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Evolutionary Robustness of an Optimal Phenotype: Re-evolution of Lysis in a Bacteriophage Deleted for Its Lysin Gene

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Abstract

Optimality models are frequently used to create expectations about phenotypic evolution based on the fittest possible phenotype. However, they often ignore genetic details, which could confound these expectations. We experimentally analyzed the ability of organisms to evolve towards an optimum in an experimentally tractable system, lysis time in bacteriophage T7. T7 lysozyme helps lyse the host cell by degrading its cell wall at the end of infection, allowing viral escape to infect new hosts. Artificial deletion of lysozyme greatly reduced fitness and delayed lysis, but after evolution both phenotypes approached wild-type values. Phage with a lysis-deficient lysozyme evolved similarly. Several mutations were involved in adaptation, but most of the change in lysis timing and fitness increase was mediated by changes in gene 16, an internal virion protein not formerly considered to play a role in lysis. Its muralytic domain, which normally aids genome entry through the cell wall, evolved to cause phage release. Theoretical models suggest there is an optimal lysis time, and lysis more rapid or delayed than this optimum decreases fitness. Artificially constructed lines with very rapid lysis had lower fitness than wild-type T7, in accordance with the model. However, while a slow-lysing line also had lower fitness than wild-type, this low fitness resulted at least partly from genetic details that violated model assumptions.

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Acknowledgments

We thank X. Zhang, F.W. Studier, and A.R. Poteete for phages and plasmids used in this work. Helpful suggestions were provided by R. Young, S. Hedtke, I. Wang, two anonymous reviewers, and the Bull lab group. This study was funded by NIH GM 57756 to J.J.B. and GM 32095 to I.J.M.

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Authors and Affiliations

  1. Section of Integrative Biology, University of Texas, Austin, Texas, 78712, USA

    Richard H. Heineman & James J. Bull

  2. Section of Molecular Genetics and Microbiology, University of Texas, Austin, Texas, 78712, USA

    Ian J. Molineux

  3. Institute for Cell and Molecular Biology, University of Texas, Austin, Texas, 78712, USA

    Ian J. Molineux & James J. Bull

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  1. Richard H. Heineman
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  2. Ian J. Molineux
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  3. James J. Bull
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Correspondence to Richard H. Heineman.

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Heineman, R.H., Molineux, I.J. & Bull, J.J. Evolutionary Robustness of an Optimal Phenotype: Re-evolution of Lysis in a Bacteriophage Deleted for Its Lysin Gene. J Mol Evol 61, 181–191 (2005). https://doi.org/10.1007/s00239-004-0304-4

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  • DOI: https://doi.org/10.1007/s00239-004-0304-4

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