Abstract
Experimental adaptation of the bacteriophage phiX174 to a Salmonella host depressed its ability to grow on the traditional Escherichia host, whereas adaptation to Escherichia did not appreciably affect growth on Salmonella. Continued host switching consistently exhibited this pattern. Growth inhibition on Escherichia resulted from two to three substitutions in the major capsid gene. When these phages were forced to grow again on Escherichia, fitness recovery occurred predominantly by reversions at these same sites, rather than by second-site compensatory changes, the more frequently observed mechanism in most microbial systems. The affected residues lie on the virion surface and they alter attachment efficiency, yet they occur in a region distinct from a putative binding region previously identified from X-ray crystallography. These residues not only experienced high rates of evolution in our experiments, but also exhibited high levels of radical amino acid variation among phiX174 and its known relatives, consistent with a history of adaptation involving these sites.
Full Text
The Full Text of this article is available as a PDF (250.8 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Andrade M. A., O'Donoghue S. I., Rost B. Adaptation of protein surfaces to subcellular location. J Mol Biol. 1998 Feb 20;276(2):517–525. doi: 10.1006/jmbi.1997.1498. [DOI] [PubMed] [Google Scholar]
- Bayer M. E., Starkey T. W. The adsorption of bacteriophage phi X174 and its interaction with Escherichia coli; a kinetic and morphological study. Virology. 1972 Jul;49(1):236–256. doi: 10.1016/s0042-6822(72)80026-6. [DOI] [PubMed] [Google Scholar]
- Bieniasz P. D., Fridell R. A., Aramori I., Ferguson S. S., Caron M. G., Cullen B. R. HIV-1-induced cell fusion is mediated by multiple regions within both the viral envelope and the CCR-5 co-receptor. EMBO J. 1997 May 15;16(10):2599–2609. doi: 10.1093/emboj/16.10.2599. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Björkman J., Hughes D., Andersson D. I. Virulence of antibiotic-resistant Salmonella typhimurium. Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):3949–3953. doi: 10.1073/pnas.95.7.3949. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Borman A. M., Paulous S., Clavel F. Resistance of human immunodeficiency virus type 1 to protease inhibitors: selection of resistance mutations in the presence and absence of the drug. J Gen Virol. 1996 Mar;77(Pt 3):419–426. doi: 10.1099/0022-1317-77-3-419. [DOI] [PubMed] [Google Scholar]
- Boucher C. A., van Leeuwen R., Kellam P., Schipper P., Tijnagel J., Lange J. M., Larder B. A. Effects of discontinuation of zidovudine treatment on zidovudine sensitivity of human immunodeficiency virus type 1 isolates. Antimicrob Agents Chemother. 1993 Jul;37(7):1525–1530. doi: 10.1128/aac.37.7.1525. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brown D. T., MacKenzie J. M., Bayer M. E. Mode of host cell penetration by bacteriophage phi X174. J Virol. 1971 Jun;7(6):836–846. doi: 10.1128/jvi.7.6.836-846.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bull J. J., Badgett M. R., Wichman H. A., Huelsenbeck J. P., Hillis D. M., Gulati A., Ho C., Molineux I. J. Exceptional convergent evolution in a virus. Genetics. 1997 Dec;147(4):1497–1507. doi: 10.1093/genetics/147.4.1497. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Burch C. L., Chao L. Evolution by small steps and rugged landscapes in the RNA virus phi6. Genetics. 1999 Mar;151(3):921–927. doi: 10.1093/genetics/151.3.921. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Domingo E., Holland J. J. RNA virus mutations and fitness for survival. Annu Rev Microbiol. 1997;51:151–178. doi: 10.1146/annurev.micro.51.1.151. [DOI] [PubMed] [Google Scholar]
- Dowell C. E. Growth of bacteriophage phiX-174 at elevated temperatures. J Gen Virol. 1980 Jul;49(1):41–50. doi: 10.1099/0022-1317-49-1-41. [DOI] [PubMed] [Google Scholar]
- Dowell C. E., Jansz H. S., Zandberg J. Infection of escherichia coli K-12 by bacteriophage phi X-174. Virology. 1981 Oct 15;114(1):252–255. doi: 10.1016/0042-6822(81)90271-3. [DOI] [PubMed] [Google Scholar]
- Escarmís C., Dávila M., Domingo E. Multiple molecular pathways for fitness recovery of an RNA virus debilitated by operation of Muller's ratchet. J Mol Biol. 1999 Jan 15;285(2):495–505. doi: 10.1006/jmbi.1998.2366. [DOI] [PubMed] [Google Scholar]
- Gao F., Bailes E., Robertson D. L., Chen Y., Rodenburg C. M., Michael S. F., Cummins L. B., Arthur L. O., Peeters M., Shaw G. M. Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature. 1999 Feb 4;397(6718):436–441. doi: 10.1038/17130. [DOI] [PubMed] [Google Scholar]
- Goldman N., Thorne J. L., Jones D. T. Assessing the impact of secondary structure and solvent accessibility on protein evolution. Genetics. 1998 May;149(1):445–458. doi: 10.1093/genetics/149.1.445. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hashemolhosseini S., Holmes Z., Mutschler B., Henning U. Alterations of receptor specificities of coliphages of the T2 family. J Mol Biol. 1994 Jul 8;240(2):105–110. doi: 10.1006/jmbi.1994.1424. [DOI] [PubMed] [Google Scholar]
- Hashemolhosseini S., Montag D., Krämer L., Henning U. Determinants of receptor specificity of coliphages of the T4 family. A chaperone alters the host range. J Mol Biol. 1994 Aug 26;241(4):524–533. doi: 10.1006/jmbi.1994.1529. [DOI] [PubMed] [Google Scholar]
- Kutter E., Gachechiladze K., Poglazov A., Marusich E., Shneider M., Aronsson P., Napuli A., Porter D., Mesyanzhinov V. Evolution of T4-related phages. Virus Genes. 1995;11(2-3):285–297. doi: 10.1007/BF01728666. [DOI] [PubMed] [Google Scholar]
- McKenna R., Ilag L. L., Rossmann M. G. Analysis of the single-stranded DNA bacteriophage phi X174, refined at a resolution of 3.0 A. J Mol Biol. 1994 Apr 15;237(5):517–543. doi: 10.1006/jmbi.1994.1253. [DOI] [PubMed] [Google Scholar]
- Miyata T., Miyazawa S., Yasunaga T. Two types of amino acid substitutions in protein evolution. J Mol Evol. 1979 Mar 15;12(3):219–236. doi: 10.1007/BF01732340. [DOI] [PubMed] [Google Scholar]
- Montag D., Riede I., Eschbach M. L., Degen M., Henning U. Receptor-recognizing proteins of T-even type bacteriophages. Constant and hypervariable regions and an unusual case of evolution. J Mol Biol. 1987 Jul 5;196(1):165–174. doi: 10.1016/0022-2836(87)90519-5. [DOI] [PubMed] [Google Scholar]
- Newbold J. E., Sinsheimer R. L. The process of infection with bacteriophage phiX174. XXXII. Early steps in the infection process: attachment, eclipse and DNA penetration. J Mol Biol. 1970 Apr 14;49(1):49–66. doi: 10.1016/0022-2836(70)90375-x. [DOI] [PubMed] [Google Scholar]
- Novella I. S., Clarke D. K., Quer J., Duarte E. A., Lee C. H., Weaver S. C., Elena S. F., Moya A., Domingo E., Holland J. J. Extreme fitness differences in mammalian and insect hosts after continuous replication of vesicular stomatitis virus in sandfly cells. J Virol. 1995 Nov;69(11):6805–6809. doi: 10.1128/jvi.69.11.6805-6809.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Novella I. S., Hershey C. L., Escarmis C., Domingo E., Holland J. J. Lack of evolutionary stasis during alternating replication of an arbovirus in insect and mammalian cells. J Mol Biol. 1999 Apr 2;287(3):459–465. doi: 10.1006/jmbi.1999.2635. [DOI] [PubMed] [Google Scholar]
- Parker J. S., Parrish C. R. Canine parvovirus host range is determined by the specific conformation of an additional region of the capsid. J Virol. 1997 Dec;71(12):9214–9222. doi: 10.1128/jvi.71.12.9214-9222.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Parrish C. R., O'Connell P. H., Evermann J. F., Carmichael L. E. Natural variation of canine parvovirus. Science. 1985 Nov 29;230(4729):1046–1048. doi: 10.1126/science.4059921. [DOI] [PubMed] [Google Scholar]
- Sanger F., Air G. M., Barrell B. G., Brown N. L., Coulson A. R., Fiddes C. A., Hutchison C. A., Slocombe P. M., Smith M. Nucleotide sequence of bacteriophage phi X174 DNA. Nature. 1977 Feb 24;265(5596):687–695. doi: 10.1038/265687a0. [DOI] [PubMed] [Google Scholar]
- Schrag S. J., Perrot V., Levin B. R. Adaptation to the fitness costs of antibiotic resistance in Escherichia coli. Proc Biol Sci. 1997 Sep 22;264(1386):1287–1291. doi: 10.1098/rspb.1997.0178. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sinsheimer R. L. Bacteriophage phi-X174 and related viruses. Prog Nucleic Acid Res Mol Biol. 1968;8:115–169. [PubMed] [Google Scholar]
- Speck R. F., Wehrly K., Platt E. J., Atchison R. E., Charo I. F., Kabat D., Chesebro B., Goldsmith M. A. Selective employment of chemokine receptors as human immunodeficiency virus type 1 coreceptors determined by individual amino acids within the envelope V3 loop. J Virol. 1997 Sep;71(9):7136–7139. doi: 10.1128/jvi.71.9.7136-7139.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Subbarao E. K., London W., Murphy B. R. A single amino acid in the PB2 gene of influenza A virus is a determinant of host range. J Virol. 1993 Apr;67(4):1761–1764. doi: 10.1128/jvi.67.4.1761-1764.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Truyen U., Evermann J. F., Vieler E., Parrish C. R. Evolution of canine parvovirus involved loss and gain of feline host range. Virology. 1996 Jan 15;215(2):186–189. doi: 10.1006/viro.1996.0021. [DOI] [PubMed] [Google Scholar]
- Turner P. E., Chao L. Sex and the evolution of intrahost competition in RNA virus phi6. Genetics. 1998 Oct;150(2):523–532. doi: 10.1093/genetics/150.2.523. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Weisbeek P. J., van de Pol J. H., van Arkel G. A. Mapping of host range mutants of bacteriophage phiX174. Virology. 1973 Apr;52(2):408–416. doi: 10.1016/0042-6822(73)90335-8. [DOI] [PubMed] [Google Scholar]
- Wichman H. A., Badgett M. R., Scott L. A., Boulianne C. M., Bull J. J. Different trajectories of parallel evolution during viral adaptation. Science. 1999 Jul 16;285(5426):422–424. doi: 10.1126/science.285.5426.422. [DOI] [PubMed] [Google Scholar]
- Yin F. H., Lomax N. B. Host range mutants of human rhinovirus in which nonstructural proteins are altered. J Virol. 1983 Nov;48(2):410–418. doi: 10.1128/jvi.48.2.410-418.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]