Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Science and Society
  • Published:

From The Origin of Species to the origin of bacterial flagella

Abstract

In the recent Dover trial, and elsewhere, the 'Intelligent Design' movement has championed the bacterial flagellum as an irreducibly complex system that, it is claimed, could not have evolved through natural selection. Here we explore the arguments in favour of viewing bacterial flagella as evolved, rather than designed, entities. We dismiss the need for any great conceptual leaps in creating a model of flagellar evolution and speculate as to how an experimental programme focused on this topic might look.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

References

  1. Musgrave, I. in Why Intelligent Design Fails: a Scientific Critique of the New Creationism (eds Young, M. & Edis, T.) 72?84 (Rutgers University Press, Piscataway USA, 2004).

    Google Scholar 

  2. Miller, K. R. in Debating Design: from Darwin to DNA (eds Dembski, W. & Ruse, M.) 81?97 (Cambridge University Press, New York, 2004).

    Google Scholar 

  3. Mayr, E. Darwin's influence on modern thought. Sci. Am. 283, 78?83 (2000).

    CAS  Google Scholar 

  4. Kubori, T. et al. Purification and characterization of the flagellar hook-basal body complex of Bacillus subtilis. Mol. Microbiol. 24, 399?410 (1997).

    CAS  Google Scholar 

  5. Li, C., Motaleb, A., Sal, M., Goldstein, S. F. & Charon, N. W. Spirochete periplasmic flagella and motility. J. Mol. Microbiol. Biotechnol. 2, 345?354 (2000).

    CAS  Google Scholar 

  6. McCarter, L. L. Dual flagellar systems enable motility under different circumstances. J. Mol. Microbiol. Biotechnol. 7, 18?29 (2004).

    CAS  Google Scholar 

  7. Kita-Tsukamoto, K., Wada, M., Yao, K., Nishino, T. & Kogure, K. Flagellar motors of marine bacteria Halomonas are driven by both protons and sodium ions. Can. J. Microbiol. 50, 369?374 (2004).

    CAS  Google Scholar 

  8. Armitage, J. P. & Macnab, R. M. Unidirectional, intermittent rotation of the flagellum of Rhodobacter sphaeroides. J. Bacteriol. 169, 514?518 (1987).

    CAS  PubMed Central  Google Scholar 

  9. Attmannspacher, U., Scharf, B. & Schmitt, R. Control of speed modulation (chemokinesis) in the unidirectional rotary motor of Sinorhizobium meliloti. Mol. Microbiol. 56, 708?718 (2005).

    CAS  Google Scholar 

  10. Shibata, S., Alam, M. & Aizawa, S. Flagellar filaments of the deep-sea bacteria Idiomarina ioihiensis belong to a family different from those of Salmonella typhimurium. J. Mol. Biol. 352, 510?516 (2005).

    CAS  Google Scholar 

  11. Burnens, A. P. et al. The flagellin N-methylase gene fliB and an adjacent serovar-specific IS200 element in Salmonella typhimurium. Microbiology 143, 1539?1547 (1997).

    CAS  Google Scholar 

  12. Logan, S. M. Flagellar glycosylation ? a new component of the motility repertoire? Microbiology 152, 1249?1262 (2006).

    CAS  Google Scholar 

  13. Read, T. D. et al. Genome sequences of Chlamydia trachomatis MoPn and Chlamydia pneumoniae AR39. Nucleic Acids Res. 28, 1397?1406 (2000).

    CAS  PubMed Central  Google Scholar 

  14. Darwin, C. The Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life (John Murray, London, 1859).

    Google Scholar 

  15. Beatson, S. A., Minamino, T. & Pallen, M. J. Variation in bacterial flagellins: from sequence to structure. Trends Microbiol. 14, 151?155 (2006).

    CAS  Google Scholar 

  16. Ely, B., Ely, T. W., Crymes, W. B. Jr & Minnich, S. A. A family of six flagellin genes contributes to the Caulobacter crescentus flagellar filament. J. Bacteriol. 182, 5001?5004 (2000).

    CAS  PubMed Central  Google Scholar 

  17. Venter, J. C. et al. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304, 66?74 (2004).

    CAS  Google Scholar 

  18. Halling, S. M. On the presence and organization of open reading frames of the nonmotile pathogen Brucella abortus similar to class II, III, and IV flagellar genes and to LcrD virulence superfamily. Microb. Comp. Genomics 3, 21?29 (1998).

    CAS  Google Scholar 

  19. Al Mamun, A. A., Tominaga, A. & Enomoto, M. Cloning and characterization of the region III flagellar operons of the four Shigella subgroups: genetic defects that cause loss of flagella of Shigella boydii and Shigella sonnei. J. Bacteriol. 179, 4493?4500 (1997).

    CAS  PubMed Central  Google Scholar 

  20. Monday, S. R., Minnich, S. A. & Feng, P. C. A 12-base-pair deletion in the flagellar master control gene flhC causes nonmotility of the pathogenic German sorbitol-fermenting Escherichia coli O157:H- strains. J. Bacteriol. 186, 2319?2327 (2004).

    CAS  PubMed Central  Google Scholar 

  21. Ren, C. P., Beatson, S. A., Parkhill, J. & Pallen, M. J. The Flag-2 locus, an ancestral gene cluster, is potentially associated with a novel flagellar system from Escherichia coli. J. Bacteriol. 187, 1430?1440 (2005).

    CAS  PubMed Central  Google Scholar 

  22. Fretin, D. et al. The sheathed flagellum of Brucella melitensis is involved in persistence in a murine model of infection. Cell. Microbiol. 7, 687?698 (2005).

    CAS  Google Scholar 

  23. Webber, C. & Ponting, C. P. Genes and homology. Curr. Biol. 14, R332?R333 (2004).

    CAS  Google Scholar 

  24. Quevillon, E. et al. InterProScan: protein domains identifier. Nucleic Acids Res. 33, W116?W120 (2005).

    CAS  PubMed Central  Google Scholar 

  25. Pallen, M. J., Penn, C. W. & Chaudhuri, R. R. Bacterial flagellar diversity in the post-genomic era. Trends Microbiol. 13, 143?149 (2005).

    CAS  Google Scholar 

  26. Agrain, C. et al. Characterization of a Type III secretion substrate specificity switch (T3S4) domain in YscP from Yersinia enterocolitica. Mol. Microbiol. 56, 54?67 (2005).

    CAS  Google Scholar 

  27. Ohnishi, K., Kutsukake, K., Suzuki, H. & Iino, T. Gene fliA encodes an alternative σ factor specific for flagellar operons in Salmonella typhimurium. Mol. Gen. Genet. 221, 139?147 (1990).

    CAS  Google Scholar 

  28. Sorenson, M. K., Ray, S. S. & Darst, S. A. Crystal structure of the flagellar σ/anti-σ complex σ28/FlgM reveals an intact σ factor in an inactive conformation. Mol. Cell 14, 127?138 (2004).

    CAS  Google Scholar 

  29. Iyer, L. M. & Aravind, L. The emergence of catalytic and structural diversity within the β-clip fold. Proteins 55, 977?991 (2004).

    CAS  Google Scholar 

  30. Nambu, T., Minamino, T., Macnab, R. M. & Kutsukake, K. Peptidoglycan-hydrolyzing activity of the FlgJ protein, essential for flagellar rod formation in Salmonella typhimurium. J. Bacteriol. 181, 1555?1561 (1999).

    CAS  PubMed Central  Google Scholar 

  31. Zhai, Y. F., Heijne, W. & Saier, M. H. Jr. Molecular modeling of the bacterial outer membrane receptor energizer, ExbBD/TonB, based on homology with the flagellar motor, MotAB. Biochim. Biophys. Acta 1614, 201?210 (2003).

    CAS  Google Scholar 

  32. Szurmant, H. & Ordal, G. W. Diversity in chemotaxis mechanisms among the bacteria and archaea. Microbiol. Mol. Biol. Rev. 68, 301?319 (2004).

    CAS  PubMed Central  Google Scholar 

  33. Faguy, D. M. & Jarrell, K. F. A twisted tale: the origin and evolution of motility and chemotaxis in prokaryotes. Microbiology 145, 279?281 (1999).

    Google Scholar 

  34. Nguyen, L., Paulsen, I. T., Tchieu, J., Hueck, C. J. & Saier, M. H. Jr. Phylogenetic analyses of the constituents of Type III protein secretion systems. J. Mol. Microbiol. Biotechnol. 2, 125?144 (2000).

    CAS  Google Scholar 

  35. Pallen, M. J., Beatson, S. A. & Bailey, C. M. Bioinformatics, genomics and evolution of non-flagellar type-III secretion systems: a Darwinian perspective. FEMS Microbiol. Rev. 29, 201?229 (2005).

    CAS  Google Scholar 

  36. Gophna, U., Ron, E. Z. & Graur, D. Bacterial type III secretion systems are ancient and evolved by multiple horizontal-transfer events. Gene 312, 151?163 (2003).

    CAS  Google Scholar 

  37. Vogler, A. P., Homma, M., Irikura, V. M. & Macnab, R. M. Salmonella typhimurium mutants defective in flagellar filament regrowth and sequence similarity of FliI to F0F1, vacuolar, and archaebacterial ATPase subunits. J. Bacteriol. 173, 3564?3572 (1991).

    CAS  PubMed Central  Google Scholar 

  38. Pallen, M. J., Bailey, C. M. & Beatson, S. A. Evolutionary links between FliH/YscL-like proteins from bacterial type III secretion systems and second-stalk components of the F0F1 and vacuolar ATPases. Protein Sci. 15, 935?941 (2006).

    CAS  PubMed Central  Google Scholar 

  39. Woolfson, D. N. The design of coiled-coil structures and assemblies. Adv. Protein Chem. 70, 79?112 (2005).

    CAS  Google Scholar 

  40. Wagner, D. E. et al. Toward the development of peptide nanofilaments and nanoropes as smart materials. Proc. Natl Acad. Sci. USA 102, 12656?12661 (2005).

    CAS  Google Scholar 

  41. Fernandez, L. A. & Berenguer, J. Secretion and assembly of regular surface structures in Gram-negative bacteria. FEMS Microbiol. Rev. 24, 21?44 (2000).

    CAS  Google Scholar 

  42. Ton-That, H. & Schneewind, O. Assembly of pili in Gram-positive bacteria. Trends Microbiol. 12, 228?234 (2004).

    CAS  Google Scholar 

  43. Bardy, S. L., Ng, S. Y. & Jarrell, K. F. Prokaryotic motility structures. Microbiology 149, 295?304 (2003).

    CAS  Google Scholar 

  44. Knutton, S. et al. A novel EspA-associated surface organelle of enteropathogenic Escherichia coli involved in protein translocation into epithelial cells. EMBO J. 17, 2166?2176 (1998).

    CAS  PubMed Central  Google Scholar 

  45. Delahay, R. M. et al. The coiled-coil domain of EspA is essential for the assembly of the type III secretion translocon on the surface of enteropathogenic Escherichia coli. J. Biol. Chem. 274, 35969?35974 (1999).

    CAS  Google Scholar 

  46. Daniell, S. J. et al. 3D structure of EspA filaments from enteropathogenic Escherichia coli. Mol. Microbiol. 49, 301?308 (2003).

    CAS  Google Scholar 

  47. Crepin, V. F., Shaw, R., Abe, C. M., Knutton, S. & Frankel, G. Polarity of enteropathogenic Escherichia coli EspA filament assembly and protein secretion. J. Bacteriol. 187, 2881?2889 (2005).

    CAS  PubMed Central  Google Scholar 

  48. Yip, C. K., Finlay, B. B. & Strynadka, N. C. Structural characterization of a type III secretion system filament protein in complex with its chaperone. Nature Struct. Mol. Biol. 12, 75?81 (2005).

    CAS  Google Scholar 

  49. Kim, J. F. Revisiting the chlamydial type III protein secretion system: clues to the origin of type III protein secretion. Trends Genet. 17, 65?69 (2001).

    CAS  Google Scholar 

  50. Gould, S. J. & Vrba, E. S. Exaptation ? a missing term in the science of form. Paleobiology 8, 4?15 (1982).

    Google Scholar 

  51. Regal, P. J. The evolutionary origin of feathers. Q. Rev. Biol. 50, 35?66 (1975).

    CAS  Google Scholar 

  52. Norell, M. et al. Palaeontology: 'modern' feathers on a non-avian dinosaur. Nature 416, 36?37 (2002).

    CAS  Google Scholar 

  53. Dobzhansky, T. Nothing in biology makes sense except in the light of evolution. Am. Biol. Teach. 35, 125?129 (1973).

    Google Scholar 

  54. Macnab, R. M. Type III flagellar protein export and flagellar assembly. Biochim. Biophys. Acta 1694, 207?217 (2004).

    CAS  Google Scholar 

  55. Minamino, T. & Namba, K. Self-assembly and type III protein export of the bacterial flagellum. J. Mol. Microbiol. Biotechnol. 7, 5?17 (2004).

    CAS  Google Scholar 

  56. Suzuki, H., Yonekura, K. & Namba, K. Structure of the rotor of the bacterial flagellar motor revealed by electron cryomicroscopy and single-particle image analysis. J. Mol. Biol. 337, 105?113 (2004).

    CAS  Google Scholar 

  57. Saijo-Hamano, Y., Minamino, T., Macnab, R. M. & Namba, K. Structural and functional analysis of the C-terminal cytoplasmic domain of FlhA, an integral membrane component of the type III flagellar protein export apparatus in Salmonella. J. Mol. Biol. 343, 457?466 (2004).

    CAS  Google Scholar 

  58. Samatey, F. A. et al. Structure of the bacterial flagellar protofilament and implications for a switch for supercoiling. Nature 410, 331?337 (2001).

    CAS  Google Scholar 

  59. Yonekura, K., Maki-Yonekura, S. & Namba, K. Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature 424, 643?650 (2003).

    CAS  Google Scholar 

  60. Journet, L., Hughes, K. T. & Cornelis, G. R. Type III secretion: a secretory pathway serving both motility and virulence. Mol. Membr. Biol. 22, 41?50 (2005).

    CAS  Google Scholar 

  61. Aldridge, P. & Hughes, K. T. Regulation of flagellar assembly. Curr. Opin. Microbiol. 5, 160?165 (2002).

    CAS  Google Scholar 

  62. Sowa, Y. et al. Direct observation of steps in rotation of the bacterial flagellar motor. Nature 437, 916?919 (2005).

    CAS  Google Scholar 

  63. Brown, P. N., Hill, C. P. & Blair, D. F. Crystal structure of the middle and C-terminal domains of the flagellar rotor protein FliG. EMBO J. 21, 3225?3234 (2002).

    CAS  PubMed Central  Google Scholar 

  64. Blair, D. F. Flagellar movement driven by proton translocation. FEBS Lett. 545, 86?95 (2003).

    CAS  Google Scholar 

  65. McCarter, L. L. Regulation of flagella. Curr. Opin. Microbiol. 9, 180?186 (2006).

    CAS  Google Scholar 

  66. Rabus, R. et al. The genome of Desulfotalea psychrophila, a sulfate-reducing bacterium from permanently cold Arctic sediments. Environ. Microbiol. 6, 887?902 (2004).

    CAS  Google Scholar 

  67. Medina, M. Genomes, phylogeny, and evolutionary systems biology. Proc. Natl Acad. Sci. USA 102, (Suppl. 1) 6630?6635 (2005).

    CAS  Google Scholar 

  68. Wilkins, A. S. 'Intelligent design' as both problem and symptom. Bioessays 28, 327?329 (2006).

    Google Scholar 

  69. Field, S. F., Bulina, M. Y., Kelmanson, I. V., Bielawski, J. P. & Matz, M. V. Adaptive evolution of multicolored fluorescent proteins in reef-building corals. J. Mol. Evol. 62, 332?339 (2006).

    CAS  Google Scholar 

  70. Chang, B. S., Ugalde, J. A. & Matz, M. V. Applications of ancestral protein reconstruction in understanding protein function: GFP-like proteins. Methods Enzymol 395, 652?670 (2005).

    CAS  Google Scholar 

  71. Wouters, M. A., Liu, K., Riek, P. & Husain, A. A despecialization step underlying evolution of a family of serine proteases. Mol. Cell 12, 343?354 (2003).

    CAS  Google Scholar 

  72. Ugalde, J. A., Chang, B. S. & Matz, M. V. Evolution of coral pigments recreated. Science 305, 1433 (2004).

    CAS  Google Scholar 

  73. Chang, B. S. & Donoghue, M. J. Recreating ancestral proteins. Trends Ecol. Evol. 15, 109?114 (2000).

    CAS  Google Scholar 

  74. Chang, B. S., Kazmi, M. A. & Sakmar, T. P. Synthetic gene technology: applications to ancestral gene reconstruction and structure-function studies of receptors. Meth. Enzymol. 343, 274?294 (2002).

    Google Scholar 

  75. Chang, B. S., Jonsson, K., Kazmi, M. A., Donoghue, M. J. & Sakmar, T. P. Recreating a functional ancestral archosaur visual pigment. Mol. Biol. Evol. 19, 1483?1489 (2002).

    CAS  Google Scholar 

  76. Dusenbery, D. B. Fitness landscapes for effects of shape on chemotaxis and other behaviors of bacteria. J. Bacteriol. 180, 5978?5983 (1998).

    CAS  PubMed Central  Google Scholar 

  77. Dusenbery, D. B. Minimum size limit for useful locomotion by free-swimming microbes. Proc. Natl Acad. Sci. USA 94, 10949?10954 (1997).

    CAS  Google Scholar 

  78. Pallen, M. J., Beatson, S. A. & Bailey, C. M. Bioinformatics analysis of the locus for enterocyte effacement provides novel insights into type-III secretion. BMC Microbiol. 5, 9 (2005).

    PubMed Central  Google Scholar 

  79. Minamino, T., Gonzalez-Pedrajo, B., Kihara, M., Namba, K. & Macnab, R. M. The ATPase FliI can interact with the type III flagellar protein export apparatus in the absence of its regulator, FliH. J. Bacteriol. 185, 3983?3988 (2003).

    CAS  PubMed Central  Google Scholar 

  80. Raha, M., Sockett, H. & Macnab, R. M. Characterization of the fliL gene in the flagellar regulon of Escherichia coli and Salmonella typhimurium. J. Bacteriol. 176, 2308?2311 (1994).

    CAS  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank D. Blair, P. Aldridge and R. Berry for critical comments on this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mark J. Pallen.

Ethics declarations

Competing interests

Nicholas J. Matzke is employed by the National Center for Science Education, a not-for-profit organization that defends the teaching of evolution in public schools.

Related links

Related links

DATABASES

Entrez Genome Project

Aquifex aeolicus

Brucella melitensis

Chromobacterium violaceum

Desulfotalea psychrophila

Edwardsiella ictaluri

Escherichia coli

Myxococcus xanthus

Rhodobacter sphaeroides

Salmonella enterica serovar Typhimurium

Shewanella baltica

Sinorhizobium meliloti

Sodalis glossinidius

Vibrio parahaemolyticus

Yersinia bercovieri

Yersinia frederiksenii

FURTHER INFORMATION

Mark Pallen's homepage

Evolution in (Brownian) space: a model for the origin of the bacterial flagellum

Kitzmiller versus Dover trial information

Ken Miller's 'the flagellum unspun'

Nanotechnology Researchers Network Center of Japan

The Minnich and Miller expert witness reports

The Minnich and Miller expert witness reports

Talk Reason

The Pandas Thumb

The Talk. Origins Archive

Glossary

β-clip domain

A fold found in a diverse group of protein domains typified by the presence of two characteristic waist-like constrictions, flanking a central extended region. The flagellar P-ring protein FlgA and type IV pilus assembly protein CpaB are two examples of β-clip-domain-containing proteins.

Chemotaxis

A behavioural response by bacteria whereby a bacterial cell senses a chemical gradient and moves towards or away from the chemical stimulus.

Essentialism

Also referred to as typology. The idea that a specific kind of entity can be defined by an invariant essence. A triangle illustrates essentialism: all triangles have the same fundamental characteristics and are sharply delimited against quadrangles or any other geometric figures. An intermediate between a triangle and a quadrangle is inconceivable. Typological thinking is however unable to accommodate the profligate variation that occurs in biology.

Establishment clause

A clause from the First Amendment to the American Constitution that states that: 'Congress shall make no law respecting an establishment of religion'. This is now interpreted to forbid any state funding of religious education in the United States.

Intelligent design

(ID). The concept that some aspects of the natural universe are better explained by an intelligent cause rather than by an undirected process such as natural selection.

Irreducible complexity

The notion that some biological systems are so complex that they could not function if they were any simpler, and so could not have been formed by successive additions to a precursor system with the same functionality.

Occam's razor

The principle that the explanation of any phenomenon should make as few assumptions as possible.

Proton-motive force

Storage of energy as a combination of a proton and voltage gradient across the bacterial inner membrane. The proton-motive force is exploited by the membrane-associated F-type ATPase to generate ATP, and by the flagellar motor to generate torque. In some bacteria, an analogous sodium-motive force drives flagellar rotation.

SpoA domain

A β-sheet domain found at the C terminus of flagellar proteins FliM and FliN and non-flagellar T3SS proteins such as YscQ and HrcQb.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pallen, M., Matzke, N. From The Origin of Species to the origin of bacterial flagella. Nat Rev Microbiol 4, 784–790 (2006). https://doi.org/10.1038/nrmicro1493

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro1493

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing