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.

Evolutionary determinants of genome-wide nucleotide composition

Nature Ecology & Evolution volume 2, pages 237–240 (2018)Cite this article

Subjects

Abstract

One of the long-standing mysteries of evolutionary genomics is the source of the wide phylogenetic diversity in genome nucleotide composition (G + C versus A + T), which must be a consequence of interspecific differences in mutation bias, the efficiency of selection for different nucleotides or a combination of the two. We demonstrate that although genomic G + C composition is strongly driven by mutation bias, it is also substantially modified by direct selection and/or as a by-product of biased gene conversion. Moreover, G + C composition at fourfold redundant sites is consistently elevated above the neutral expectation—more so than for any other class of sites.

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

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

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

Fig. 1: Relationship between genome-wide nucleotide composition and the neutral expectation.
Fig. 2: Expected equilibrium levels of within-population nucleotide diversity scaled by the neutral expectation.

References

  1. Sueoka, N. Proc. Natl Acad. Sci. USA 48, 582–592 (1962).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  2. Gu, X., Hewett-Emmett, D. & Li, W. H. Genetica 102–103, 383–391 (1998).

    Article  PubMed  Google Scholar 

  3. Chen, S. L., Lee, W., Hottes, A. K., Shapiro, L. & McAdams, H. H. Proc. Natl Acad. Sci. USA 101, 3480–3485 (2004).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  4. Lynch, M. The Origin of Genome Architecture. Sinauer Associates: Sunderland, 2007.

  5. Rocha, E. P. C. & Feil, E. J. PLoS Genet. 6, e1001104 (2010).

    Article  PubMed Central  PubMed  Google Scholar 

  6. Hershberg, R. & Petrov, D. A. PLoS Genet. 6, e1001115 (2010).

    Article  PubMed Central  PubMed  Google Scholar 

  7. Hildebrand, F., Meyer, A. & Eyre-Walker, A. PLoS Genet. 6, e1001107 (2010).

    Article  PubMed Central  PubMed  Google Scholar 

  8. Lynch, M. Proc. Natl Acad. Sci. USA 107, 961–968 (2010).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Lynch, M. et al. Nat. Rev. Genet. 17, 704–714 (2016).

    Article  CAS  PubMed  Google Scholar 

  10. Li, W. H. J. Mol. Evol. 24, 337–345 (1987).

    Article  CAS  PubMed  Google Scholar 

  11. Bulmer, M. Genetics 129, 897–907 (1991).

    CAS  PubMed Central  PubMed  Google Scholar 

  12. McVean, G. A. T. & Charlesworth, B. Genet. Res. 74, 145–158 (1999).

    Article  Google Scholar 

  13. Raghavan, R., Kelkar, Y. D. & Ochman, H. Proc. Natl Acad. Sci. USA 109, 14504–14507 (2012).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  14. Kelkar, Y. D., Phillips, D. S. & Ochman, H. G3 5, 1247–1252 (2015).

    Article  PubMed Central  PubMed  Google Scholar 

  15. Marais, G., Mouchiroud, D. & Duret, L. Genet. Res. 81, 79–87 (2003).

    Article  CAS  PubMed  Google Scholar 

  16. Mancera, E., Bourgon, R., Brozzi, A., Huber, W. & Steinmetz, L. M. Nature 454, 479–485 (2008).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. Galtier, N., Duret, L., Glemin, S. & Ranwez, V. Trends Genet. 25, 1–5 (2009).

    Article  CAS  PubMed  Google Scholar 

  18. Pessia, E. et al. Genome Biol. Evol. 4, 675–682 (2012).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. Williams, A. L. et al. eLife 4, e04637 (2015).

    Article  PubMed Central  Google Scholar 

  20. Mugal, C. F., Weber, C. C. & Ellegren, H. Bioessays 37, 1317–1326 (2015).

    Article  CAS  PubMed  Google Scholar 

  21. Lassalle, F. et al. PLoS. Genet. 11, e1004941 (2015).

    Article  PubMed Central  PubMed  Google Scholar 

  22. Lynch, M. Proc. Natl Acad. Sci. USA 109, 18851–18856 (2012).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Long, H. et al. Genome Biol. Evol. 8, 3815–3821 (2016).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. McKenna, A. et al. Genome Res. 20, 1297–1303 (2010).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  25. DePristo, M. A. et al. Nat. Genet. 43, 491–498 (2011).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Van der Auwera, G. A. et al. Curr. Protoc. Bioinformatics 43, 11.10.1–33 (2013).

    Google Scholar 

  27. Thorvaldsdottir, H., Robinson, J. T. & Mesirov, J. P. Brief. Bioinform. 14, 178–192 (2013).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Support was provided by the Multidisciplinary University Research Initiative awards W911NF-09-1-0444 and W911NF-14-1-0411 from the US Army Research Office to M.L., National Institutes of Health awards R01-GM036827 and R35-GM122566 to M.L., National Natural Science Foundation of China 31741071 to H.L., R01-GM51986 and R35-GM122556 to Y.V.B., F32-GM083581 to D.T.K. and National Science Foundation grant DOB 1442246 to J.T.L. We thank T. G. Doak, P. Keightley, K. Morris, R. Ness, I. Ruiz-Trillo, S. Simpson, W. K. Thomas, A. Uchimura and Z. Ye for providing strains and/or technical help in data acquisition. We thank L. Duret for helpful comments.

Author information

Author notes

  1. Hongan Long, Way Sung and Sibel Kucukyildirim contributed equally to this work.

Authors and Affiliations

  1. Institute of Evolution and Marine Biodiversity, KLMME, Ocean University of China, Qingdao, China

    Hongan Long

  2. Department of Bioinformatics and Genomics, University of North Carolina, Charlotte, NC, USA

    Way Sung

  3. Department of Biology, Hacettepe University, Ankara, Turkey

    Sibel Kucukyildirim

  4. Center for Mechanisms of Evolution, Arizona State University, PO Box 877701, Tempe, AZ, USA

    Emily Williams, Wanfeng Guo & Michael Lynch

  5. Department of Biology, Indiana University, Bloomington, IN, USA

    Samuel F. Miller, Caitlyn Patterson, Colin Gregory, Chloe Strauss, Casey Stone, Cécile Berne, David Kysela, William R. Shoemaker, Jay T. Lennon & Yves V. Brun

  6. Department of Plant Biology, University of Illinois, Urbana–Champaign, Champaign, IL, USA

    Mario E. Muscarella

  7. School of Life Sciences and Partner State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Shatin, Hong Kong

    Haiwei Luo

Authors
  1. Hongan Long
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Way Sung
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sibel Kucukyildirim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Emily Williams
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Samuel F. Miller
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wanfeng Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Caitlyn Patterson
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Colin Gregory
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Chloe Strauss
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Casey Stone
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Cécile Berne
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. David Kysela
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. William R. Shoemaker
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Mario E. Muscarella
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Haiwei Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Jay T. Lennon
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Yves V. Brun
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Michael Lynch
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

H.L., W.S., and M.L. conceived and designed the study, performed the data analyses and wrote the manuscript. All authors contributed to data collection and provided input to the manuscript.

Corresponding author

Correspondence to Michael Lynch.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Tables 1–6

Table 1 shows details of mutation datasets used in this study. Tables 2 and 3 list mutations from 12 microbial organisms that are first reported here. Table 4 shows results of linear regressions involving genome G/C content vs the expectations based on mutation bias. Table 5 gives parameters from regressions of selection coefficients at different genomic sites, as well as those of selection coefficients vs the mutation bias m. Table 6 shows the relationship between expression level and G/C content within 17 organisms.

Life Sciences Reporting Summary

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Long, H., Sung, W., Kucukyildirim, S. et al. Evolutionary determinants of genome-wide nucleotide composition. Nat Ecol Evol 2, 237–240 (2018). https://doi.org/10.1038/s41559-017-0425-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-017-0425-y

This article is cited by

Search

Advanced 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