Active Lysogeny in Listeria Monocytogenes Is a Bacteria-Phage Adaptive Response in the Mammalian Environment

Abstract

Summary Some Listeria monocytogenes ( Lm ) strains harbor a prophage within the comK gene, which renders it inactive. During Lm infection of macrophage cells, the prophage turns into a molecular switch, promoting comK gene expression and therefore Lm intracellular growth. During this process, the prophage does not produce infective phages or cause bacterial lysis, suggesting it has acquired an adaptive behavior suited to the pathogenic lifestyle of its host. In this study, we demonstrate that this non-classical phage behavior, named active lysogeny, relies on a transcriptional response that is specific to the intracellular niche. While the prophage undergoes lytic induction, the process is arrested midway, preventing the transcription of the late genes. Further, we demonstrate key phage factors, such as LlgA transcription regulator and a DNA replicase, that support the phage adaptive behavior. This study provides molecular insights into the adaptation of phages to their pathogenic hosts, uncovering unusual cooperative interactions.

Phenotypic Characterization and Whole-Genome Analysis of a Novel Bacteriophage HCF1 Infecting Citrobacter amalonaticus and C. freundii

“…Putative antirepressor and transcriptional regulator in bacteriophage HCF1 genome indicates the presence of a mechanism for decrease in the transcription of early genes and increase in the transcription of late genes. Recently, it has been established that late gene activation promotes the lytic pathway and the early gene activation plays a role in active lysogeny ( Pasechnek et al, 2020 ). In addition, no ORFs were identified corresponding to excisionase, integrase, or repressor genes in the genome of HCF1.…”

An Efficient, Counter-Selection-Based Method for Prophage Curing in Pseudomonas aeruginosa Strains

“…The principle of the method and the high observed efficiency gives a better understanding of prophage–host interactions. The prophage-excision event mostly attributed to the phage disadvantage for staying integrated [ 37 ] or regulated by the host for a temporary extra-chromosomal state (active lysogeny) [ 38 ], but here, we showed that under certain conditions, when the prophage’s contents endanger the host, it would prefer to lose the whole prophage rather than the specific risk-containing region. This fact emphasizes the need for curing rather than deletion methods for such regions.…”

Mobile elements habouring heavy metal and bacitracin resistance cassettes are common amongListeria monocytogenespersisting on dairy farms

“…Prophages inserted into comK and tRNA genes were assigned to genera of Siphoviridae that are known to only infect Listeria . Surprisingly, in the isolate HC189, a 67 Kb Myovirus was inserted into comK , a site usually occupied by Siphoviridae (Pasechnek et al, 2020).…”

“…There is increasing evidence that prophages can mediate beneficial phenotypes for their host. Phages mediate resistance or virulence properties in numerous bacterial species (Harrison & Brockhurst, 2017), and in Listeria , Siphoviruses inserted into comK were found to regulate the gene in a symbiotic manner (Pasechnek et al 2020). Here, we discovered phage-mediated carriage of cadmium resistance and various antimicrobials in Listeria , suggesting that prophages contribute to the spread of phenotypes supporting persistence.…”