An evolutionary link between capsular biogenesis and surface motility in bacteria

Nature Reviews Microbiology

Volumn 13, Issue 5, 2015, Pages 318-326

  Agrebi, Rym ^a   Wartel, Morgane ^a   Brochier Armanet, Céline ^b   Mignot, Tâm ^a  

^a AIX MARSEILLE UNIVERSITÉ   (France)

^b UNIVERSITÉ LYON 1   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL CAPSULE; BACTERIAL GENOME; BIOGENESIS; CILIARY MOTILITY; GENE DUPLICATION; MOLECULAR EVOLUTION; MYXOCOCCUS XANTHUS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SPOROGENESIS; EVOLUTION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOVEMENT (PHYSIOLOGY); PHYSIOLOGY;

BACTERIA (MICROORGANISMS); MYXOCOCCUS XANTHUS;

BACTERIAL CAPSULES; BIOLOGICAL EVOLUTION; GENE EXPRESSION REGULATION, BACTERIAL; MOVEMENT; MYXOCOCCUS XANTHUS;

EID: 84928387585     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro3431     Document Type: Review

References (60)

1. Faro-Trindade, I. & Cook, P. R. Transcription factories: structures conserved during differentiation and evolution. Biochem. Soc. Trans. 34, 1133-1137 (2006).
2. Lapuente-Brun, E. et al. Supercomplex assembly determines electron flux in the mitochondrial electron transport chain. Science 340, 1567-1570 (2013).
3. Fronzes, R., Christie, P. J. & Waksman, G. The structural biology of type IV secretion systems. Nature Rev. Microbiol. 7, 703-714 (2009).
4. Jarrell, K. F. & McBride, M. J. The surprisingly diverse ways that prokaryotes move. Nature Rev. Microbiol. 6, 466-476 (2008).
5. Chevance, F. F. V. & Hughes, K. T. Coordinating assembly of a bacterial macromolecular machine. Nature Rev. Microbiol. 6, 455-465 (2008).
6. Pallen, M. J. & Matzke, N. J. From The Origin of Species to the origin of bacterial flagella. Nature Rev. Microbiol. 4, 784-790 (2006).
7. Snyder, L. A. S., Loman, N. J., Fütterer, K. & Pallen, M. J. Bacterial flagellar diversity and evolution: seek simplicity and distrust it? Trends Microbiol. 17, 1-5 (2009).
8. Abby, S. S. & Rocha, E. P. C. The non-flagellar type III secretion system evolved from the bacterial flagellum and diversified into host-cell adapted systems. PLoS Genet. 8, e1002983 (2012).
9. Wadhams, G. H. & Armitage, J. P. Making sense of it all: bacterial chemotaxis. Nature Rev. Mol. Cell Biol. 5, 1024-1037 (2004).
10. Liu, R. & Ochman, H. Stepwise formation of the bacterial flagellar system. Proc. Natl Acad. Sci. USA 104, 7116-7121 (2007).
11. Ko, M. & Park, C. Two novel flagellar components and H-NS are involved in the motor function of Escherichia coli. J. Mol. Biol. 303, 371-382 (2000).
12. Pelicic, V. Type IV pili: e pluribus unum? Mol. Microbiol. 68, 827-837 (2008).
13. Kroos, L. The Bacillus and Myxococcus developmental networks and their transcriptional regulators. Annu. Rev. Genet. 41, 13-39 (2007).
14. Chater, K. F., Biró, S., Lee, K. J., Palmer, T. & Schrempf, H. The complex extracellular biology of Streptomyces. FEMS Microbiol. Rev. 34, 171-198 (2010).
15. Wartel, M. et al. A versatile class of cell surface directional motors gives rise to gliding motility and sporulation in Myxococcus xanthus. PLoS Biol. 11, e1001728 (2013).
16. Zhang, Y., Ducret, A., Shaevitz, J. & Mignot, T. From individual cell motility to collective behaviors: insights from a prokaryote, Myxococcus xanthus. FEMS Microbiol. Rev. 36, 149-164 (2012).
17. Bui, N. K. et al. The peptidoglycan sacculus of Myxococcus xanthus has unusual structural features and is degraded during glycerol-induced myxospore development. J. Bacteriol. 191, 494-505 (2009).
18. Müller, F. D., Schink, C. W., Hoiczyk, E., Cserti, E. & Higgs, P. I. Spore formation in Myxococcus xanthus is tied to cytoskeleton functions and polysaccharide spore coat deposition. Mol. Microbiol. 83, 486-505 (2012).
19. Holkenbrink, C., Hoiczyk, E., Kahnt, J. & Higgs, P. I. Synthesis and assembly of a novel glycan layer in Myxococcus xanthus spores. J. Biol. Chem. 289, 32364-32378 (2014).
20. Sun, H., Zusman, D. R. & Shi, W. Y. Type IV pilus of Myxococcus xanthus is a motility apparatus controlled by the frz chemosensory system. Curr. Biol. 10, 1143-1146 (2000).
21. Nan, B. & Zusman, D. R. Uncovering the mystery of gliding motility in the myxobacteria. Annu. Rev. Genet. 45, 21-39 (2011).
22. Shi, W. & Zusman, D. R. The two motility systems of Myxococcus xanthus show different selective advantages on various surfaces. Proc. Natl Acad. Sci. USA 90, 3378-3382 (1993).
23. Mignot, T., Shaevitz, J. W., Hartzell, P. L. & Zusman, D. R. Evidence that focal adhesion complexes power bacterial gliding motility. Science 315, 853-856 (2007).
24. Luciano, J. et al. Emergence and modular evolution of a novel motility machinery in bacteria. PLoS Genet. 7, e1002268 (2011).
25. Nan, B., Mauriello, E. M., Sun, I. H., Wong, A. & Zusman, D. R. A multi-protein complex from Myxococcus xanthus required for bacterial gliding motility. Mol. Microbiol. 76, 1539-1554 (2010).
26. Morimoto, Y. V. & Minamino, T. Structure and function of the bi-directional bacterial flagellar motor. Biomolecules 4, 217-234 (2014).
27. Cascales, E., Lloubès, R. & Sturgis, J. N. The TolQ-TolR proteins energize TolA and share homologies with the flagellar motor proteins MotA-MotB. Mol. Microbiol. 42, 795-807 (2001).
28. Postle, K. & Larsen, R. A. TonB-dependent energy transduction between outer and cytoplasmic membranes. Biometals 20, 453-465 (2007).
29. Nan, B. et al. Myxobacteria gliding motility requires cytoskeleton rotation powered by proton motive force. Proc. Natl Acad. Sci. USA 108, 2498-2503 (2011).
30. Nan, B. et al. Flagella stator homologs function as motors for myxobacterial gliding motility by moving in helical trajectories. Proc. Natl Acad. Sci. USA 110, E1508-E1513 (2013).
31. Balagam, R. et al. Myxococcus xanthus gliding motors are elastically coupled to the substrate as predicted by the focal adhesion model of gliding motility. PLoS Comput. Biol. 10, e1003619 (2014).
32. Ducret, A., Valignat, M.-P., Mouhamar, F., Mignot, T. & Theodoly, O. Wet-surface-enhanced ellipsometric contrast microscopy identifies slime as a major adhesion factor during bacterial surface motility. Proc. Natl Acad. Sci. USA 109, 10036-10041 (2012).
33. Nan, B., McBride, M. J., Chen, J., Zusman, D. R. & Oster, G. Bacteria that glide with helical tracks. Curr. Biol. 24, R169-R173 (2014).
34. Sun, M., Wartel, M., Cascales, E., Shaevitz, J. W. & Mignot, T. Motor-driven intracellular transport powers bacterial gliding motility. Proc. Natl Acad. Sci. USA 108, 7559-7564 (2011).
35. Burchard, R. P. Trail following by gliding bacteria. J. Bacteriol. 152, 495-501 (1982).
36. Mauriello, E. M. F. et al. Bacterial motility complexes require the actin-like protein, MreB and the Ras homologue, MglA. EMBO J. 29, 315-326 (2010).
37. Patryn, J., Allen, K., Dziewanowska, K., Otto, R. & Hartzell, P. L. Localization of MglA, an essential gliding motility protein in Myxococcus xanthus. Cytoskeleton 67, 322-337 (2010).
38. Kojima, S. & Blair, D. F. The bacterial flagellar motor: structure and function of a complex molecular machine. Int. Rev. Cytol. 233, 93-134 (2004).
39. Goemaere, E. L., Cascales, E. & Lloubes, R. Mutational analyses define helix organization and key residues of a bacterial membrane energy-transducing complex. J. Mol. Biol. 366, 1424-1436 (2007).
40. Lazzaroni, J. C. et al. Transmembrane α-helix interactions are required for the functional assembly of the Escherichia coli Tol complex. J. Mol. Biol. 246, 1-7 (1995).
41. Goemaere, E. L., Devert, A., Lloubès, R. & Cascales, E. Movements of the TolR C-terminal domain depend on TolQR ionizable key residues and regulate activity of the Tol complex. J. Biol. Chem. 282, 17749-17757 (2007).
42. Zhang, X. Y.-Z. et al. Mapping the interactions between Escherichia coli tol subunits: rotation of the TolR transmembrane helix. J. Biol. Chem. 284, 4275-4282 (2009).
43. Dong, J.-H., Wen, J.-F. & Tian, H.-F. Homologs of eukaryotic Ras superfamily proteins in prokaryotes and their novel phylogenetic correlation with their eukaryotic analogs. Gene 396, 116-124 (2007).
44. Ozyamak, E., Kollman, J. M. & Komeili, A. Bacterial actins and their diversity. Biochemistry 52, 6928-6939 (2013).
45. Thomas, S. H. et al. The mosaic genome of Anaeromyxobacter dehalogenans strain 2CP-C suggests an aerobic common ancestor to the Delta-proteobacteria. PLoS ONE 3, e2103 (2008).
46. Goldman, B. S. et al. Evolution of sensory complexity recorded in a myxobacterial genome. Proc. Natl Acad. Sci. USA 103, 15200-15205 (2006).
47. Finnigan, G. C., Hanson-Smith, V., Stevens, T. H. & Thornton, J. W. Evolution of increased complexity in a molecular machine. Nature 481, 360-364 (2012).
48. Capra, E. J., Perchuk, B. S., Skerker, J. M. & Laub, M. T. Adaptive mutations that prevent crosstalk enable the expansion of paralogous signaling protein families. Cell 150, 222-232 (2012).
49. Skerker, J. M. et al. Rewiring the specificity of two-component signal transduction systems. Cell 133, 1043-1054 (2008).
50. Fiegna, F., Yu, Y.-T. N., Kadam, S. V. & Velicer, G. J. Evolution of an obligate social cheater to a superior cooperator. Nature 441, 310-314 (2006).
51. Velicer, G. J. & Yu, Y.-T. N. Evolution of novel cooperative swarming in the bacterium Myxococcus xanthus. Nature 425, 75-78 (2003).
52. Hizukuri, Y., Kojima, S. & Homma, M. Disulphide cross-linking between the stator and the bearing components in the bacterial flagellar motor. J. Biochem. 148, 309-318 (2010).
53. Howard, C. J. et al. Ancestral resurrection reveals evolutionary mechanisms of kinase plasticity. eLife 3, e04126 (2014).
54. Pallen, M. J., Penn, C. W. & Chaudhuri, R. R. Bacterial flagellar diversity in the post-genomic era. Trends Microbiol. 13, 143-149 (2005).
55. Paul, K., Erhardt, M., Hirano, T., Blair, D. F. & Hughes, K. T. Energy source of flagellar type III secretion. Nature 451, 489-492 (2008).
56. Whitfield, C. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu. Rev. Biochem. 75, 39-68 (2006).
57. Nakane, D., Sato, K., Wada, H., McBride, M. J. & Nakayama, K. Helical flow of surface protein required for bacterial gliding motility. Proc. Natl Acad. Sci. USA 110, 11145-11150 (2013).
58. Shrivastava, A., Rhodes, R. G., Pochiraju, S., Nakane, D. & McBride, M. J. Flavobacterium johnsoniae RemA is a mobile cell surface lectin involved in gliding. J. Bacteriol. 194, 3678-3688 (2012).
59. Shih, A. C.-C., Lee, D. T., Peng, C.-L. & Wu, Y.-W. Phylo-mLogo: an interactive and hierarchical multiple-logo visualization tool for alignment of many sequences. BMC Bioinformatics 8, 63 (2007).
60. Ronquist, F. et al. MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst. Biol.61, 539-542 (2012).