Bacteriophage experimental evolution

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Experimental evolution studies are a means of testing evolutionary theory under carefully designed, reproducible experiments. While theoretically any organism could be used for experimental evolution studies, those with rapid generation times, high mutation rates, large population sizes, and small sizes increase the feasibility of experimental studies in a laboratory context. For these reasons, bacteriophages (i.e. viruses that infect bacteria) are especially favored by experimental evolutionary biologists. Bacteriophages, and microbial organisms, can be frozen in stasis, facilitating comparison of evolved strains to ancestors. Additionally, microbes are especially labile from a molecular biologic perspective. Many molecular tools have been developed to manipulate the genetic material of microbial organisms, and because of their small genome sizes, sequencing the full genomes of evolved strains is trivial. Therefore, comparisons can be made for the exact molecular changes in evolved strains during adaptation to novel conditions. This article explains how such experiments are conducted, and contains annotated references for experimental evolution studies conducted with bacteriophages, as well as an expansion of a table presented by Breitbart et al. (2005). .

Experimental studies, by category

Laboratory phylogenetics

Phylogenetics is the study of the evolutionary relatedness of organisms. Laboratory phylogenetics is the study of the evolutionary relatedness of laboratory-evolved organisms. An advantage of laboratory phylogenetics is the exact evolutionary history of an organism is known, rather than estimated as is the case for most organisms.

  • Hahn, M. W., M. D. Rausher, and C. W. Cunningham, 2002. Distinguishing between selection and population expansion in an experimental lineage of bacteriophage T7. Genetics 161:11-20. full text
  • Oakley, T. H., and C. W. Cunningham, 2000. Independent contrasts succeed where ancestor reconstruction fails in a known bacteriophage phylogeny. Evolution 54:397-405. abstract
  • Cunningham, C.W., K. Jeng, J. Husti, M. Badgett, I.J. Molineux, D.M. Hillis and J.J. Bull, 1997. Parallel molecular evolution of deletions and nonsense mutations in bacteriophage T7. Mol. Biol. Evol. 14:113-116. full text
  • Bull, J. J., C. W. Cunningham, I. J. Molineux, M. R. Badgett, and D. M. Hills, 1993. Experimental molecular evolution of bacteriophage T7. Evolution 47:993-1007. abstract
  • Hillis, D.M., J.J. Bull, M.E. White, M.R. Badgett and I.J. Molineux, 1992. Experimental phylogenetics: generation of a known phylogeny. Science. 255:589-592. abstract & pay article
  • Studier, F. W., 1980. The last of the T phages, p. 72-78. In N. H. Horowitz and E. Hutchings, Jr. (eds.), Genes, Cells, and Behavior: A View of Biology Fifty Years Later.
  • Studier, F. W., 1979. Relationships among different strains of T7 and among T7-related bacteriophages. Virology 95:70-84.

Epistasis

Epistasis is the dependence of the effect of one gene or mutation on the presence of another gene or mutation. Theoretically epistasis can be of three forms: no epistasis (additive inheritance), synergystic (or positive) epistasis and antagonistic (or negative) epistasis. In synergystic epistasis, each additional mutation has increasing negative impact on fitness. In antagonistic epistasis, the effect of each mutation declines with increasing numbers of mutation. Understanding whether the majority of genetic interactions are synergistic or antagonistic will help solve such problems as the evolution of sex.

  • Burch, C.L., and L. Chao. 2004. Epistasis and its relationships to canalization in the RNA virus Φ6. Genetics. 167:559-567. full text
  • You, L., and J. Yin. 2002. Dependence of epistasis on environment and mutation severity as revealed by in silico mutagenesis of phage T7. Genetics. 160:1273-1281. full text
  • Schuppli, D., J. Georgijevic, and H. Weber. 2000. Synergism of mutations in bacteriophage Qβ RNA affecting host factor dependence of Qβ replicase. J. Mol. Biol. 295:149-154.

The phage literature provides many examples of epistasis which are not studied under the context of experimental evolution nor necessarily described as examples of epistasis.

Experimental adaptation

Experimental adaptation involves selection of organisms either for specific traits or under specific conditions. For example, strains could be evolved under conditions of high temperatures to observe the molecular changes that facilitate survival and reproduction under those conditions.

  • Bull, J. J., J. Millstein, J. Orcutt and H.A. Wichman. 2006. Evolutionary feedback mediated through population density, illustrated with viruses in chemostats. Am. Nat. 167:E39-E51. abstract
  • Bull, J. J., M. R. Badgett, R. Springman, and I. J. Molineux. 2004. Genome properties
  • Bull, J. J., M. R. Badgett, D. Rokyta, and I. J. Molineux. 2003. Experimental evolution yields hundreds of mutations in a functional viral genome. J. Mol. Evol. 57:241-248. abstract & pay article
  • Bull, J. J., M.R. Badgett, H.A. Wichman, J.P. Hulsenbeck, D.M. Hillis, A. Gulati, C. Ho and I.J. Molineux. 1997. Exceptional convergent evolution in a virus. Genetics. 147:1497-1507. full text

The reader should be aware that numerous phage experimental adaptations were performed in the early decades of phage study.

Adaptation to usual hosts.

  • Wichman, H. A., J. Wichman, and J. J. Bull. 2005. Adaptive molecular evolution for 13,000 phage generations: A possible arms race. Genetics 170:19-31. full text
  • Rokyta, D., M. R. Badgett, I. J. Molineux, and J. J. Bull. 2002. Experimental genomic evolution: extensive compensation for loss of DNA ligase activity in a virus. Mol. Biol. Evol. 19:230-238. full text
  • Burch, C. L., and L. Chao. 2000. Evolvability of an RNA virus is determined by its mutational neighbourhood. Nature 406:625-628. abstract & pay article
  • Wichman, H. A., L. A. Scott, C. D. Yarber, and J. J. Bull. 2000. Experimental evolution
  • Wichman, H. A., M. R. Badgett, L. A. Scott, C. M. Boulianne, and J. J. Bull. 1999. Different trajectories of parallel evolution during viral adaptation. Science 285:422-424. abstract & pay article

Adaptation to new or modified hosts.

  • Duffy, S., P. E. Turner, and C. L. Burch. 2006. Pleiotropic Costs of Niche Expansion in the RNA Bacteriophage Φ6. Genetics 172:751-757. full text
  • Pepin, K. M., M. A. Samuel, and H. A. Wichman. 2006. Variable Pleiotropic Effects From Mutations at the Same Locus Hamper Prediction of Fitness From a Fitness Component. Genetics 172:2047-2056. full text
  • Crill, W. D., H. A. Wichman, and J. J. Bull. 2000. Evolutionary reversals during viral adaptation to alternating hosts. Genetics 154:27-37. full text
  • Bull, J. J., A. Jacoboson, M. R. Badgett, and I. J. Molineux. 1998. Viral escape from antisense RNA. Mol. Microbiol. 28:835-846. full text
  • Hibma, A. M., S. A. Jassim, and M. W. Griffiths. 1997. Infection and removal of L-forms of Listeria monocytogenes with bred bacteriophage. Int. J. Food Microbiol. 34:197-207. abstract & pay article
  • Jassim, S. A. A., S. P. Denyer, and G. S. A. B. Stewart. 1995. Virus breeding. International Patent Application. WO 9523848. full text (under tab labeled "documents")
  • Schuppli, D., G. Miranda, H. C. T. Tsui, M. E. Winkler, J. M. Sogo, and H. Weber. 1997. Altered 3'-terminal RNA structure in phage Qβ adapted to host factor-less Escherichia coli. Proc. Natl. Acad. Sci. USA 94:10239-10242. full text
  • Hashemolhosseini, S., Z. Holmes, B. Mutschler, and U. Henning. 1994. Alterations of receptor specificities of coliphages of the T2 family. J. Mol. Biol. 240:105-110. abstract & pay article

The older phage literature, e.g., pre-1950s, contains numerous examples of phage adaptations to different hosts.

Adaptation to modified conditions

  • Bacher, J. M., J. J. Bull, and A. D. Ellington. 2003. Evolution of phage with chemically ambiguous proteomes. BMC Evol. Biol. 3:24 full text
  • Bull, J. J., A. Jacoboson, M. R. Badgett, and I. J. Molineux. 1998. Viral escape from
  • Merril, C. R., B. Biswas, R. Carlton, N. C. Jensen, G. J. Creed, S. Zullo, and S. Adhya. 1996. Long-circulating bacteriophage as antibacterial agents. Proc. Natl. Acad. Sci. USA 93:3188-3192. full text
  • Gupta, K., Y. Lee and J. Yin. 1995. Extremo-phage: in vitro selection of tolerance to a hostile environment. J. Mol. Evol. 41:113-114. abstract & pay article

The older phage literature, e.g., pre-1950s, also contains examples of phage adaptations to different culture conditions, such as phage T2 adaptation to low salt conditions.

Adaptation to high temperatures.

  • Knies, J.L., R. Izem, K.L. Supler. J.G. Kingsolver, and C.L. Burch. 2006. The genetic basis of thermal reaction norm evolution in lab and natural phage population. PLoS Biology. 4:e201. full text
  • Poon, A., and L. Chao. 2005. The rate of compensatory mutation in the DNA bacteriophage ΦX174. Genetics. 170:989-999. full text
  • Poon, A., and L. Chao. 2004. Drift increases the advantage of sex in RNA bacteriophage Φ6. Genetics 166:19-24. full text
  • Holder, K. K., and J. J. Bull. 2001. Profiles of adaptation in two similar viruses. Genetics 159:1393-1404. full text
  • Bull, J. J., M. R. Badgett, and H. A. Wichman. 2000. Big-benefit mutations in a bacteriophage inhibited with heat. Mol. Biol. Evol. 17:942-950. full text

Adaptation as compensation for deleterious mutations.

  • Poon, A., and L. Chao. 2005. The rate of compensatory mutation in the DNA bacteriophage ΦX174. Genetics. 170:989-999. full text
  • Heineman, R. H., I. J. Molineux, and J. J. Bull. 2005. Evolutionary robustness of an optimal phenotype: re-evolution of lysis in a bacteriophage deleted for its lysin gene. J. Mol. Evol. 61:181-191. abstract & pay article
  • Hayashi, Y., H. Sakata, Y. Makino, I. Urabe, and T. Yomo. 2003. Can an arbitrary sequence evolve towards acquiring a biological function? J. Mol. Evol. 56:162-168. abstract & pay article
  • Rokyta, D., M. R. Badgett, I. J. Molineux, and J. J. Bull. 2002. Experimental genomic evolution: extensive compensation for loss of DNA ligase activity in a virus. Mol. Biol. Evol. 19:230-238. full text
  • Burch, C. L., and L. Chao. 1999. Evolution by small steps and rugged landscapes in the RNA virus Φ6. Genetics 151:921-927. full text
  • Klovins, J., N. A. Tsareva, M. H. de Smit, V. Berzins, and D. Van. 1997. Rapid evolution of translational control mechanisms in RNA genomes. J. Mol. Biol. 265:372-384. abstract &
  • Olsthoorn, R. C., and J. van Duin. 1996. Evolutionary reconstruction of a hairpin deleted from the genome of an RNA virus. Proc. Natl. Acad. Sci. USA 93:12256-12261. full text
  • Nelson, M. A., M. Ericson, L. Gold, and J. F. Pulitzer. 1982. The isolation and characterization of TabR bacteria: Hosts that restrict bacteriophage T4 rII mutants Mol. Gen. Genet. 188:60-68. abstract & pay article
  • Nelson, M.A. and L. Gold. 1982. The isolation and characterization of bacterial strains (Tab32) that restrict bacteriophage T4 gene 32 mutants Mol. Gen. Genet. 188:69-76.

There are many examples in the early phage literature of phage adapting and compensating for deleterious mutations.

Adaptation as toward change in phage virulence

Virulence is the negative impact that a pathogen (or parasite) has on the Darwinian fitness of a harboring organism (host). For phage, virulence results either in reduction of bacterial division rates or, more typically, in the death (via lysis) of individual bacteria. A number of theory papers exist on this subject, especially as it applies to the evolution of phage latent period.

  • Kerr, B., C. Neuhauser, B. J. M. Bohannan, and A. M. Dean. 2006. Local migration promotes competitive restraint in a host–pathogen 'tragedy of the commons'. Nature 442:75-78. abstract & pay article

Wang, I.-N. 2006. Lysis timing and bacteriophage fitness. Genetics 172:17-26. full text

  • Abedon, S. T., P. Hyman, and C. Thomas. 2003. Experimental examination of bacteriophage latent-period evolution as a response to bacterial availability. Appl. Environ. Microbiol. 69:7499-7506. full text
  • Messenger, S. L., I. J. Molineux, and J. J. Bull. 1999. Virulence evolution in a virus obeys a trade-off. Proc. R. Soc. Lond. B Biol. Sci. 266:397-404. abstract
  • Bull, J. J., and I. J. Molineux. 1992. Molecular genetics of adaptation in an experimental model of cooperation. Evolution 46:882-895.
  • Bull, J. J., I. J. Molineux, and W. R. Rice. 1991. Selection for benevolence in a host-parasite system. Evolution 45:875-882.

The older phage literature contains numerous references to phage virulence, and phage virulence evolution. However, the reader should be warned that virulence is often used as a synonym for "not temperature", a usage which is neither employed here nor to be encouraged generally.

Impact of sex/coinfection

More than one phage can coinfect the same bacterial cell. When this happens, the phage can exchange genes, which is equivalent to "sex." Note that a number of the immediately following studies employ sex to overcome Muller's ratchet while papers that demonstrate Muller's ratchet (i.e., without employing sex to overcome the result) are instead presented under that heading.

  • Froissart, R., C. O. Wilke, R. Montville, S. K. Remold, L. Chao, and P. E. Turner. 2004. Co-infection weakens selection against epistatic mutations in RNA viruses. Genetics
  • Montville, R., R. Froissart, S. K. Remold, O. Tenaillon, and P. E. Turner. 2005. Evolution of mutational robustness in an RNA virus. PLoS Biology 3:e381 full text
  • Sachs, J.L. and J. J. Bull. 2005. Experimental evolution of conflict mediation between genomes. Proc. Natl. Acad. Sci. 102:390-395. full text
  • Poon, A., and L. Chao. 2004. Drift increases the advantage of sex in RNA bacteriophage
  • Turner, P. E., and L. Chao. 1998. Sex and the evolution of intrahost competition in RNA virus Φ6. Genetics 150:523-532. full text
  • L. Chao, T. T. Tran, and T. T. Tran. 1997. The advantage of sex in the RNA virus Φ6. Genetics 147:953-959. full text
  • Malmberg, R. L. 1977. The evolution of epistasis and the advantage of recombination in populations of bacteriophage T4. Genetics 86:607-621. full text

Muller’s ratchet

Muller’s ratchet is the gradual, but irreversible accumulation of deleterious mutations in asexual organisms. Asexual organisms do not undergo gene exchange and therefore can't recreate mutation-free genomes. Chao, 1997, provides a phage-emphasizing review of the subject.

  • de la Peña, M., S. F. Elena, and A. Moya. 2000. Effect of deleterious mutation-accumulation on the fitness of RNA bacteriophage MS2. Evolution 54:686-691. abstract
  • L. Chao. 1990. Fitness of RNA virus decreased by Muller's ratchet. Nature 348:454-455. abstract

Prisoner’s Dilemma

Prisoner's dilemma is a part of game theory which involves two individuals choosing to cooperate or defect, reaping differential rewards. During phage coinfection, it pertains to viruses which produce more protein products than they use (cooperators) and viruses which use more protein products than they produce (defectors).

  • Turner, P. E., and L. Chao. 2003. Escape from Prisoner's Dilemma in RNA phage Φphi6. Am. Nat. 161:497-505. abstract
  • Turner, P. E., and L. Chao. 1999. Prisoner's dilemma in an RNA virus. Nature 398:441-443. abstract

Coevolution

Coevolution is the study of the evolutionary influence that two species have upon each other. Phage-bacterial coevolution is typically studied within the context of phage community ecololgy.

  • Buckling, A., Y. Wei, R. C. Massey, M. A. Brockhurst, and M. E. Hochberg. 2006. Antagonistic coevolution with parasites increases the cost of host deleterious mutations. Proc. R. Soc. Lond. B Biol. Sci. 273:45-49. abstract
  • Morgan, A. D., S. Gandon, and A. Buckling. 2005. The effect of migration on local adaptation in a coevolving host-parasite system. Nature 437:253-256. abstract & pay article
  • Forde, S. E., J. N. Thompson, and B. J. M. Bohannan. 2004. Adaptation varies through space and time in a coevolving host–parasitoid interaction. Nature 431:841-844. abstract
  • Mizoguchi, K., M. Morita, C. R. Fischer, M. Yoichi, Y. Tanji, and H. Unno. 2003. Coevolution of bacteriophage PP01 and Escherichia coli O157:H7 in continuous culture. Appl. Environ. Microbiol. 69:170-176. full text
  • Buckling, A., and P. B. Rainey. 2002. Antagonistic coevolution between a bacterium and a bacteriophage. Proc. R. Soc. Lond. B Biol. Sci. 269:931-936. full text
  • Buckling, A., and P. B. Rainey. 2002. The role of parasites in sympatric and allopatric host diversification. Nature 420:496-499. abstract & pay article
  • Lenski, R.E. and B.R. Levin. 1985. Constraints on the coevolution of bacteria and virulent phage – a model, some experiments and predictions for natural communities. Am. Nat. 125:585-602.
  • Chao, L., B.R. Levin, and F.M. Stewart. 1977. A complex community in a simple habitat: an experimental study with bacteria and phage. Ecology. 58:369-378. abstract

Historical considerations

The following is quoted from d'Hérelle and Smith, 1924.

ADAPTATION AND THE BACTERIOPHAGE

All authors admit that the virulence of the bacteriophage may increase for a given bacterium, or that it may diminish, according to the condition of the moment. This is then a phenomenon of adaptation analogous to that observed with all parasites.

The fact of attenuation and of exaltation of virulence is sufficient by itself to show that the bacteriophage is an autonomous parasite. Certain authors (Seiffert) while admitting the fact, have tried to maintain that it is not the bateriophage which adapts itself, but rather the bacterium. An obvious reply would be that it is not the bacterium with which the passages are made, since each passage involves the action of the filtrate of a preceding lysed culture upon a fresh normal suspension of bacteria. By virtue of the fact that only the filtrate is concerned in the passages the adaptation must be something which is found in the filtrate.

But this is not all. It is certain that the bacterium, which is also a living being, must react, must likewise undergo adaptation. Constant experience shows that this is just what happens, but the adaptation which takes place, far from tending toward a destructive action, as would be the case if the bacterium adapted itself to the secretion of a lytic substance, reacts against the bacteriophage by a process of adaptation tending to hinder the action of the bacteriophage. The bacterium acquires a resistance. This resistance may, indeed, reach to a completely refractory condition, and, in such a case, it is the bacterium which destroys the bacteriophage (d'Herelle, Flu).

The bacteriophage adapts itself to a more and more vigorous attack against the bacterium, and the bacterium accustoms itself to resist this attack. Considering only experimental facts this is clearly evident when no pretense is made to interpret these facts to make them fit into a preconceived theoretical scheme.

But there are still other points. The bacteriophage adapts itself to harmful effects of the medium. I have shown that the bacteriophage can gradually adapt itself to the harmful action of glycerol and of acids. Asheshov has habituated a bacteriophage, originally unable to effect bacteriophagy in an acid medium, to act very strongly after a number of passages in a medium of increasing acidity. Wolff and Janzen have succeeded in adapting it to different antiseptics.

We have already seen that the bacteriophage functions as an antigen and that the serum of an animal which has received serial injections of a bacteriophage possesses the property of inhibiting bacteriophagous actions. Prausnitz has shown further that it is possible to adapt the bacteriophage to resist the inhibiting action of an antiserum. Once this adaptation is accomplished bacteriophagy takes place in any quantity of antiserium, although prior to the adaptation, an amount of a thousandth of a cubic centimeter or even less paralyzed bacteriophagy completely.

The proofs are then multiple: The bacteriophage possesses the power of adaptation. We have seen that it also possesses that of assimilation. It possesses likewise the two corollaries of these powers; the faculties of multiplication and variability as everyone admits. (pp. 267-268)

The bacteriophagous corpuscles are endowed with the powers of assimilation and adaptation, the faculties of multiplication and of variation. They are this necessarily living beings since they possess all of the characteristics of other living things.

A single bacteriophage is usually virulent, at the same time, for a certain number of bacterial species. This virulence is variable and is subject to increase or attenuation. Increase may always be secured in vitro by the method of passages at the expense of the bacterium for which it is desired to increase the virulence.

The bacterium does not remain passive before the attack of the bacteriophage. It is capable of resistance. It is even able, when the conditions for it are favorable, to acquire a complete immunity. (pp. 269-270)

See also

Experimental evolution

Evolution

References

Breitbart, M., F. Rohwer, and S. T. Abedon. 2005. Phage ecology and bacterial pathogenesis, p. 66-91. In M. K. Waldor, D. I. Friedman, and S. L. Adhya (eds.), Phages: Their Role in Bacterial Pathogenesis and Biotechnology. ASM Press, Washington DC. ISBN 1-55581-307-0

d'Hérelle, F., and G. H. Smith. 1924. Immunity in Natural Infectious Disease. Williams & Wilkins Co., Baltimore.

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