Sustained coevolution of phage Lambda and Escherichia coli involves inner- as well as outer-membrane defences and counter-defences.

Alita R Burmeister,Rachel M Sullivan,Richard E Lenski,Jenna Gallie

doi:10.1099/mic.0.001063

Abstract

Bacteria often evolve resistance to phage through the loss or modification of cell surface receptors. In Escherichia coli 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 E. coli evolves mutations in mannose permease-encoding genes manY and manZ that impair λ’s ability to eject its DNA into the cytoplasm. We show that these man 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 man 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.

Highlights

An issue of longstanding interest is whether the coevolution of bacteria and virulent phages involves endless rounds of bacterial defences and phage counter-defences
Based on experiments in chemostats, Lenski and Levin [1] suggested that bacteria typically had the upper hand, as Escherichia coli often eventually evolved resistance by deleting or inactivating the phage’s specific receptor, which the phage could not readily overcome
Lenski and Levin pointed out that bacteria would lose the upper hand if the phage targeted a receptor that was essential for the bacteria to survive in their current environment

Summary

Introduction

An issue of longstanding interest is whether the coevolution of bacteria and virulent (lytic) phages involves endless rounds of bacterial defences and phage counter-defences. Some of the phage populations evolved the ability to use the outer-membrane protein OmpF as a receptor, some of the bacterial populations evolved mutations that affected mannose metabolism and some communities changed in both respects.

Results

Conclusion