1887

Microbiology Society logo

Volume 162, Issue 1

The predatory life cycle of Free

Abstract

is a predatory bacterium and a model system for social behaviour in bacteria. forms thin biofilms, where cells work together to colonize new territory, invade prey colonies and lyse prey cells. Prey-cell lysis occurs at close proximity, and utilizes antibiotics such as myxovirescin, hydrolytic enzymes such as the protease MepA and extracellular outer-membrane vesicles that may facilitate delivery. Many questions about the mechanism of prey lysis remain, as well as a complete understanding of the vast hydrolytic and secondary metabolite potential present in the genome. However, it is clear that predation presents unique challenges for this bacterium, which are solved, in part, through the social behaviours at the disposal of . Here, we discuss the life cycle of , and the hypothesis that multicellular behaviour in this organism is critical to, and derives from, the challenges of growth as a bacterial predator.

  • Published Online:
© 2016 The Authors
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000208
2016-01-01
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/162/1/1.html?itemId=/content/journal/micro/10.1099/mic.0.000208&mimeType=html&fmt=ahah

References

  1. Abellón-Ruiz J., Bernal-Bernal D., Abellán M., Fontes M., Padmanabhan S., Murillo F. J., Elías-Arnanz M. 2014; The CarD/CarG regulatory complex is required for the action of several members of the large set of Myxococcus xanthus extracytoplasmic function σ factors. Environ Microbiol 16:2475–2490 [View Article][PubMed]
     [Google Scholar]
  2. Avadhani M., Geyer R., White D. C., Shimkets L. J. 2006; Lysophosphatidylethanolamine is a substrate for the short-chain alcohol dehydrogenase SocA from Myxococcus xanthus . J Bacteriol 188:8543–8550 [View Article][PubMed]
     [Google Scholar]
  3. Bacun-Druzina V., Cagalj Z., Gjuracic K. 2007; The growth advantage in stationary-phase (GASP) phenomenon in mixed cultures of enterobacteria. FEMS Microbiol Lett 266:119–127 [View Article][PubMed]
     [Google Scholar]
  4. Beebe J. M. 1941; The morphology and cytology of Myxococcus xanthus, n. sp. J Bacteriol 42:193–223[PubMed]
     [Google Scholar]
  5. Berg H. C., Brown D. A. 1972; Chemotaxis in Escherichia coli analysed by three-dimensional tracking. Nature 239:500–504 [View Article][PubMed]
     [Google Scholar]
  6. Berleman J. E., Bauer C. E. 2004; Characterization of cyst cell formation in the purple photosynthetic bacterium Rhodospirillum centenum . Microbiology 150:383–390 [View Article][PubMed]
     [Google Scholar]
  7. Berleman J. E., Kirby J. R. 2007; Multicellular development in Myxococcus xanthus is stimulated by predator-prey interactions. J Bacteriol 189:5675–5682 [View Article][PubMed]
     [Google Scholar]
  8. Berleman J. E., Kirby J. R. 2009; Deciphering the hunting strategy of a bacterial wolfpack. FEMS Microbiol Rev 33:942–957 [View Article][PubMed]
     [Google Scholar]
  9. Berleman J. E., Chumley T., Cheung P., Kirby J. R. 2006; Rippling is a predatory behavior in Myxococcus xanthus . J Bacteriol 188:5888–5895 [View Article][PubMed]
     [Google Scholar]
  10. Berleman J. E., Scott J., Chumley T., Kirby J. R. 2008; Predataxis behavior in Myxococcus xanthus . Proc Natl Acad Sci U S A 105:17127–17132 [View Article][PubMed]
     [Google Scholar]
  11. Berleman J. E., Vicente J. J., Davis A. E., Jiang S. Y., Seo Y.-E., Zusman D. R. 2011; FrzS regulates social motility in Myxococcus xanthus by controlling exopolysaccharide production. PLoS One 6:e23920 [View Article][PubMed]
     [Google Scholar]
  12. Berleman J. E., Allen S., Danielewicz M. A., Remis J. P., Gorur A., Cunha J., Hadi M. Z., Zusman D. R., Northen T. R., other authors. 2014; The lethal cargo of Myxococcus xanthus outer membrane vesicles. Front Microbiol 5:474[PubMed] [CrossRef]
     [Google Scholar]
  13. Dawid W. 2000; Biology and global distribution of myxobacteria in soils. FEMS Microbiol Rev 24:403–427 [View Article][PubMed]
     [Google Scholar]
  14. Ducret A., Valignat M.-P., Mouhamar F., Mignot T., Theodoly O. 2012; Wet-surface-enhanced ellipsometric contrast microscopy identifies slime as a major adhesion factor during bacterial surface motility. Proc Natl Acad Sci U S A 109:10036–10041 [View Article][PubMed]
     [Google Scholar]
  15. Ducret A., Fleuchot B., Bergam P., Mignot T. 2013; Direct live imaging of cell–cell protein transfer by transient outer membrane fusion in Myxococcus xanthus . eLife 2:e00868 [View Article][PubMed]
     [Google Scholar]
  16. Dworkin M. 1963; Nutritional regulation of morphogenesis in Myxococcus xanthus . J Bacteriol 86:67–72[PubMed]
     [Google Scholar]
  17. Eckhert E., Rangamani P., Davis A. E., Oster G., Berleman J. E. 2014; Dual biochemical oscillators may control cellular reversals in Myxococcus xanthus . Biophys J 107(11):2700–11 [CrossRef]
     [Google Scholar]
  18. Erken M., Lutz C., McDougald D. 2013; The rise of pathogens: predation as a factor driving the evolution of human pathogens in the environment. Microb Ecol 65:860–868 [View Article][PubMed]
     [Google Scholar]
  19. Evans A.G.L., Davey H. M., Cookson A., Currinn H., Cooke-Fox G., Stanczyk P. J., Whitworth D. E. 2012; Predatory activity of Myxococcus xanthus outer-membrane vesicles and properties of their hydrolase cargo. Microbiology 158:2742–2752 [View Article][PubMed]
     [Google Scholar]
  20. Fiegna F., Velicer G. J. 2005; Exploitative and hierarchical antagonism in a cooperative bacterium. PLoS Biol 3:e370 [View Article][PubMed]
     [Google Scholar]
  21. Giglio K. M., Caberoy N., Suen G., Kaiser D., Garza A. G. 2011; A cascade of coregulating enhancer binding proteins initiates and propagates a multicellular developmental program. Proc Natl Acad Sci U S A 108:E431–E439 [View Article][PubMed]
     [Google Scholar]
  22. Goldman B. S., Nierman W. C., Kaiser D., Slater S. C., Durkin A. S., Eisen J. A., Ronning C. M., Barbazuk W. B., Blanchard M., other authors. 2006; Evolution of sensory complexity recorded in a myxobacterial genome. Proc Natl Acad Sci U S A 103:15200–15205 [View Article][PubMed]
     [Google Scholar]
  23. Hagen D. C., Bretscher A. P., Kaiser D. 1978; Synergism between morphogenetic mutants of Myxococcus xanthus . Dev Biol 64:284–296 [View Article][PubMed]
     [Google Scholar]
  24. Hart B. A., Zahler S. A. 1966; Lytic enzyme produced by Myxococcus xanthus . J Bacteriol 92:1632–1637[PubMed]
     [Google Scholar]
  25. Hillesland K. L., Velicer G. J. 2005; Resource level affects relative performance of the two motility systems of Myxococcus xanthus . Microb Ecol 49:558–566 [View Article][PubMed]
     [Google Scholar]
  26. Hillesland K. L., Lenski R. E., Velicer G. J. 2007; Ecological variables affecting predatory success in Myxococcus xanthus . Microb Ecol 53:571–578 [View Article][PubMed]
     [Google Scholar]
  27. Hobley L., King J. R., Sockett R. E. 2006; Bdellovibrio predation in the presence of decoys: three-way bacterial interactions revealed by mathematical and experimental analyses. Appl Environ Microbiol 72:6757–6765 [View Article][PubMed]
     [Google Scholar]
  28. Holkenbrink C., Hoiczyk E., Kahnt J., Higgs P. I. 2014; Synthesis and assembly of a novel glycan layer in Myxococcus xanthus spores. J Biol Chem 289:32364–32378 [View Article][PubMed]
     [Google Scholar]
  29. Hu W., Yang Z., Lux R., Zhao M., Wang J., He X., Shi W. 2012; Direct visualization of the interaction between pilin and exopolysaccharides of Myxococcus xanthus with eGFP-fused PilA protein. FEMS Microbiol Lett 326:23–30 [View Article][PubMed]
     [Google Scholar]
  30. Huntley S., Hamann N., Wegener-Feldbrügge S., Treuner-Lange A., Kube M., Reinhardt R., Klages S., Müller R., Ronning C. M., other authors. 2011; Comparative genomic analysis of fruiting body formation in Myxococcales. Mol Biol Evol 28:1083–1097 [View Article][PubMed]
     [Google Scholar]
  31. Hyun H., Chung J., Kim J., Lee J. S., Kwon B.-M., Son K.-H., Cho K. 2008; Isolation of Sorangium cellulosum carrying epothilone gene clusters. J Microbiol Biotechnol 18:1416–1422[PubMed]
     [Google Scholar]
  32. Inouye S., Harada W., Zusman D., Inouye M. 1981; Development-specific protein S of Myxococcus xanthus: purification and characterization. J Bacteriol 148:678–683[PubMed]
     [Google Scholar]
  33. Jelsbak L., Givskov M., Kaiser D. 2005; Enhancer-binding proteins with a forkhead-associated domain and the σ54 regulon in Myxococcus xanthus fruiting body development. Proc Natl Acad Sci U S A 102:3010–3015 [View Article][PubMed]
     [Google Scholar]
  34. Justice S. S., Harrison A., Becknell B., Mason K. M. 2014; Bacterial differentiation, development, and disease: mechanisms for survival. FEMS Microbiol Lett 360:1–8 [View Article][PubMed]
     [Google Scholar]
  35. Kaimer C., Zusman D. R. 2013; Phosphorylation-dependent localization of the response regulator FrzZ signals cell reversals in Myxococcus xanthus . Mol Microbiol 88:740–753 [View Article][PubMed]
     [Google Scholar]
  36. Kaimer C., Berleman J. E., Zusman D. R. 2012; Chemosensory signaling controls motility and subcellular polarity in Myxococcus xanthus . Curr Opin Microbiol 15:751–757 [View Article][PubMed]
     [Google Scholar]
  37. 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 [View Article][PubMed]
     [Google Scholar]
  38. Kaiser D. 2003; Coupling cell movement to multicellular development in myxobacteria. Nat Rev Microbiol 1:45–54 [View Article][PubMed]
     [Google Scholar]
  39. Kaiser D., Crosby C. 1983; Cell movement and its coordination in swarms of Myxococcus xanthus . Cell Motil 3:227–245 [View Article]
     [Google Scholar]
  40. Kearns D. B., Losick R. 2005; Cell population heterogeneity during growth of Bacillus subtilis . Genes Dev 19:3083–3094 [View Article][PubMed]
     [Google Scholar]
  41. Keilberg D., Søgaard-Andersen L. 2014; Regulation of bacterial cell polarity by small GTPases. Biochemistry 53:1899–1907 [View Article][PubMed]
     [Google Scholar]
  42. 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 [View Article][PubMed]
     [Google Scholar]
  43. Kottel R. H., Bacon K., Clutter D., White D. 1975; Coats from Myxococcus xanthus: characterization and synthesis during myxospore differentiation. J Bacteriol 124:550–557[PubMed]
     [Google Scholar]
  44. Kroos L., Kuspa A., Kaiser D. 1990; Defects in fruiting body development caused by Tn5 lac insertions in Myxococcus xanthus . J Bacteriol 172(1):484–7
     [Google Scholar]
  45. Lambert C., Fenton A. K., Hobley L., Sockett R. E. 2011; Predatory Bdellovibrio bacteria use gliding motility to scout for prey on surfaces. J Bacteriol 193:3139–3141 [View Article][PubMed]
     [Google Scholar]
  46. Lee B., Holkenbrink C., Treuner-Lange A., Higgs P. I. 2012; Myxococcus xanthus developmental cell fate production: heterogeneous accumulation of developmental regulatory proteins and reexamination of the role of MazF in developmental lysis. J Bacteriol 194:3058–3068 [View Article][PubMed]
     [Google Scholar]
  47. Lerner T. R., Lovering A. L., Bui N. K., Uchida K., Aizawa S., Vollmer W., Sockett R. E. 2012; Specialized peptidoglycan hydrolases sculpt the intra-bacterial niche of predatory Bdellovibrio and increase population fitness. PLoS Pathog 8:e1002524 [View Article][PubMed]
     [Google Scholar]
  48. Li Y., Sun H., Ma X., Lu A., Lux R., Zusman D., Shi W. 2003; Extracellular polysaccharides mediate pilus retraction during social motility of Myxococcus xanthus . Proc Natl Acad Sci U S A 100:5443–5448 [View Article][PubMed]
     [Google Scholar]
  49. Li J., Wang Y., Zhang C. Y., Zhang W. Y., Jiang D. M., Wu Z. H., Liu H., Li Y. Z. 2010; Myxococcus xanthus viability depends on GroEL supplied by either of two genes, but the paralogs have different functions during heat shock, predation, and development. J Bacteriol 192:1875–1881 [View Article][PubMed]
     [Google Scholar]
  50. Lindsay D., Brözel V. S., Von Holy A. 2006; Biofilm-spore response in Bacillus cereus and Bacillus subtilis during nutrient limitation. J Food Prot 69:1168–1172[PubMed]
     [Google Scholar]
  51. Liu W.-T., Yang Y.-L., Xu Y., Lamsa A., Haste N. M., Yang J. Y., Ng J., Gonzalez D., Ellermeier C. D., other authors. 2010; Imaging mass spectrometry of intraspecies metabolic exchange revealed the cannibalistic factors of Bacillus subtilis . Proc Natl Acad Sci U S A 107:16286–16290 [View Article][PubMed]
     [Google Scholar]
  52. Lueders T., Kindler R., Miltner A., Friedrich M. W., Kaestner M. 2006; Identification of bacterial micropredators distinctively active in a soil microbial food web. Appl Environ Microbiol 72:5342–5348 [View Article][PubMed]
     [Google Scholar]
  53. Mauriello E.M.F., Mignot T., Yang Z., Zusman D. R. 2010; Gliding motility revisited: how do the myxobacteria move without flagella?. Microbiol Mol Biol Rev 74:229–249 [View Article][PubMed]
     [Google Scholar]
  54. McBride M. J., Zusman D. R. 1996; Behavioral analysis of single cells of Myxococcus xanthus in response to prey cells of Escherichia coli . FEMS Microbiol Lett 137:227–231 [View Article][PubMed]
     [Google Scholar]
  55. Mendes-Soares H., Velicer G. J. 2013; Decomposing predation: testing for parameters that correlate with predatory performance by a social bacterium. Microb Ecol 65:415–423 [View Article][PubMed]
     [Google Scholar]
  56. Müller F. D., Schink C. W., Hoiczyk E., Cserti E., Higgs P. I. 2012; Spore formation in Myxococcus xanthus is tied to cytoskeleton functions and polysaccharide spore coat deposition. Mol Microbiol 83:486–505 [View Article][PubMed]
     [Google Scholar]
  57. Nan B., Zusman D. R. 2011; Uncovering the mystery of gliding motility in the Myxobacteria. Annu Rev Genet 45:21–39 [View Article][PubMed]
     [Google Scholar]
  58. Nan B., Chen J., Neu J. C., Berry R. M., Oster G., Zusman D. R. 2011; Myxobacteria gliding motility requires cytoskeleton rotation powered by proton motive force. Proc Natl Acad Sci U S A 108:2498–2503 [View Article][PubMed]
     [Google Scholar]
  59. Nandy S. K., Bapat P. M., Venkatesh K. V. 2007; Sporulating bacteria prefers predation to cannibalism in mixed cultures. FEBS Lett 581(1):151–6 [CrossRef]
     [Google Scholar]
  60. Noren B., Raper K. B. 1962; Antibiotic activity of myxobacteria in relation to their bacteriolytic capacity. J Bacteriol 84:157–162[PubMed]
     [Google Scholar]
  61. Nudleman E., Wall D., Kaiser D. 2005; Cell-to-cell transfer of bacterial outer membrane lipoproteins. Science 309:125–127 [View Article][PubMed]
     [Google Scholar]
  62. O'Connor K. A., Zusman D. R. 1991; Behavior of peripheral rods and their role in the life cycle of Myxococcus xanthus . J Bacteriol 173:3342–3355[PubMed]
     [Google Scholar]
  63. Palsdottir H., Remis J. P., Schaudinn C., O'Toole E., Lux R., Shi W., McDonald K. L., Costerton J. W., Auer M. 2009; Three-dimensional macromolecular organization of cryofixed Myxococcus xanthus biofilms as revealed by electron microscopic tomography. J Bacteriol 191:2077–2082 [View Article][PubMed]
     [Google Scholar]
  64. Pan H., He X., Lux R., Luan J., Shi W. 2013; Killing of Escherichia coli by Myxococcus xanthus in aqueous environments requires exopolysaccharide-dependent physical contact. Microb Ecol 66:630–638 [View Article][PubMed]
     [Google Scholar]
  65. Pathak D. T., Wall D. 2012; Identification of the cglC, cglD, cglE, and cglF genes and their role in cell contact-dependent gliding motility in Myxococcus xanthus . J Bacteriol 194:1940–1949 [View Article][PubMed]
     [Google Scholar]
  66. Pathak D. T., Wei X., Wall D. 2012; Myxobacterial tools for social interactions. Res Microbiol 163:579–591 [View Article][PubMed]
     [Google Scholar]
  67. Pérez J., Jiménez-Zurdo J. I., Martínez-Abarca F., Millán V., Shimkets L. J., Muñoz-Dorado J. 2014; Rhizobial galactoglucan determines the predatory pattern of Myxococcus xanthus and protects Sinorhizobium meliloti from predation. Environ Microbiol 16:2341–2350 [View Article][PubMed]
     [Google Scholar]
  68. Pham V. D., Shebelut C. W., Diodati M. E., Bull C. T., Singer M. 2005; Mutations affecting predation ability of the soil bacterium Myxococcus xanthus . Microbiology 151:1865–1874 [View Article][PubMed]
     [Google Scholar]
  69. Pukatzki S., Provenzano D. 2013; Vibrio cholerae as a predator: lessons from evolutionary principles. Front Microbiol 4:384[PubMed] [CrossRef]
     [Google Scholar]
  70. Remis J. P., Wei D., Gorur A., Zemla M., Haraga J., Allen S., Witkowska H. E., Costerton J. W., Berleman J. E., Auer M. 2014; Bacterial social networks: structure and composition of Myxococcus xanthus outer membrane vesicle chains. Environ Microbiol 16:598–610 [View Article][PubMed]
     [Google Scholar]
  71. 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[PubMed]
     [Google Scholar]
  72. Rodriguez-Soto J. P., Kaiser D. 1997; Identification and localization of the Tgl protein, which is required for Myxococcus xanthus social motility. J Bacteriol 179:4372–4381[PubMed]
     [Google Scholar]
  73. Rosenberg E., Vaks B., Zuckerberg A. 1973; Bactericidal action of an antibiotic produced by Myxococcus xanthus . Antimicrob Agents Chemother 4:507–513 [View Article][PubMed]
     [Google Scholar]
  74. Rosenberg E., Keller K. H., Dworkin M. 1977; Cell density-dependent growth of Myxococcus xanthus on casein. J Bacteriol 129:770–777[PubMed]
     [Google Scholar]
  75. Shank E. A., Klepac-Ceraj V., Collado-Torres L., Powers G. E., Losick R., Kolter R. 2011; Interspecies interactions that result in Bacillus subtilis forming biofilms are mediated mainly by members of its own genus. Proc Natl Acad Sci U S A 108:E1236–E1243 [View Article][PubMed]
     [Google Scholar]
  76. 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 [View Article][PubMed]
     [Google Scholar]
  77. 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 [View Article][PubMed]
     [Google Scholar]
  78. Singh B. N. 1947; Myxobacteria in soils and composts; their distribution, number and lytic action on bacteria. J Gen Microbiol 1:1–10 [View Article][PubMed]
     [Google Scholar]
  79. Sockett R. E. 2009; Predatory lifestyle of Bdellovibrio bacteriovorus . Annu Rev Microbiol 63:523–539 [View Article][PubMed]
     [Google Scholar]
  80. Sun H., Zusman D. R., Shi W. 2000; Type IV pilus of Myxococcus xanthus is a motility apparatus controlled by the frz chemosensory system. Curr Biol 10:1143–1146 [View Article][PubMed]
     [Google Scholar]
  81. van Elsas J. D., Semenov A. V., Costa R., Trevors J. T. 2011; Survival of Escherichia coli in the environment: fundamental and public health aspects. ISME J 5:173–183 [View Article][PubMed]
     [Google Scholar]
  82. Vlamakis H., Aguilar C., Losick R., Kolter R. 2008; Control of cell fate by the formation of an architecturally complex bacterial community. Genes Dev 22:945–953 [View Article][PubMed]
     [Google Scholar]
  83. Volz C., Kegler C., Müller R. 2012; Enhancer binding proteins act as hetero-oligomers and link secondary metabolite production to myxococcal development, motility, and predation. Chem Biol 19:1447–1459 [View Article][PubMed]
     [Google Scholar]
  84. Wang Y., Li X., Zhang W., Zhou X., Li Y. Z. 2014; The groEL2 gene, but not groEL1, is required for biosynthesis of the secondary metabolite myxovirescin in Myxococcus xanthus DK1622. Microbiology 160:488–495 [View Article][PubMed]
     [Google Scholar]
  85. Wartel M., Ducret A., Thutupalli S., Czerwinski F., Le Gall A.-V., Mauriello E.M.F., Bergam P., Brun Y. V., Shaevitz J., Mignot T. 2013; A versatile class of cell surface directional motors gives rise to gliding motility and sporulation in Myxococcus xanthus . PLoS Biol 11:e1001728 [View Article][PubMed]
     [Google Scholar]
  86. Welch R., Kaiser D. 2001; Cell behavior in traveling wave patterns of myxobacteria. Proc Natl Acad Sci U S A 98:14907–14912 [View Article][PubMed]
     [Google Scholar]
  87. Wolgemuth C., Hoiczyk E., Kaiser D., Oster G. 2002; How myxobacteria glide. Curr Biol 12:369–377 [View Article][PubMed]
     [Google Scholar]
  88. Xiao Y., Wei X., Ebright R., Wall D. 2011; Antibiotic production by myxobacteria plays a role in predation. J Bacteriol 193:4626–4633 [View Article][PubMed]
     [Google Scholar]
  89. Xiao Y., Gerth K., Müller R., Wall D. 2012; Myxobacterium-produced antibiotic TA (myxovirescin) inhibits type II signal peptidase. Antimicrob Agents Chemother 56:2014–2021 [View Article][PubMed]
     [Google Scholar]
  90. Zhang H., Vaksman Z., Litwin D. B., Shi P., Kaplan H. B., Igoshin O. A. 2012; The mechanistic basis of Myxococcus xanthus rippling behavior and its physiological role during predation. PLOS Comput Biol 8:e1002715 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000208
Loading
The predatory life cycle of Myxococcus xanthus
Microbiology 162, 1 (2016); https://doi.org/10.1099/mic.0.000208
/content/journal/micro/10.1099/mic.0.000208
/content/journal/micro/10.1099/mic.0.000208
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error