1887

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.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000208
2016-01-01
2020-03-30
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 Microbiol16:2475–2490 [CrossRef][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 Bacteriol188:8543–8550 [CrossRef][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 Lett266:119–127 [CrossRef][PubMed]
    [Google Scholar]
  4. Beebe J. M.. 1941; The morphology and cytology of Myxococcus xanthus, n. sp. J Bacteriol42:193–223[PubMed]
    [Google Scholar]
  5. Berg H. C., Brown D. A.. 1972; Chemotaxis in Escherichia coli analysed by three-dimensional tracking. Nature239:500–504 [CrossRef][PubMed]
    [Google Scholar]
  6. Berleman J. E., Bauer C. E.. 2004; Characterization of cyst cell formation in the purple photosynthetic bacterium Rhodospirillum centenum . Microbiology150:383–390 [CrossRef][PubMed]
    [Google Scholar]
  7. Berleman J. E., Kirby J. R.. 2007; Multicellular development in Myxococcus xanthus is stimulated by predator-prey interactions. J Bacteriol189:5675–5682 [CrossRef][PubMed]
    [Google Scholar]
  8. Berleman J. E., Kirby J. R.. 2009; Deciphering the hunting strategy of a bacterial wolfpack. FEMS Microbiol Rev33:942–957 [CrossRef][PubMed]
    [Google Scholar]
  9. Berleman J. E., Chumley T., Cheung P., Kirby J. R.. 2006; Rippling is a predatory behavior in Myxococcus xanthus . J Bacteriol188:5888–5895 [CrossRef][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 A105:17127–17132 [CrossRef][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 One6:e23920 [CrossRef][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 Microbiol5:474[PubMed][CrossRef]
    [Google Scholar]
  13. Dawid W.. 2000; Biology and global distribution of myxobacteria in soils. FEMS Microbiol Rev24:403–427 [CrossRef][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 A109:10036–10041 [CrossRef][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 . eLife2:e00868 [CrossRef][PubMed]
    [Google Scholar]
  16. Dworkin M.. 1963; Nutritional regulation of morphogenesis in Myxococcus xanthus . J Bacteriol86:67–72[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 J107(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 Ecol65:860–868 [CrossRef][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. Microbiology158:2742–2752 [CrossRef][PubMed]
    [Google Scholar]
  20. Fiegna F., Velicer G. J.. 2005; Exploitative and hierarchical antagonism in a cooperative bacterium. PLoS Biol3:e370 [CrossRef][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 A108:E431–E439 [CrossRef][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 A103:15200–15205 [CrossRef][PubMed]
    [Google Scholar]
  23. Hagen D. C., Bretscher A. P., Kaiser D.. 1978; Synergism between morphogenetic mutants of Myxococcus xanthus . Dev Biol64:284–296 [CrossRef][PubMed]
    [Google Scholar]
  24. Hart B. A., Zahler S. A.. 1966; Lytic enzyme produced by Myxococcus xanthus . J Bacteriol92:1632–1637[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 Ecol49:558–566 [CrossRef][PubMed]
    [Google Scholar]
  26. Hillesland K. L., Lenski R. E., Velicer G. J.. 2007; Ecological variables affecting predatory success in Myxococcus xanthus . Microb Ecol53:571–578 [CrossRef][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 Microbiol72:6757–6765 [CrossRef][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 Chem289:32364–32378 [CrossRef][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 Lett326:23–30 [CrossRef][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 Evol28:1083–1097 [CrossRef][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 Biotechnol18:1416–1422[PubMed]
    [Google Scholar]
  32. Inouye S., Harada W., Zusman D., Inouye M.. 1981; Development-specific protein S of Myxococcus xanthus: purification and characterization. J Bacteriol148:678–683[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 A102:3010–3015 [CrossRef][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 Lett360:1–8 [CrossRef][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 Microbiol88:740–753 [CrossRef][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 Microbiol15:751–757 [CrossRef][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 A76:5952–5956 [CrossRef][PubMed]
    [Google Scholar]
  38. Kaiser D.. 2003; Coupling cell movement to multicellular development in myxobacteria. Nat Rev Microbiol1:45–54 [CrossRef][PubMed]
    [Google Scholar]
  39. Kaiser D., Crosby C.. 1983; Cell movement and its coordination in swarms of Myxococcus xanthus . Cell Motil3:227–245 [CrossRef]
    [Google Scholar]
  40. Kearns D. B., Losick R.. 2005; Cell population heterogeneity during growth of Bacillus subtilis . Genes Dev19:3083–3094 [CrossRef][PubMed]
    [Google Scholar]
  41. Keilberg D., Søgaard-Andersen L.. 2014; Regulation of bacterial cell polarity by small GTPases. Biochemistry53:1899–1907 [CrossRef][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 . Cell61:19–26 [CrossRef][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 Bacteriol124:550–557[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 Bacteriol172(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 Bacteriol193:3139–3141 [CrossRef][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 Bacteriol194:3058–3068 [CrossRef][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 Pathog8:e1002524 [CrossRef][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 A100:5443–5448 [CrossRef][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 Bacteriol192:1875–1881 [CrossRef][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 Prot69:1168–1172[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 A107:16286–16290 [CrossRef][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 Microbiol72:5342–5348 [CrossRef][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 Rev74:229–249 [CrossRef][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 Lett137:227–231 [CrossRef][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 Ecol65:415–423 [CrossRef][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 Microbiol83:486–505 [CrossRef][PubMed]
    [Google Scholar]
  57. Nan B., Zusman D. R.. 2011; Uncovering the mystery of gliding motility in the Myxobacteria. Annu Rev Genet45:21–39 [CrossRef][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 A108:2498–2503 [CrossRef][PubMed]
    [Google Scholar]
  59. Nandy S. K., Bapat P. M., Venkatesh K. V.. 2007; Sporulating bacteria prefers predation to cannibalism in mixed cultures. FEBS Lett581(1):151–6[CrossRef]
    [Google Scholar]
  60. Noren B., Raper K. B.. 1962; Antibiotic activity of myxobacteria in relation to their bacteriolytic capacity. J Bacteriol84:157–162[PubMed]
    [Google Scholar]
  61. Nudleman E., Wall D., Kaiser D.. 2005; Cell-to-cell transfer of bacterial outer membrane lipoproteins. Science309:125–127 [CrossRef][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 Bacteriol173:3342–3355[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 Bacteriol191:2077–2082 [CrossRef][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 Ecol66:630–638 [CrossRef][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 Bacteriol194:1940–1949 [CrossRef][PubMed]
    [Google Scholar]
  66. Pathak D. T., Wei X., Wall D.. 2012; Myxobacterial tools for social interactions. Res Microbiol163:579–591 [CrossRef][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 Microbiol16:2341–2350 [CrossRef][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 . Microbiology151:1865–1874 [CrossRef][PubMed]
    [Google Scholar]
  69. Pukatzki S., Provenzano D.. 2013; Vibrio cholerae as a predator: lessons from evolutionary principles. Front Microbiol4:384[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 Microbiol16:598–610 [CrossRef][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 Bacteriol181:4381–4390[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 Bacteriol179:4372–4381[PubMed]
    [Google Scholar]
  73. Rosenberg E., Vaks B., Zuckerberg A.. 1973; Bactericidal action of an antibiotic produced by Myxococcus xanthus . Antimicrob Agents Chemother4:507–513 [CrossRef][PubMed]
    [Google Scholar]
  74. Rosenberg E., Keller K. H., Dworkin M.. 1977; Cell density-dependent growth of Myxococcus xanthus on casein. J Bacteriol129:770–777[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 A108:E1236–E1243 [CrossRef][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 A90:3378–3382 [CrossRef][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 A93:4142–4146 [CrossRef][PubMed]
    [Google Scholar]
  78. Singh B. N.. 1947; Myxobacteria in soils and composts; their distribution, number and lytic action on bacteria. J Gen Microbiol1:1–10 [CrossRef][PubMed]
    [Google Scholar]
  79. Sockett R. E.. 2009; Predatory lifestyle of Bdellovibrio bacteriovorus . Annu Rev Microbiol63:523–539 [CrossRef][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 Biol10:1143–1146 [CrossRef][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 J5:173–183 [CrossRef][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 Dev22:945–953 [CrossRef][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 Biol19:1447–1459 [CrossRef][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. Microbiology160:488–495 [CrossRef][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 Biol11:e1001728 [CrossRef][PubMed]
    [Google Scholar]
  86. Welch R., Kaiser D.. 2001; Cell behavior in traveling wave patterns of myxobacteria. Proc Natl Acad Sci U S A98:14907–14912 [CrossRef][PubMed]
    [Google Scholar]
  87. Wolgemuth C., Hoiczyk E., Kaiser D., Oster G.. 2002; How myxobacteria glide. Curr Biol12:369–377 [CrossRef][PubMed]
    [Google Scholar]
  88. Xiao Y., Wei X., Ebright R., Wall D.. 2011; Antibiotic production by myxobacteria plays a role in predation. J Bacteriol193:4626–4633 [CrossRef][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 Chemother56:2014–2021 [CrossRef][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 Biol8:e1002715 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000208
Loading
/content/journal/micro/10.1099/mic.0.000208
Loading

Data & Media loading...

Most cited this month

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