Population Fitness and the Regulation of Escherichia coli Genes by Bacterial Viruses

Ying Chen,Ling Guo,Satoshi Sawai,Ido Golding,Edward C Cox,Matt Waldor

doi:10.1371/journal.pbio.0030229

Abstract

Temperate bacteriophage parasitize their host by integrating into the host genome where they provide additional genetic information that confers higher fitness on the host bacterium by protecting it against invasion by other bacteriophage, by increasing serum resistance, and by coding for toxins and adhesion factors that help the parasitized bacterium invade or evade its host. Here we ask if a temperate phage can also regulate host genes. We find several different host functions that are down-regulated in lysogens. The pckA gene, required for gluconeogenesis in all living systems, is regulated directly by the principal repressor of many different temperate prophage, the cI protein. cI binds to the regulatory region of pckA, thereby shutting down pckA transcription. The pckA regulatory region has target sequences for many other temperate phage repressors, and thus we suggest that down-regulation of the host pckA pathway increases lysogen fitness by lowering the growth rate of lysogens in energy-poor environments, perhaps as an adaptive response to the host predation system or as an aspect of lysogeny that must be offset by down-regulating pckA.

Highlights

A central question in the biology of host–parasite interactions is how a balance between the costs and benefits to both is achieved
The lysogenic state imposes a cost on the bacterium because every so often the viral genome replicates and kills the host
Temperate phage may confer fitness on a host by coding for genes that enhance host virulence and resistance to the immune system [4], of which there are dozens of examples: the Shiga toxin produced by some strains of Escherichia coli; the b toxin produced by Corynebacterium diptheriae, the causative agent of diphtheria; endotoxin production by Clostridium botulinum; staphylococcal endotoxins; and cholera toxin produced by Vibrio cholerae, to name a few

Summary

Introduction

A central question in the biology of host–parasite interactions is how a balance between the costs and benefits to both is achieved. Speaking, they either invade and kill the host or they invade and lie dormant, either integrated into the host genome or outside it as extrachromosomal elements [1]. The lysogenic state imposes a cost on the bacterium because every so often the viral genome (prophage) replicates and kills the host. This selective disadvantage is offset, in several important ways. Because prophage produce a repressor that keeps the prophage genes from being expressed, the host bacterium enjoys immunity from lytic infection by temperate family members. There are several advantages to being a lysogen, and at least one big disadvantage: Occasionally the prophage replicates and kills the host

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Conclusion