Letter | Published:

Sequential evolution of bacterial morphology by co-option of a developmental regulator

Nature volume 506, pages 489493 (27 February 2014) | Download Citation

This article has been updated

Abstract

What mechanisms underlie the transitions responsible for the diverse shapes observed in the living world? Although bacteria exhibit a myriad of morphologies1, the mechanisms responsible for the evolution of bacterial cell shape are not understood. We investigated morphological diversity in a group of bacteria that synthesize an appendage-like extension of the cell envelope called the stalk2,3. The location and number of stalks varies among species, as exemplified by three distinct subcellular positions of stalks within a rod-shaped cell body: polar in the genus Caulobacter and subpolar or bilateral in the genus Asticcacaulis4. Here we show that a developmental regulator of Caulobacter crescentus, SpmX5, is co-opted in the genus Asticcacaulis to specify stalk synthesis either at the subpolar or bilateral positions. We also show that stepwise evolution of a specific region of SpmX led to the gain of a new function and localization of this protein, which drove the sequential transition in stalk positioning. Our results indicate that changes in protein function, co-option and modularity are key elements in the evolution of bacterial morphology. Therefore, similar evolutionary principles of morphological transitions apply to both single-celled prokaryotes and multicellular eukaryotes.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Change history

  • 26 February 2014

    A minor change was made to the Figure 3 legend.

Accessions

Data deposits

Genomic data of strains sequenced in this study are deposited in GenBank/EMBL/DDBJ under accession numbers AWGD00000000 (Asticcacaulis sp. AC460), AWGE00000000 (Asticcacaulis sp. AC466), AWGC00000000 (Asticcacaulis sp. AC402), AWGF00000000 (Asticcacaulis sp. YBE204) and AWGB00000000 (Asticcacaulis benevestitus DSM16100).

References

  1. 1.

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

  2. 2.

    & Out on a limb: how the Caulobacter stalk can boost the study of bacterial cell shape. Mol. Microbiol. 64, 28–33 (2007)

  3. 3.

    & The fine structure of stalked bacteria belonging to the family Caulobacteraceae. J. Cell Biol. 23, 587–607 (1964)

  4. 4.

    & The fine structure of two unusual stalked bacteria. J. Cell Biol. 27, 133–150 (1965)

  5. 5.

    , & The dynamic interplay between a cell fate determinant and a lysozyme homolog drives the asymmetric division cycle of Caulobacter crescentus. Genes Dev. 22, 212–225 (2008)

  6. 6.

    Biological properties and classification of the Caulobacter group. Bacteriol. Rev. 28, 231–295 (1964)

  7. 7.

    , , , & Regulation of stalk elongation by phosphate in Caulobacter crescentus. J. Bacteriol. 182, 337–347 (2000)

  8. 8.

    , , , & A nutrient uptake role for bacterial cell envelope extensions. Proc. Natl Acad. Sci. USA 103, 11772–11777 (2006)

  9. 9.

    et al. General protein diffusion barriers create compartments within bacterial cells. Cell 151, 1270–1282 (2012)

  10. 10.

    et al. Protein localization and dynamics within a bacterial organelle. Proc. Natl Acad. Sci. USA 107, 5599–5604 (2010)

  11. 11.

    , , & Complex regulatory pathways coordinate cell-cycle progression and development in Caulobacter crescentus. Adv. Microb. Physiol. 54, 1–101 (2009)

  12. 12.

    & The development of cellular stalks in bacteria. J. Cell Biol. 28, 423–436 (1966)

  13. 13.

    et al. In situ probing of newly synthesized peptidoglycan in live bacteria with fluorescent d-amino acids. Angew. Chem. Int. Edn Engl. 51, 12519–12523 (2012)

  14. 14.

    et al. The tubulin homologue FtsZ contributes to cell elongation by guiding cell wall precursor synthesis in Caulobacter crescentus. Mol. Microbiol. 64, 938–952 (2007)

  15. 15.

    , & Restricted mobility of cell surface proteins in the polar regions of Escherichia coli. J. Bacteriol. 186, 2594–2602 (2004)

  16. 16.

    et al. Polar growth in the alphaproteobacterial order Rhizobiales. Proc. Natl Acad. Sci. USA 109, 1697–1701 (2012)

  17. 17.

    & Getting in the loop: regulation of development in Caulobacter crescentus. Microbiol. Mol. Biol. Rev. 74, 13–41 (2010)

  18. 18.

    , , , & A histidine protein kinase homologue required for regulation of bacterial cell division and differentiation. Proc. Natl Acad. Sci. USA 89, 10297–10301 (1992)

  19. 19.

    et al. Two developmental modules establish 3D beak-shape variation in Darwin’s finches. Proc. Natl Acad. Sci. USA 108, 4057–4062 (2011)

  20. 20.

    & Evolution of shape by multiple regulatory changes to a growth gene. Science 335, 943–947 (2012)

  21. 21.

    , , & Generation of a novel wing colour pattern by the Wingless morphogen. Nature 464, 1143–1148 (2010)

  22. 22.

    et al. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327, 302–305 (2010)

  23. 23.

    , & Hox protein mutation and macroevolution of the insect body plan. Nature 415, 914–917 (2002)

  24. 24.

    On the Origin of Species by Means of Natural Selection, ix + 502 pp. (John Murray, 1859)

  25. 25.

    ImageJ for microscopy. Biotechniques 43, 25–30 (2007)

  26. 26.

    , & Calibrating bacterial evolution. Proc. Natl Acad. Sci. USA 96, 12638–12643 (1999)

  27. 27.

    Selection for nonbuoyant morphological mutants of Caulobacter crescentus. J. Bacteriol. 135, 1141–1145 (1978)

  28. 28.

    , , & The adhesive and cohesive properties of a bacterial polysaccharide adhesin are modulated by a deacetylase. Mol. Microbiol. 88, 486–500 (2013)

  29. 29.

    & Characterization of the adhesive holdfast of marine and freshwater caulobacters. Appl. Environ. Microbiol. 54, 2078–2085 (1988)

  30. 30.

    , & I-TASSER: a unified platform for automated protein structure and function prediction. Nature Protocols 5, 725–738 (2010)

  31. 31.

    & Time-efficient, linear-space local similarity algorithm. Adv. Appl. Math. 12, 337–357 (1991)

  32. 32.

    & MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013)

  33. 33.

    , , , & Jalview version 2–a multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189–1191 (2009)

  34. 34.

    et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731–2739 (2011)

  35. 35.

    , & A robust species tree for the alphaproteobacteria. J. Bacteriol. 189, 4578–4586 (2007)

  36. 36.

    Bias and confidence in not quite large samples. Ann Math Stats 614 (1958)

  37. 37.

    , & A comprehensive set of plasmids for vanillate- and xylose-inducible gene expression in Caulobacter crescentus. Nucleic Acids Res. 35, e137 (2007)

  38. 38.

    PCR-mediated recombination and mutagenesis. SOEing together tailor-made genes. Mol. Biotechnol. 3, 93–99 (1995)

  39. 39.

    et al. Asticcacaulis benevestitus sp. nov., a psychrotolerant, dimorphic, prosthecate bacterium from tundra wetland soil. Int. J. Syst. Evol. Microbiol. 56, 2083–2088 (2006)

  40. 40.

    Evolutionary implications of horizontal gene transfer. Annu. Rev. Genet. 46, 341–358 (2012)

Download references

Acknowledgements

We thank members of the Brun laboratory and C. Fuqua for comments on the manuscript. We thank D. Kysela, V. Hughes and V. Silvanose for help in environmental sampling and phylogenetic analysis, L. Zhuo and C. Huang for help in statistical analysis, S. Shaw for advice on quantitative image analysis, M. Hahn, M. Lynch and R. Raff for discussions on evolution, and the Center for Genomics and Bioinformatics at Indiana University for help in sequencing. We thank the Indiana University Light Microscopy Imaging Center for their help with OMX super-resolution microscopy, supported by National Institutes of Health grant S10RR028697-01, and the Indiana Molecular biology Institute electron microscopy facility at Indiana University for their help with electron microscopy. We thank M. Thanbichler, J. Poindexter, P. Caccamo and P. Viollier for providing us with Caulobacter strain and plasmids, J. Poindexter, J. Peterson, J. Lindquist and A. Quinones for help in locating the strain collection of the late Jack Pate from which we obtained some of the A. excentricus and A. biprosthecum strains used in this study, and M. Wortinger, S. Green, E. Quardokus and J. (Wagner) Herman for early work with Asticcacaulis that helped set the stage for this study. This work was supported by National Institutes of Health grant GM051986, National Science Foundation grant MCB0731950 and by a grant from the Indiana University Metabolomics and Cytomics Initiative (METACyt) program, which was financed, in part, by a major endowment from the Lilly Foundation. P.J.B.B. was supported by National Institutes of Health National Research Service Award AI072992.

Author information

Author notes

    • Pamela J. B. Brown

    Present address: Division of Biological Sciences, University of Missouri, Columbia, Missouri 65211, USA.

Affiliations

  1. Department of Biology, Indiana University, Bloomington, Indiana 47405, USA

    • Chao Jiang
    • , Pamela J. B. Brown
    • , Adrien Ducret
    •  & Yves V. Brun

Authors

  1. Search for Chao Jiang in:

  2. Search for Pamela J. B. Brown in:

  3. Search for Adrien Ducret in:

  4. Search for Yves V. Brun in:

Contributions

C.J., P.J.B.B. and Y.V.B. designed the experiments. C.J. performed the experiments and A.D. developed the automated image analysis tools. C.J., P.J.B.B., A.D. and Y.V.B. analysed and interpreted the data. C.J. and Y.V.B. wrote the paper. C.J., P.J.B.B., A.D. and Y.V.B. edited the paper.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Yves V. Brun.

Extended data

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Text and References and Supplementary Tables 1a-i.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nature12900

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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