Independent evolution of shape and motility allows evolutionary flexibility in Firmicutes bacteria


Functional morphological adaptation is an implicit assumption across many ecological studies. However, despite a few pioneering attempts to link bacterial form and function, functional morphology is largely unstudied in prokaryotes. One intriguing candidate for analysis is bacterial shape, as multiple lines of theory indicate that cell shape and motility should be strongly correlated. Here we present a large-scale use of modern phylogenetic comparative methods to explore this relationship across 325 species of the phylum Firmicutes. In contrast to clear predictions from theory, we show that cell shape and motility are not coupled, and that transitions to and from flagellar motility are common and strongly associated with lifestyle (free-living or host-associated). We find no association between shape and lifestyle, and contrary to recent evidence, no indication that shape is associated with pathogenicity. Our results suggest that the independent evolution of shape and motility in this group might allow a greater evolutionary flexibility.

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Figure 1: Phylogenetic distribution of phenotypic data and transition rate estimates.


  1. 1

    Díaz, S. et al. The global spectrum of plant form and function. Nature 529, 167–171 (2016).

    Article  PubMed  Google Scholar 

  2. 2

    Hale, M. S. & Mitchell, J. G. Functional morphology of diatom frustule microstructures: hydrodynamic control of brownian particle diffusion and advection. Aquat. Microb. Ecol. 24, 287–295 (2001).

    Article  Google Scholar 

  3. 3

    Wainwright, P. C. Functional versus morphological diversity in macroevolution. Annu. Rev. Ecol. Evol. Syst. 38, 381–401 (2007).

    Article  Google Scholar 

  4. 4

    Martiny, J. B. H., Jones, S. E., Lennon, J. T. & Martiny, A. C. Microbiomes in light of traits: a phylogenetic perspective. Science 350, aac9323 (2015).

    Article  PubMed  Google Scholar 

  5. 5

    Dusenbery, D. B. Living at Micro Scale: The Unexpected Physics of Being Small (Harvard Univ. Press, 2009).

    Google Scholar 

  6. 6

    Persat, A., Stone, H. A. & Gitai, Z. The curved shape of Caulobacter–crescentus enhances surface colonization in flow. Nat. Commun. 5, 3824 (2014).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. 7

    Young, K. D. The selective value of bacterial shape. Microbiol. Mol. Biol. Rev. 70, 660–703 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  8. 8

    Young, K. D. Bacterial morphology: why have different shapes? Curr. Opin. Microbiol. 10, 596–600 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  9. 9

    Mitchell, J. G. The energetics and scaling of search strategies in bacteria. Am. Nat. 160, 727–740 (2002).

    Article  PubMed  Google Scholar 

  10. 10

    Cooper, S. & Denny, M. W. A conjecture on the relationship of bacterial shape to motility in rod-shaped bacteria. FEMS Microbiol. Lett. 148, 227–231 (1997).

    CAS  Article  Google Scholar 

  11. 11

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

    CAS  PubMed  PubMed Central  Google Scholar 

  12. 12

    Ramos, H. C., Rumbo, M. & Sirard, J. C. Bacterial flagellins: mediators of pathogenicity and host immune responses in mucosa. Trends Microbiol. 12, 509–517 (2004).

    CAS  Article  PubMed  Google Scholar 

  13. 13

    Cullender, T. C. et al. Innate and adaptive immunity interact to quench microbiome flagellar motility in the gut. Cell Host Microbe 14, 571–581 (2013).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. 14

    Lovewell, R. R. et al. Step-wise loss of bacterial flagellar torsion confers progressive phagocytic evasion. PLoS Pathog. 7, (2011).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. 15

    Patankar, Y. R. et al. Flagellar motility is a key determinant of the magnitude of the inflammasome response to Pseudomonas aeruginosa. Infect. Immun. 81, 2043–2052 (2013).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. 16

    Chaban, B., Hughes, H. V. & Beeby, M. The flagellum in bacterial pathogens: for motility and a whole lot more. Semin. Cell Dev. Biol. 46, 91–103 (2015).

    CAS  Article  PubMed  Google Scholar 

  17. 17

    Dalia, A. B. & Weiser, J. N. Minimization of bacterial size allows for complement evasion and is overcome by the agglutinating effect of antibody. Cell Host Microbe 10, 486–496 (2011).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. 18

    Frirdich, E. & Gaynor, E. C. Peptidoglycan hydrolases, bacterial shape, and pathogenesis. Curr. Opin. Microbiol. 16, 767–778 (2013).

    CAS  Article  PubMed  Google Scholar 

  19. 19

    Sycuro, L. K. et al. Multiple peptidoglycan modification networks modulate Helicobacter–pylori’s cell shape, motility, and colonization potential. PLoS Pathog. 8, e1002603 (2012).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. 20

    Champion, J. A. & Mitragotri, S . Role of target geometry in phagocytosis. Proc. Natl Acad. Sci. USA 103, 4930–4934 (2006).

    CAS  Article  PubMed  Google Scholar 

  21. 21

    Doshi, N. & Mitragotri, S. Macrophages recognize size and shape of their targets. PLoS ONE 5, e10051 (2010).

  22. 22

    Veyrier, F. J. et al. Common cell shape evolution of two nasopharyngeal pathogens. PLoS Genet. 11, e1005338 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  23. 23

    Stackebrandt, E. & Woese, C. R. A phylogenetic dissection of the family micrococcaceae. Curr. Microbiol. 2, 317–322 (1979).

    CAS  Article  Google Scholar 

  24. 24

    Siefert, J. L. & Fox, G. E. Phylogenetic mapping of bacterial morphology. Microbiology 144, 2803–2808 (1998).

    CAS  Article  PubMed  Google Scholar 

  25. 25

    Tamames, J., González-Moreno, M., Mingorance, J., Valencia, A. & Vicente, M . Bringing gene order into bacterial shape. Trends Genet. 17, 124–126 (2001).

    CAS  Article  PubMed  Google Scholar 

  26. 26

    Ley, R., Turnbaugh, P., Klein, S. & Gordon, J. Microbial ecology: human gut microbes associated with obesity. Nature 444, 1022–1023 (2006).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. 27

    Wrighton, K. C. et al. A novel ecological role of the Firmicutes identified in thermophilic microbial fuel cells. ISME J. 2, 1146–1156 (2008).

    CAS  Article  PubMed  Google Scholar 

  28. 28

    Sharmin, F., Wakelin, S., Huygens, F. & Hargreaves, M. Firmicutes dominate the bacterial taxa within sugar-cane processing plants. Sci. Rep. 3, 3107 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  29. 29

    Hadfield, J. D. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1–22 (2010).

    Article  Google Scholar 

  30. 30

    Maddison, W. P. & FitzJohn, R. G. The unsolved challenge to phylogenetic correlation tests for categorical characters. Syst. Biol. 64, 127–136 (2015).

    Article  PubMed  Google Scholar 

  31. 31

    Pagel, M. Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proc. R. Soc. Lond. B 255, 37–45 (1994).

    Article  Google Scholar 

  32. 32

    Taylor, T. B. et al. Evolutionary resurrection of flagellar motility via rewiring of the nitrogen regulation system. Science 347, 1014–1017 (2015).

    CAS  Article  PubMed  Google Scholar 

  33. 33

    Chiara, M. et al. Comparative genomics of Listeria sensu lato: genus-wide differences in evolutionary dynamics and the progressive gain of complex, potentially pathogenicity-related traits through lateral gene transfer. Genome Biol. Evol. 7, 2154–2172 (2015).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. 34

    Cousin, F. J. et al. Detection and genomic characterization of motility in Lactobacillus curvatus: confirmation of motility in a species outside the Lactobacillus salivarius clade. Appl. Environ. Microbiol. 81, 1297–1308 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  35. 35

    Palmer, K. L., Schaik, W. Van, Willems, R. J. L. & Gilmore, M. S. in Enterococci: From Commensals to Leading Causes of Drug Resistant Infection (eds Gilmore, M. S. et al.) (2014);

  36. 36

    Mendes-Soares, H., Suzuki, H., Hickey, R. J. & Forneya, L. J. Comparative functional genomics of Lactobacillus spp. reveals possible mechanisms for specialization of vaginal lactobacilli to their environment. J. Bacteriol. 196, 1458–1470 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  37. 37

    Poggio, S. et al. A complete set of flagellar genes acquired by horizontal transfer coexists with the endogenous flagellar system in Rhodobacter sphaeroides. J. Bacteriol. 189, 3208–3216 (2007).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  38. 38

    Shah, N. et al. Reductive evolution and the loss of PDC/PAS domains from the genus Staphylococcus. BMC Genomics 14, 524 (2013).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. 39

    Koch, A. L. Were Gram-positive rods the first bacteria? Trends Microbiol. 11, 166–170 (2003).

    CAS  Article  PubMed  Google Scholar 

  40. 40

    Errington, J. L-form bacteria, cell walls and the origins of life. Open Biol. 3, 120143 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  41. 41

    Martiny, A. C., Treseder, K. & Pusch, G. Phylogenetic conservatism of functional traits in microorganisms. ISME J. 7, 830–838 (2013).

    CAS  Article  PubMed  Google Scholar 

  42. 42

    Li, L. et al. Leaf economics and hydraulic traits are decoupled in five species-rich tropical-subtropical forests. Ecol. Lett. 18, 899–906 (2015).

    CAS  Article  PubMed  Google Scholar 

  43. 43

    Pagel, M. in Phylogenetics and Ecology (eds Eggleton, P. & Richard, V.-W. ) 29–51 (Linnean Society Symposium Series, 1994).

    Google Scholar 

  44. 44

    Chang, F. & Huang, K. C. How and why cells grow as rods. BMC Biol. 12, 54 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  45. 45

    Jiang, C., Caccamo, P. D. & Brun, Y. V. Mechanisms of bacterial morphogenesis: Evolutionary cell biology approaches provide new insights. BioEssays 37, 413–425 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  46. 46

    Randich, A. M. & Brun, Y. V. Molecular mechanisms for the evolution of bacterial morphologies and growth modes. Front. Microbiol. 6, 580 (2015).

  47. 47

    Dworkin, J. Form equals function? Bacterial shape and its consequences for pathogenesis. Mol. Microbiol. 78, 792–795 (2010).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  48. 48

    Bonner, J. T. Randomness in Evolution (Princeton Univ. Press, 2013).

    Google Scholar 

  49. 49

    Chai, J., Kora, G., Ahn, T.-H., Hyatt, D. & Pan, C. Functional phylogenomics analysis of bacteria and archaea using consistent genome annotation with UniFam. BMC Evol. Biol. 14, 1–13 (2014).

    Article  Google Scholar 

  50. 50

    Vos, P. et al. Bergey’s Manual of Systematic Bacteriology Vol. 3 (Springer, 2009).

    Google Scholar 

  51. 51

    Pagel, M., Meade, A. & Barker, D. Bayesian estimation of ancestral character states on phylogenies. Syst. Biol. 53, 673–684 (2004).

    Article  PubMed  Google Scholar 

  52. 52

    de Villemereuil, P., Gimenez, O. & Doligez, B. Comparing parent–offspring regression with frequentist and Bayesian animal models to estimate heritability in wild populations: a simulation study for Gaussian and binary traits. Methods Ecol. Evol. 4, 260–275 (2013).

    Article  Google Scholar 

  53. 53

    Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Stat. Methodol. 57, 289–300 (1995).

    Google Scholar 

  54. 54

    Pagel, M. Inferring the historical patterns of biological evolution. Nature 401, 877–884 (1999).

    CAS  Article  PubMed  Google Scholar 

  55. 55

    Hadfield, J. D. & Nakagawa, S. General quantitative genetic methods for comparative biology: phylogenies, taxonomies and multi-trait models for continuous and categorical characters. J. Evol. Biol. 23, 494–508 (2010).

    CAS  Article  PubMed  Google Scholar 

  56. 56

    Kass, R. E. & Raftery, A. E. Bayes Factors. J. Am. Stat. Assoc. 90, 773–795 (1995).

    Article  Google Scholar 

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We thank M. Pagel, O. Guadayol Roig, R. Schuech, J. Baker and A. Meade for helpful comments and advice. This work is financially supported by The Leverhulme Trust project RLA RL-2012-022, ‘Form and function in a microbial world’, granted to S.H. C.V. was supported by a Leverhulme Trust Research Project Grant (RPG-2013-185).

Author information




S.H., C.V. and F.E.B. designed the study; F.E.B. and S.H. developed the protocol for the data collection; F.E.B. collected the data and F.E.B., C.V. and S.H. analysed the data; F.E.B. wrote the first draft of the manuscript, and all authors contributed substantially to revisions.

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Correspondence to Fouad El Baidouri.

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The authors declare no competing financial interests.

Supplementary information

Supplementary information

Supplementary Figures 1–6; Supplementary Tables 1–3. (PDF 936 kb)

Supplementary phylogenetic tree

Phylogenetic tree of 325 Firmicutes species in Newick format. (TXT 17 kb)

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El Baidouri, F., Venditti, C. & Humphries, S. Independent evolution of shape and motility allows evolutionary flexibility in Firmicutes bacteria. Nat Ecol Evol 1, 0009 (2017).

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