genes in Myxococcus xanthus. Dev Biol 117:252–266 [CrossRef]
    [Google Scholar]
  37. Kroos L., Kuspa A., Kaiser D. 1990; Defects in fruiting body development caused by Tn5 lac insertions in Myxococcus xanthus. J Bacteriol 172:484–487
    [Google Scholar]
  38. Kühlwein H., Reichenbach H. 1968; Schwarmentwicklung und Morphogenese bei Myxobakterien/Archangium–Myxococcus–Chondrococcus–Chondromyces. In Film C893/1965 Göttingen, Germany: Institut für den Wissenschaftlichen Film (IWF;
    [Google Scholar]
  39. Kuspa A., Kaiser D. 1989; Genes required for developmental signalling in Myxococcus xanthus: three asg loci. J Bacteriol 171:2762–2772
    [Google Scholar]
  40. Kuspa A., Plamann L., Kaiser D. 1992; A-signalling and the cell density requirement for Myxococcus xanthus development. J Bacteriol 174:7360–7369
    [Google Scholar]
  41. Liu K.-C., Casida L. E. J. 1983; Survival of myxobacter strain 8 in natural soil in the presence and absence of host cells. Soil Biol Biochem 15:551–555 [CrossRef]
    [Google Scholar]
  42. MacNeil S. D., Calara F., Hartzell P. L. 1994a; New clusters of genes required for gliding motility in Myxococcus xanthus. Mol Microbiol 14:61–71 [CrossRef]
    [Google Scholar]
  43. MacNeil S. D., Mouzeyan A., Hartzell P. L. 1994b; Genes required for both gliding motility and development in Myxococcus xanthus. Mol Microbiol 14:785–795 [CrossRef]
    [Google Scholar]
  44. Martin M. O. 2002; Predatory prokaryotes: an emerging research opportunity. J Mol Microbiol Biotechnol 4:467–477
    [Google Scholar]
  45. McBride M. J., Weinberg R. A., Zusman D. R. 1989; “Frizzy” aggregation genes of the gliding bacterium Myxococcus xanthus show sequence similarities to the chemotaxis genes of enteric bacteria. Proc Natl Acad Sci U S A 86:424–428 [CrossRef]
    [Google Scholar]
  46. McCleary W. R., Zusman D. R. 1990; FrzE of Myxococcus xanthus is homologous to both CheA and CheY of Salmonella typhimurium. Proc Natl Acad Sci U S A 87:5898–5902 [CrossRef]
    [Google Scholar]
  47. Pepper A. F., Martin K. J., Bull C. T. 2004; Primers specific for detection of Myxococcus spp. by polymerase chain reaction. Phytopathology 94:S83
    [Google Scholar]
  48. Pinoy P. E. 1921; Sur les Myxobactéries. Ann Inst Pasteur 35:487
    [Google Scholar]
  49. Plamann L., Kuspa A., Kaiser D. 1992; Proteins that rescue A-signal-defective mutants of Myxococcus xanthus. J Bacteriol 174:3311–3318
    [Google Scholar]
  50. Plamann L., Li Y., Cantwell B., Mayor J. 1995; The Myxococcus xanthus asgA gene encodes a novel signal transduction protein required for multicellular development. J Bacteriol 177:2014–2020
    [Google Scholar]
  51. Pollack J. S., Singer M. 2001; SdeK, a histidine kinase required for Myxococcus xanthus development. J Bacteriol 183:3589–3596 [CrossRef]
    [Google Scholar]
  52. Raverdy J. 1973; Sur l'isolement et l'activité bacteriolytique de quelques Myxobactéries isoleés de l'eau. Water Res 7:687–693 [CrossRef]
    [Google Scholar]
  53. Rodriguez A. M., Spormann A. M. 1999; Genetic and molecular analysis of cglB, a gene essential for single-cell gliding in Myxococcus xanthus . J Bacteriol 181:4381–4390
    [Google Scholar]
  54. Rosenberg E., Varon M. 1984; Antibiotics and lytic enzymes. In Myxobacteria: Development and Cell Interactions pp 109–125 Edited by Rosenberg E. New York: Springer;
    [Google Scholar]
  55. Shi W., Zusman D. R. 1993; The two motility systems of Myxococcus xanthus show different selective advantages on various surfaces. Proc Natl Acad Sci U S A 90:3378–3382 [CrossRef]
    [Google Scholar]
  56. Shi W., Zusman D. R. 1994; Sensory adaptation during negative chemotaxis in Myxococcus xanthus. J Bacteriol 176:1517–1520
    [Google Scholar]
  57. Shi W., Kohler T., Zusman D. R. 1993; Chemotaxis plays a role in the social behaviour of Myxococcus xanthus. Mol Microbiol 9:601–611 [CrossRef]
    [Google Scholar]
  58. Shi W., Ngok F. K., Zusman D. R. 1996; Cell density regulates cellular reversal frequency in Myxococcus xanthus. Proc Natl Acad Sci U S A 93:4142–4146 [CrossRef]
    [Google Scholar]
  59. Shimkets L. J. 1986; Correlation of energy-dependent cell cohesion with social motility in Myxococcus xanthus. J Bacteriol 166:837–841
    [Google Scholar]
  60. Shimkets L. J., Rafiee H. 1990; CsgA, an extracellular protein essential for Myxococcus xanthus development. J Bacteriol 172:5299–5306
    [Google Scholar]
  61. Singh B. N., Yadava J. N. S. 1976; Fructification & antagonistic effect of myxobacteria on eubacteria: lytic effect & fruiting body formation of Myxococcus, Chondrococcus & Angiococcus spp. Indian J Exp Biol 14:68–70
    [Google Scholar]
  62. Søgaard-Andersen L., Overgaard M., Lobedanz S., Ellehauge E., Jelsbak L., Rasmussen A. A. 2003; Coupling gene expression and multicellular morphogenesis during fruiting body formation in Myxococcus xanthus. Mol Microbiol 48:1–8 [CrossRef]
    [Google Scholar]
  63. Spormann A. M. 1999; Gliding motility in bacteria: insights from studies of Myxococcus xanthus. Microbiol Mol Biol Rev 63:621–641
    [Google Scholar]
  64. Spormann A. M., Kaiser D. 1999; Gliding mutants of Myxococcus xanthus with high reversal frequencies and small displacements. J Bacteriol 181:2593–2601
    [Google Scholar]
  65. Thöny-Meyer L., Kaiser D. 1993; devRS, an autoregulated and essential genetic locus for fruiting body development in Myxococcus xanthus. J Bacteriol 175:7450–7462
    [Google Scholar]
  66. Trudeau K. G., Ward M. J., Zusman D. R. 1996; Identification and characterization of FrzZ, a novel response regulator necessary for swarming and fruiting-body formation in Myxococcus xanthus. Mol Microbiol 20:645–655 [CrossRef]
    [Google Scholar]
  67. van Bruggen A. H. C., Grogan R. G., Bogdanoff C. P., Waters C. M. 1988; Corky root of lettuce in California caused by a Gram-negative bacterium. Phytopathology 78:1139–1145 [CrossRef]
    [Google Scholar]
  68. Williams R. P., Qadri S. M. H. 1980; The pigment of Serratia. In the Genus Serratia pp 31–79 Edited by von Graevenitz A., Rubin S. J. Boca Raton: CRC Press;
    [Google Scholar]
  69. Wolgemuth C., Hoiczyk E., Kaiser D., Oster G. 2002; How myxobacteria glide. Curr Biol 12:369–377 [CrossRef]
    [Google Scholar]
  70. Wu S. S., Wu J., Kaiser D. 1997; The Myxococcus xanthus pilT locus is required for social gliding motility although pili are still produced. Mol Microbiol 23:109–121 [CrossRef]
    [Google Scholar]
  71. Zusman D. R. 1982; “Frizzy” mutants: a new class of aggregation-defective developmental mutants of Myxococcus xanthus. J Bacteriol 150:1430–1437
    [Google Scholar]
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