Skip to main content
SpringerLink
Log in

Genome Comparisons of Wild Isolates of Caulobacter crescentus Reveal Rates of Inversion and Horizontal Gene Transfer

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Since previous interspecies comparisons of Caulobacter genomes have revealed extensive genome rearrangements, we decided to compare the nucleotide sequences of four C. crescentus genomes, NA1000, CB1, CB2, and CB13. To accomplish this goal, we used PacBio sequencing technology to determine the nucleotide sequence of the CB1, CB2, and CB13 genomes, and obtained each genome sequence as a single contig. To correct for possible sequencing errors, each genome was sequenced twice. The only differences we observed between the two sets of independently determined sequences were random omissions of a single base in a small percentage of the homopolymer regions where a single base is repeated multiple times. Comparisons of these four genomes indicated that horizontal gene transfer events that included small numbers of genes occurred at frequencies in the range of 10−3 to 10−4 insertions per generation. Large insertions were about 100 times less frequent. Also, in contrast to previous interspecies comparisons, we found no genome rearrangements when the closely related NA1000, CB1, and CB2 genomes were compared, and only eight inversions and one translocation when the more distantly related CB13 genome was compared to the other genomes. Thus, we estimate that inversions occur at a rate of one per 10 to 12 million generations in Caulobacter genomes. The inversions seem to be complex events that include the simultaneous creation of indels.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Ash K, Brown T, Watford T et al (2014) A comparison of the Caulobacter NA1000 and K31 genomes reveals extensive genome rearrangements and differences in metabolic potential. Open Biol 4:140128. https://doi.org/10.1098/rsob.140128

    Article  PubMed  PubMed Central  Google Scholar 

  2. Berrios L, Ely B (2018) Achieving accurate sequence and annotation data for Caulobacter vibrioides CB13. Curr Microbiol 75(12):1642–1648. https://doi.org/10.1007/s00284-018-1572-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Bolotin E, Hershberg R (2017) Horizontally acquired genes are often shared between closely related species. Front Microbiol 8:1536. https://doi.org/10.3389/fmicb.2017.01536

    Article  PubMed  PubMed Central  Google Scholar 

  4. Boto L (2015) Evolutionary change and phylogenetic relationships in light of horizontal gene transfer. J Biosci 40:465–472. https://doi.org/10.1007/s12038-015-9514-8

    Article  PubMed  Google Scholar 

  5. Chen J, Quiles-Puchalt N, Chiang YN et al (2018) Genome hypermobility by lateral transduction. Science 362:207–212. https://doi.org/10.1126/science.aat5867

    Article  CAS  PubMed  Google Scholar 

  6. Christen B, Abeliuk E, Collier JM et al (2011) The essential genome of a bacterium. Mol Syst Biol 7:528. https://doi.org/10.1038/msb.2011.58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Doolittle WF, Bapteste E (2007) Pattern pluralism and the tree of life hypothesis. Proc Natl Aad Sci USA 104:2043–2049. https://doi.org/10.1073/pnas.0610699104

    Article  CAS  Google Scholar 

  8. Darling AE, Mau B, Perna NT (2010) progressiveMAUVE: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 5:e11147. https://doi.org/10.1371/journal.pone.0011147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Drake JW, Charlesworth B, Charlesworth D, Crow JF (1998) Rates of spontaneous mutation. Genetics 148:1667–1686

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Ely, B (1991) Genetics of Caulobacter crescentus. Methods Enzymol 204:372–384

    Article  CAS  PubMed  Google Scholar 

  11. Ferber DM, Ely B (1982) Resistance to amino acid inhibition in Caulobacter crescentus. Mol Gen Genet 187:446–452

    Article  CAS  Google Scholar 

  12. Friedman R, Ely B (2012) Codon usage methods for horizontal gene transfer detection generate an abundance of false positive and false negative results. Curr Microbiol 65:639–642. https://doi.org/10.1007/s00284-012-0205-5

    Article  CAS  PubMed  Google Scholar 

  13. Hentchel KL, Reyes Ruiz LM, Curtis PD et al (2018) Genome-scale fitness profile of Caulobacter crescentus grown in natural freshwater. ISME J. https://doi.org/10.1038/s41396-018-0295-6

    Article  PubMed  PubMed Central  Google Scholar 

  14. Johnson RC, Ely B (1977) Isolation of spontaneously derived mutants of Caulobacter crescentus. Genetics 86:25–32

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Koonin EV, Puigbo P, Wolf YI (2011) Comparison of Phylogenetic trees and search for a central trend in the “Forest of Life”. J Comput Biol 18:917–924. https://doi.org/10.1089/cmb.2010.0185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Marks ME, Castro-Rojas CM, Telling C et al (2010) The genetic basis of laboratory adaptation in Caulobacter crescentus. J Bacteriol 192:3678–3688. https://doi.org/10.1128/JB.00255-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Nierman WC, Feldblyum TV, Laub MT et al (2001) Complete genome sequence of Caulobacter crescentus. Proc Natl Acad Sci USA 98:4136–4141. https://doi.org/10.1073/pnas.061029298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304

    Article  CAS  PubMed  Google Scholar 

  19. Oliveira PH, Touchon M, Cury J, Rocha EPC (2017) The chromosomal organization of horizontal gene transfer in bacteria. Nat Commun 8:841. https://doi.org/10.1038/s41467-017-00808-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Poindexter JS (1964) Biological properties and classification of the Caulobacter group. Bacteriol Rev 28:231–295

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Quail MA, Smith M, Coupland P (2012) A tale of three next generation sequencing platforms: comparison of Ion Torrent, Pacific Biosciences and Illumina MiSeq sequencers. BMC Genom 13:341. https://doi.org/10.1186/1471-2164-13-341

    Article  CAS  Google Scholar 

  22. Rocha EPC (2016) Using sex to cure the genome. PLoS Biol 14(3):e1002417. https://doi.org/10.1371/journal.pbio.1002417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Scott D, Ely B (2015) Comparison of genome sequencing technology and assembly methods for the analysis of a GC-rich bacterial genome. Curr Microbiol 70:338–344. https://doi.org/10.1007/s00284-014-0721-6

    Article  CAS  PubMed  Google Scholar 

  24. Scott D, Ely B (2016) Conservation of the essential genome among Caulobacter and Brevundimonas species. Curr Microbiol 72:503–510. https://doi.org/10.1007/s00284-014-0721-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Shin SC, Ahndo H, Kim SJ et al (2013) Advantages of single-molecule real-time sequencing in high-GC content genomes. PLoS ONE 8:e68824. https://doi.org/10.1371/journal.pone.0068824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Souza V, Turner P, Lenski RL (1997) Long term experimental evolution in Escherichia coli. V. Effects of recombination with immigrant genotypes on the rate of bacterial evolution. J Evol Biol 10(5):7453–7769

    Article  Google Scholar 

  27. Williams KP (2002) Integration sites for genetic elements in prokaryotic tRNA and tmRNA genes: sublocation preference of integrase subfamilies. Nucleic Acids Res 30:866–875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was funded in part by NIH Grant GM076277 and by the NIH Institutional Development Award (IDeA) Grant Number P20GM103446 to DCS and by NIH Grant GM076277 to BE.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of South Carolina, Columbia, SC, 29208, USA

    Bert Ely & Kiesha Wilson

  2. Department of Biological Sciences, Delaware State University, Dover, DE, 19901, USA

    Keshawn Ross, Damyen Ingram, Tajah Lewter, Jasmine Herring, David Duncan, Anthea Aikins & Derrick Scott

Authors
  1. Bert Ely
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kiesha Wilson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Keshawn Ross
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Damyen Ingram
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tajah Lewter
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jasmine Herring
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. David Duncan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Anthea Aikins
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Derrick Scott
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bert Ely.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 549 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ely, B., Wilson, K., Ross, K. et al. Genome Comparisons of Wild Isolates of Caulobacter crescentus Reveal Rates of Inversion and Horizontal Gene Transfer. Curr Microbiol 76, 159–167 (2019). https://doi.org/10.1007/s00284-018-1606-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-018-1606-x

Search

Navigation