Science and Society | Published:

From The Origin of Species to the origin of bacterial flagella

Nature Reviews Microbiologyvolume 4pages784790 (2006) | Download Citation



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.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.


  1. 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).

  2. 2

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

  3. 3

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

  4. 4

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

  5. 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).

  6. 6

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

  7. 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).

  8. 8

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

  9. 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).

  10. 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).

  11. 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).

  12. 12

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

  13. 13

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

  14. 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).

  15. 15

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

  16. 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).

  17. 17

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

  18. 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).

  19. 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).

  20. 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).

  21. 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).

  22. 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).

  23. 23

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

  24. 24

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

  25. 25

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

  26. 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).

  27. 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).

  28. 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).

  29. 29

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

  30. 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).

  31. 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).

  32. 32

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

  33. 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).

  34. 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).

  35. 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).

  36. 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).

  37. 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).

  38. 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).

  39. 39

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

  40. 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).

  41. 41

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

  42. 42

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

  43. 43

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

  44. 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).

  45. 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).

  46. 46

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

  47. 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).

  48. 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).

  49. 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).

  50. 50

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

  51. 51

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

  52. 52

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

  53. 53

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

  54. 54

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

  55. 55

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

  56. 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).

  57. 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).

  58. 58

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

  59. 59

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

  60. 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).

  61. 61

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

  62. 62

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

  63. 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).

  64. 64

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

  65. 65

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

  66. 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).

  67. 67

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

  68. 68

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

  69. 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).

  70. 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).

  71. 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).

  72. 72

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

  73. 73

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

  74. 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).

  75. 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).

  76. 76

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

  77. 77

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

  78. 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).

  79. 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).

  80. 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).

Download references


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

Author information


  1. Division of Immunity & Infection, Medical School, University of Birmingham, Birmingham, B15 2TT, UK

    • Mark J. Pallen
  2. National Center for Science Education, Oakland, 94609?2509, California, USA

    • Nicholas J. Matzke


  1. Search for Mark J. Pallen in:

  2. Search for Nicholas J. Matzke in:

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.

Corresponding author

Correspondence to Mark J. Pallen.

Related links


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.


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


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.

About this article

Publication history


Issue Date


Further reading