A window into lysogeny: revealing temperate phage biology with transcriptomics.

Siân V Owen,Nicolas Wenner,Rocío Canals,Jay C D Hinton,Carsten Kröger,Disa L Hammarlöf

doi:10.1099/mgen.0.000330

Siân V Owen, Nicolas Wenner + Show 4 more

Open Access

https://doi.org/10.1099/mgen.0.000330

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Abstract

Prophages are integrated phage elements that are a pervasive feature of bacterial genomes. The fitness of bacteria is enhanced by prophages that confer beneficial functions such as virulence, stress tolerance or phage resistance, and these functions are encoded by ‘accessory’ or ‘moron’ loci. Whilst the majority of phage-encoded genes are repressed during lysogeny, accessory loci are often highly expressed. However, it is challenging to identify novel prophage accessory loci from DNA sequence data alone. Here, we use bacterial RNA-seq data to examine the transcriptional landscapes of five Salmonella prophages. We show that transcriptomic data can be used to heuristically enrich for prophage features that are highly expressed within bacterial cells and represent functionally important accessory loci. Using this approach, we identify a novel antisense RNA species in prophage BTP1, STnc6030, which mediates superinfection exclusion of phage BTP1. Bacterial transcriptomic datasets are a powerful tool to explore the molecular biology of temperate phages.

Highlights

Temperate bacteriophages can integrate into the genome of host bacteria, and persist as vertically inherited genomic elements known as prophages
The S. enterica serovar Typhimurium strain D23580 is a representative of the sequence type (ST) 313 lineage 2, which is currently responsible for the epidemic of invasive non- typhoidal salmonellosis in Africa [33]
Because the transcriptome data generated by RNA-seq represents the mean gene expression across an entire bacterial population, we propose that the apparent low-level expression of lytic genes reflects extremely high-level transcription of lytic genes within the fraction of the population in which the BTP1 prophage is spontaneously induced

Summary

Introduction

Temperate bacteriophages can integrate into the genome of host bacteria (lysogeny), and persist as vertically inherited genomic elements known as prophages. The majority of the temperate phage genome encodes proteins dedicated to virion production and host cell lysis, functions that are toxic to bacterial cells. To exist stably as passive genomic elements, the expression of the majority of prophage genes must be repressed at the transcriptional level. Those functions necessary to maintain and favour lysogeny are expressed. Molecular studies investigating the gene expression of phage lambda lysogens showed that four additional lambda genes are expressed from the integrated prophage genome during lysogenic growth: the rexAB operon, encoding a superinfection immunity system; and the lom and bor genes, which encode virulence factors [2,3,4,5,6]

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