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Volume 167, Issue 5

Editor's Choice Sustained coevolution of phage Lambda and involves inner- as well as outer-membrane defences and counter-defences Open Access

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Abstract

Bacteria often evolve resistance to phage through the loss or modification of cell surface receptors. In and phage λ, such resistance can catalyze a coevolutionary arms race focused on host and phage structures that interact at the outer membrane. Here, we analyse another facet of this arms race involving interactions at the inner membrane, whereby evolves mutations in mannose permease-encoding genes and that impair λ’s ability to eject its DNA into the cytoplasm. We show that these mutants arose concurrently with the arms race at the outer membrane. We tested the hypothesis that λ evolved an additional counter-defence that allowed them to infect bacteria with deleted genes. The deletions severely impaired the ancestral λ, but some evolved phage grew well on the deletion mutants, indicating that they regained infectivity by evolving the ability to infect hosts independently of the mannose permease. This coevolutionary arms race fulfils the model of an inverse gene-for-gene infection network. Taken together, the interactions at both the outer and inner membranes reveal that coevolutionary arms races can be richer and more complex than is often appreciated.

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© 2021 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2021-05-25
2024-04-26
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References

  1. Lenski RE, Levin BR. Constraints on the coevolution of bacteria and virulent phage: a model, some experiments, and predictions for natural communities. Am Nat 1985; 125:585–602 [View Article]
     [Google Scholar]
  2. Chao L, Levin BR, Stewart FM. A complex community in a simple habitat: an experimental study with bacteria and phage. Ecology 1977; 58:369–378 [View Article]
     [Google Scholar]
  3. Levin BR, Stewart FM, Chao L. Resource-limited growth, competition, and predation: a model and experimental studies with bacteria and bacteriophage. The American Naturalist 1977; 111:3–24 [View Article]
     [Google Scholar]
  4. Waterbury JB, Valois FW. Resistance to co-occurring phages enables marine Synechococcus communities to coexist with cyanophages abundant in seawater. Appl Environ Microbiol 1993; 59:3393–3399 [View Article] [PubMed]
     [Google Scholar]
  5. Williams Smith H, Huggins MB. The association of the O18, K1 and H7 antigens and the CoIV plasmid of a strain of Escherichia coli with its virulence and immunogenicity. Microbiology 1980; 121:387–400 [View Article]
     [Google Scholar]
  6. Williams Smith H, Huggins MB. Successful treatment of experimental Escherichia coli infections in mice using phage: its general superiority over antibiotics. J Gen Microbiol 1982; 128:307–318 [View Article] [PubMed]
     [Google Scholar]
  7. Burmeister AR, Fortier A, Roush C, Lessing AJ, Bender RG et al. Pleiotropy complicates a trade-off between phage resistance and antibiotic resistance. Proc Natl Acad Sci U S A 2020; 117:11207–11216 [View Article] [PubMed]
     [Google Scholar]
  8. Chan BK, Sistrom M, Wertz JE, Kortright KE, Narayan D et al. Phage selection restores antibiotic sensitivity in MDR Pseudomonas aeruginosa . Sci Rep 2016; 6:26717 [View Article] [PubMed]
     [Google Scholar]
  9. Kortright KE, Chan BK, Koff JL, Turner PE. Phage therapy: A renewed approach to combat antibiotic-resistant bacteria. Cell Host Microbe 2019; 25:219–232 [View Article] [PubMed]
     [Google Scholar]
  10. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P et al. CRISPR provides acquired resistance against viruses in prokaryotes. Science 2007; 315:1709 [View Article] [PubMed]
     [Google Scholar]
  11. Shmakov S, Smargon A, Scott D, Cox D, Pyzocha N et al. Diversity and evolution of class 2 CRISPR–Cas systems. Nat Rev Microbiol 2017; 15:169–182 [View Article] [PubMed]
     [Google Scholar]
  12. Westra ER, Levin BR. It is unclear how important CRISPR-Cas systems are for protecting natural populations of bacteria against infections by mobile genetic elements. Proc Natl Acad Sci USA 2020; 117:27777–27785 [View Article]
     [Google Scholar]
  13. Pawluk A, Davidson AR, Maxwell KL. Anti-CRISPR: discovery, mechanism and function. Nat Rev Microbiol 2018; 16:12 [View Article] [PubMed]
     [Google Scholar]
  14. Buckling A, Rainey PB. Antagonistic coevolution between a bacterium and a bacteriophage. Proceedings of the Royal Society of London Series B. Proc Biol Sci 2002; 269:931–936 [View Article] [PubMed]
     [Google Scholar]
  15. Scanlan PD, Buckling A. Co-evolution with lytic phage selects for the mucoid phenotype of Pseudomonas fluorescens SBW25. ISME J 2012; 6:1148–1158 [View Article] [PubMed]
     [Google Scholar]
  16. Scanlan PD, Hall AR, Lopez-Pascua LDC, Buckling A. Genetic basis of infectivity evolution in a bacteriophage. Mol Ecol 2011; 20:981–989 [View Article] [PubMed]
     [Google Scholar]
  17. Meyer JR, Dobias DT, Weitz JS, Barrick JE, Quick RT et al. Repeatability and contingency in the evolution of a key innovation in phage lambda. Science 2012; 335:428–432 [View Article] [PubMed]
     [Google Scholar]
  18. Fenton A, Antonovics J, Brockhurst MA. Inverse-gene-for-gene infection genetics and coevolutionary dynamics. Am Nat 2009; 174:E230–242 [View Article] [PubMed]
     [Google Scholar]
  19. Fenton A, Antonovics J, Brockhurst MA. Two-step infection processes can lead to coevolution between functionally independent infection and resistance pathways. Evolution 2012; 66:2030–2041 [View Article] [PubMed]
     [Google Scholar]
  20. Sieber M, Robb M, Forde SE, Gudelj I. Dispersal network structure and infection mechanism shape diversity in a coevolutionary bacteria-phage system. ISME J 2014; 8:504–514 [View Article]
     [Google Scholar]
  21. Agrawal A, Lively CM. Infection genetics: gene-for-gene versus matching-alleles models and all points in between. Evol Ecol Res 2002; 4:79–90
     [Google Scholar]
  22. Dennehy JJ. What can phages tell us about host-pathogen coevolution?. Int J Evol Biol 2012; 2012:396165 [View Article] [PubMed]
     [Google Scholar]
  23. Koskella B, Brockhurst MA. Bacteria-phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiol Rev 2014; 38:916–931 [View Article] [PubMed]
     [Google Scholar]
  24. Chaudhry WN, Pleška M, Shah NN, Weiss H, McCall IC et al. Leaky resistance and the conditions for the existence of lytic bacteriophage. PLoS Biol 2018; 16:e2005971 [View Article] [PubMed]
     [Google Scholar]
  25. Hofnung M, Jezierska A, Braun-Breton C. lamB mutations in E. coli K12: growth of lambda host range mutants and effect of nonsense suppressors. Mol Gen Genet 1976; 145:207–213 [View Article] [PubMed]
     [Google Scholar]
  26. Thirion JP, Hofnung M. On some genetic aspects of phage lambda resistance in E. coli K12. Genetics 1972; 71:207–216 [PubMed]
     [Google Scholar]
  27. Elliott J, Arber W. E. coli K-12 pel mutants, which block phage lambda DNA injection, coincide with ptsM, which determines a component of a sugar transport system. Mol Gen Genet 1978; 161:1–8 [View Article] [PubMed]
     [Google Scholar]
  28. Erni B, Zanolari B, Kocher HP. The mannose permease of Escherichia coli consists of three different proteins: amino acid sequence and function in sugar transport, sugar phosphorylation, and penetration of phage lambda DNA. J Biol Chem 1987; 262:5238–5247 [PubMed]
     [Google Scholar]
  29. Esquinas-Rychen M, Erni B. Facilitation of bacteriophage lambda DNA injection by inner membrane proteins of the bacterial phosphoenol-pyruvate: carbohydrate phosphotransferase system (PTS. J Mol Microbiol Biotechnol 2001; 3:361–370 [PubMed]
     [Google Scholar]
  30. Scandella D, Arber W. An Escherichia coli mutant which inhibits the injection of phage lambda DNA. Virology 1974; 58:504–513 [View Article] [PubMed]
     [Google Scholar]
  31. Spanakis E, Horne MT. Co-adaptation of Escherichia coli and coliphage λvir in continuous culture. J Gen Microbiol 1987; 133:353–360 [View Article] [PubMed]
     [Google Scholar]
  32. Meyer JR, Agrawal AA, Quick RT, Dobias DT, Schneider D et al. Parallel changes in host resistance to viral infection during 45,000 generations of relaxed selection. Evolution 2010; 64:3024–3034 [View Article] [PubMed]
     [Google Scholar]
  33. Burmeister AR, Lenski RE, Meyer JR. Host coevolution alters the adaptive landscape of a virus. Proc Roy Soc B: Biol Sci 2016; 283:20161528
     [Google Scholar]
  34. Meyer JR, Flores CO, Weitz JS, Lenski RE. Key innovation in a virus catalyzes a coevolutionary arms race. ALife Proceedings 2008; 13:532–533
     [Google Scholar]
  35. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2006; 2:0008 [View Article] [PubMed]
     [Google Scholar]
  36. Burmeister AR, Sullivan R, Lenski RE. Fitness costs and benefits of resistance to phage lambda in experimentally evolved Escherichia coli . Banzhaf W, Cheng B, Deb K, Holekamp K, Lenski RE. eds In Evolution in action: Past, present, and futuraction: Past, present, and future New York, NY: Springer; 2020 pp 123–143
     [Google Scholar]
  37. Williams N, Fox DK, Shea C, Roseman S. Pel, the protein that permits lambda DNA penetration of Escherichia coli, is encoded by a gene in ptsM and is required for mannose utilization by the phosphotransferase system. Proc Natl Acad Sci U S A 1986; 83:8934–8938 [View Article] [PubMed]
     [Google Scholar]
  38. Scandella D, Arber W. Phage lambda-DNA injection into Escherichia coli pel - mutants is restored by mutations in phage gene V or gene H . Virology 1976; 69:206–215 [View Article] [PubMed]
     [Google Scholar]
  39. Gupta A, Peng S, Leung CY, Borin JM, Weitz JS et al. Leapfrog dynamics in phage-bacteria coevolution revealed by joint analysis of cross-infection phenotypes and whole genome sequencing. bioRxiv 2020 [View Article]
     [Google Scholar]
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Sustained coevolution of phage Lambda and Escherichia coli involves inner- as well as outer-membrane defences and counter-defences
Microbiology 167, 001063 (2021); https://doi.org/10.1099/mic.0.001063
/content/journal/micro/10.1099/mic.0.001063
/content/journal/micro/10.1099/mic.0.001063
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