1887

Abstract

Fifty years of research has transformed our understanding of bacterial movement from one of description, based on a limited number of electron micrographs and some low-magnification studies of cells moving towards or away from chemical effectors, to probably the best understood behavioural system in biology. We have a molecular understanding of how bacteria sense and respond to changes in their environment and detailed structural insights into the workings of one of the most complex motor structures we know of. Thanks to advances in genomics we also understand how, through evolution, different species have tuned and adapted a core shared system to optimize behaviour in their specific environment. In this review, I will highlight some of the unexpected findings we made during my over 40-year career, how those findings changed some of our understanding of bacterial behaviour and biochemistry and some of the battles to have those observations accepted.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2024-02-16
2024-05-20
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References

  1. Sourjik V, Wingreen NS. Responding to chemical gradients: bacterial chemotaxis. Curr Opin Cell Biol 2012; 24:262–268 [View Article] [PubMed]
    [Google Scholar]
  2. Mesibov R, Ordal GW, Adler J. The range of attractant concentrations for bacterial chemotaxis and the threshold and size of response over this range. Weber law and related phenomena. J Gen Physiol 1973; 62:203–223 [View Article] [PubMed]
    [Google Scholar]
  3. Gumerov VM, Andrianova EP, Zhulin IB. Diversity of bacterial chemosensory systems. Curr Opin Microbiol 2021; 61:42–50 [View Article] [PubMed]
    [Google Scholar]
  4. Beeby M, Ribardo DA, Brennan CA, Ruby EG, Jensen GJ et al. Diverse high-torque bacterial flagellar motors assemble wider stator rings using a conserved protein scaffold. Proc Natl Acad Sci U S A 2016; 113:E1917–E1926 [View Article] [PubMed]
    [Google Scholar]
  5. Asai Y, Kojima S, Kato H, Nishioka N, Kawagishi I et al. Putative channel components for the fast-rotating sodium-driven flagellar motor of a marine bacterium. J Bacteriol 1997; 179:5104–5110 [View Article] [PubMed]
    [Google Scholar]
  6. Berg HC. Physical constraints on microbial behavior how you act if you are very small. J Chem Ecol 1990; 16:119–120 [View Article] [PubMed]
    [Google Scholar]
  7. Brown DA, Berg HC. Temporal stimulation of chemotaxis in Escherichia coli. Proc Natl Acad Sci U S A 1974; 71:1388–1392 [View Article] [PubMed]
    [Google Scholar]
  8. Macnab RM. How bacteria assemble flagella. Annu Rev Microbiol 2003; 57:77–100 [View Article] [PubMed]
    [Google Scholar]
  9. Abrusci P, McDowell MA, Lea SM, Johnson S. Building a secreting nanomachine: a structural overview of the T3SS. Curr Opin Struct Biol 2014; 25:111–117 [View Article] [PubMed]
    [Google Scholar]
  10. Konishi M, Kanbe M, McMurry JL, Aizawa S-I. Flagellar formation in C-ring-defective mutants by overproduction of FliI, the ATPase specific for flagellar type III secretion. J Bacteriol 2009; 191:6186–6191 [View Article] [PubMed]
    [Google Scholar]
  11. Erhardt M, Namba K, Hughes KT. Bacterial nanomachines: the flagellum and type III injectisome. Cold Spring Harb Perspect Biol 2010; 2:a000299 [View Article] [PubMed]
    [Google Scholar]
  12. Deme JC, Johnson S, Vickery O, Aron A, Monkhouse H et al. Structures of the stator complex that drives rotation of the bacterial flagellum. Nat Microbiol 2020; 5:1553–1564 [View Article] [PubMed]
    [Google Scholar]
  13. Manson MD, Tedesco P, Berg HC, Harold FM, Van der Drift C. A protonmotive force drives bacterial flagella. Proc Natl Acad Sci U S A 1977; 74:3060–3064 [View Article] [PubMed]
    [Google Scholar]
  14. Silverman M, Simon M. Flagellar rotation and the mechanism of bacterial motility. Nature 1974; 249:73–74 [View Article] [PubMed]
    [Google Scholar]
  15. Block SM, Berg HC. Successive incorporation of force-generating units in the bacterial rotary motor. Nature 1984; 309:470–472 [View Article] [PubMed]
    [Google Scholar]
  16. Van Way SM, Hosking ER, Braun TF, Manson MD. Mot protein assembly into the bacterial flagellum: a model based on mutational analysis of the motB gene. J Mol Biol 2000; 297:7–24 [View Article] [PubMed]
    [Google Scholar]
  17. Leake MC, Chandler JH, Wadhams GH, Bai F, Berry RM et al. Stoichiometry and turnover in single, functioning membrane protein complexes. Nature 2006; 443:355–358 [View Article] [PubMed]
    [Google Scholar]
  18. Tipping MJ, Steel BC, Delalez NJ, Berry RM, Armitage JP. Quantification of flagellar motor stator dynamics through in vivo proton-motive force control. Mol Microbiol 2013; 87:338–347 [View Article] [PubMed]
    [Google Scholar]
  19. Tipping MJ, Delalez NJ, Lim R, Berry RM, Armitage JP. Load-dependent assembly of the bacterial flagellar motor. mBio 2013; 4:e00551-13 [View Article] [PubMed]
    [Google Scholar]
  20. Delalez NJ, Wadhams GH, Rosser G, Xue Q, Brown MT et al. Signal-dependent turnover of the bacterial flagellar switch protein FliM. Proc Natl Acad Sci U S A 2010; 107:11347–11351 [View Article] [PubMed]
    [Google Scholar]
  21. Delalez NJ, Berry RM, Armitage JP. Stoichiometry and turnover of the bacterial flagellar switch protein FliN. mBio 2014; 5:e01216-14 [View Article] [PubMed]
    [Google Scholar]
  22. Paulick A, Delalez NJ, Brenzinger S, Steel BC, Berry RM et al. Dual stator dynamics in the Shewanella oneidensis MR-1 flagellar motor. Mol Microbiol 2015; 96:993–1001 [View Article] [PubMed]
    [Google Scholar]
  23. Brenzinger S, Dewenter L, Delalez NJ, Leicht O, Berndt V et al. Mutations targeting the plug-domain of the Shewanella oneidensis proton-driven stator allow swimming at increased viscosity and under anaerobic conditions. Mol Microbiol 2016; 102:925–938 [View Article] [PubMed]
    [Google Scholar]
  24. Kuchma SL, Delalez NJ, Filkins LM, Snavely EA, Armitage JP et al. Cyclic di-GMP-mediated repression of swarming motility by Pseudomonas aeruginosa PA14 requires the MotAB stator. J Bacteriol 2015; 197:420–430 [View Article] [PubMed]
    [Google Scholar]
  25. Baker AE, Diepold A, Kuchma SL, Scott JE, Ha DG et al. PilZ domain protein FlgZ mediates cyclic Di-GMP-dependent swarming motility control in Pseudomonas aeruginosa. J Bacteriol 2016; 198:1837–1846 [View Article] [PubMed]
    [Google Scholar]
  26. Baker AE, Webster SS, Diepold A, Kuchma SL, Bordeleau E et al. Flagellar stators stimulate c-di-GMP production by Pseudomonas aeruginosa. J Bacteriol 2019; 201:18 [View Article] [PubMed]
    [Google Scholar]
  27. Armitage JP, Ingham C, Evans MC. Role of proton motive force in phototactic and aerotactic responses of Rhodopseudomonas sphaeroides. J Bacteriol 1985; 161:967–972 [View Article] [PubMed]
    [Google Scholar]
  28. Armitage JP, Macnab RM. Unidirectional, intermittent rotation of the flagellum of Rhodobacter sphaeroides. J Bacteriol 1987; 169:514–518 [View Article] [PubMed]
    [Google Scholar]
  29. Pilizota T, Brown MT, Leake MC, Branch RW, Berry RM et al. A molecular brake, not a clutch, stops the Rhodobacter sphaeroides flagellar motor. Proc Natl Acad Sci U S A 2009; 106:11582–11587 [View Article] [PubMed]
    [Google Scholar]
  30. Ramírez-Cabrera V, Poggio S, Domenzain C, Osorio A, Dreyfus G et al. A novel component of the Rhodobacter sphaeroides Fla1 flagellum is essential for motor rotation. J Bacteriol 2012; 194:6174–6183 [View Article] [PubMed]
    [Google Scholar]
  31. Mackenzie C, Choudhary M, Larimer FW, Predki PF, Stilwagen S et al. The home stretch, a first analysis of the nearly completed genome of Rhodobacter sphaeroides 2.4.1. Photosynth Res 2001; 70:19–41 [View Article] [PubMed]
    [Google Scholar]
  32. de la Mora J, Uchida K, del Campo AM, Camarena L, Aizawa S-I et al. Structural characterization of the Fla2 flagellum of Rhodobacter sphaeroides. J Bacteriol 2015; 197:2859–2866 [View Article] [PubMed]
    [Google Scholar]
  33. Camarena L, Dreyfus G. Living in a foster home: the single subpolar flagellum Fla1 of Rhodobacter sphaeroides. Biomolecules 2020; 10:774 [View Article] [PubMed]
    [Google Scholar]
  34. Martínez-del Campo A, Ballado T, Camarena L, Dreyfus G. In Rhodobacter sphaeroides, chemotactic operon 1 regulates rotation of the flagellar system 2. J Bacteriol 2011; 193:6781–6786 [View Article] [PubMed]
    [Google Scholar]
  35. Poggio S, Abreu-Goodger C, Fabela S, Osorio A, Dreyfus G et al. A complete set of flagellar genes acquired by horizontal transfer coexists with the endogenous flagellar system in Rhodobacter sphaeroides. J Bacteriol 2007; 189:3208–3216 [View Article] [PubMed]
    [Google Scholar]
  36. Hernandez-Valle J, Domenzain C, de la Mora J, Poggio S, Dreyfus G et al. The master regulators of the Fla1 and Fla2 flagella of Rhodobacter sphaeroides control the expression of their cognate CheY proteins. J Bacteriol 2017; 199:e00670-16 [View Article] [PubMed]
    [Google Scholar]
  37. Clayton RK. Tactic responses and metabolic activities in Rhodospirillum rubrum. Arch Mikrobiol 1955; 22:204–213 [View Article]
    [Google Scholar]
  38. Clayton RK. On the interplay of environmental factors affecting taxis and motility in Rhodospirillum rubrum. Arch Mikrobiol 1958; 29:189–212 [View Article] [PubMed]
    [Google Scholar]
  39. Adler J. Chemotaxis in bacteria. Annu Rev Biochem 1975; 44:341–356 [View Article] [PubMed]
    [Google Scholar]
  40. Wuichet K, Alexander RP, Zhulin IB. Comparative genomic and protein sequence analyses of a complex system controlling bacterial chemotaxis. Methods Enzymol 2007; 422:1–31 [View Article] [PubMed]
    [Google Scholar]
  41. Wadhams GH, Armitage JP. Making sense of it all: bacterial chemotaxis. Nat Rev Mol Cell Biol 2004; 5:1024–1037 [View Article] [PubMed]
    [Google Scholar]
  42. Bi S, Sourjik V. Stimulus sensing and signal processing in bacterial chemotaxis. Curr Opin Microbiol 2018; 45:22–29 [View Article] [PubMed]
    [Google Scholar]
  43. Romagnoli S, Packer HL, Armitage JP. Tactic responses to oxygen in the phototrophic bacterium Rhodobacter sphaeroides WS8N. J Bacteriol 2002; 184:5590–5598 [View Article] [PubMed]
    [Google Scholar]
  44. Harrison DM, Skidmore J, Armitage JP, Maddock JR. Localization and environmental regulation of MCP-like proteins in Rhodobacter sphaeroides. Mol Microbiol 1999; 31:885–892 [View Article] [PubMed]
    [Google Scholar]
  45. Wadhams GH, Martin AC, Porter SL, Maddock JR, Mantotta JC et al. TlpC, a novel chemotaxis protein in Rhodobacter sphaeroides, localizes to a discrete region in the cytoplasm. Mol Microbiol 2002; 46:1211–1221 [View Article] [PubMed]
    [Google Scholar]
  46. Porter SL, Warren AV, Martin AC, Armitage JP. The third chemotaxis locus of Rhodobacter sphaeroides is essential for chemotaxis. Mol Microbiol 2002; 46:1081–1094 [View Article] [PubMed]
    [Google Scholar]
  47. Scott KA, Porter SL, Bagg EAL, Hamer R, Hill JL et al. Specificity of localization and phosphotransfer in the CheA proteins of Rhodobacter sphaeroides. Mol Microbiol 2010; 76:318–330 [View Article] [PubMed]
    [Google Scholar]
  48. Porter SL, Wadhams GH, Armitage JP. Rhodobacter sphaeroides: complexity in chemotactic signalling. Trends Microbiol 2008; 16:251–260 [View Article] [PubMed]
    [Google Scholar]
  49. Roberts MAJ, Wadhams GH, Hadfield KA, Tickner S, Armitage JP. ParA-like protein uses nonspecific chromosomal DNA binding to partition protein complexes. Proc Natl Acad Sci U S A 2012; 109:6698–6703 [View Article] [PubMed]
    [Google Scholar]
  50. Jones CW, Armitage JP. Essential role of the cytoplasmic chemoreceptor TlpT in the De Novo formation of chemosensory complexes in Rhodobacter sphaeroides. J Bacteriol 2017; 199:19 [View Article] [PubMed]
    [Google Scholar]
  51. Porter SL, Armitage JP. Chemotaxis in Rhodobacter sphaeroides requires an atypical histidine protein kinase. J Biol Chem 2004; 279:54573–54580 [View Article] [PubMed]
    [Google Scholar]
  52. Porter SL, Wadhams GH, Martin AC, Byles ED, Lancaster DE et al. The CheYs of Rhodobacter sphaeroides. J Biol Chem 2006; 281:32694–32704 [View Article] [PubMed]
    [Google Scholar]
  53. Porter SL, Roberts MAJ, Manning CS, Armitage JP. A bifunctional kinase-phosphatase in bacterial chemotaxis. Proc Natl Acad Sci U S A 2008; 105:18531–18536 [View Article] [PubMed]
    [Google Scholar]
  54. Tindall MJ, Porter SL, Maini PK, Armitage JP. Modeling chemotaxis reveals the role of reversed phosphotransfer and a bi-functional kinase-phosphatase. PLoS Comput Biol 2010; 6:e1000896 [View Article] [PubMed]
    [Google Scholar]
  55. Beyer J de, Szöllössi A, Byles E, Fischer R, Armitage JP. Mechanism of signalling and adaptation through the Rhodobacter sphaeroides cytoplasmic chemoreceptor cluster. Int J Mol Sci 2019; 20:20 [View Article] [PubMed]
    [Google Scholar]
  56. Khoo JH, Miller H, Armitage JP, Zhulin IB. Measurement of macromolecular crowding in Rhodobacter sphaeroides under different growth conditions. mBio 2022; 13:e0367221 [View Article] [PubMed]
    [Google Scholar]
  57. Dubarry N, Willis CR, Ball G, Lesterlin C, Armitage JP. In Vivo imaging of the segregation of the 2 chromosomes and the cell division proteins of Rhodobacter sphaeroides reveals an unexpected role for MipZ. mBio 2019; 10:e02515-18 [View Article] [PubMed]
    [Google Scholar]
  58. DePamphilis ML, Adler J. Fine structure and isolation of the hook-basal body complex of flagella from Escherichia coli and Bacillus subtilis. J Bacteriol 1971; 105:384–395 [View Article] [PubMed]
    [Google Scholar]
  59. Minamino T, Imada K, Namba K. Mechanisms of type III protein export for bacterial flagellar assembly. Mol Biosyst 2008; 4:1105–1115 [View Article] [PubMed]
    [Google Scholar]
  60. Armitage JP. The bacterial flagellum – how bacteria swim. Microbiol 2024; 170:1 [View Article] [PubMed]
    [Google Scholar]
  61. Sourjik V, Armitage JP. Spatial organization in bacterial chemotaxis. EMBO J 2010; 29:2724–2733 [View Article] [PubMed]
    [Google Scholar]
  62. Briegel A, Ladinsky MS, Oikonomou C, Jones CW, Harris MJ et al. Structure of bacterial cytoplasmic chemoreceptor arrays and implications for chemotactic signaling. eLife 2014; 3:e02151 [View Article] [PubMed]
    [Google Scholar]
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