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An Lsr2-like xenogeneic silencer confers immunity against AT-rich bacteriophage infection

ABSTRACT: Lsr2-like xenogeneic silencers are widespread nucleoid-associated proteins in Actinomycetota and are encoded by diverse bacteriophages. However, their potential roles during bacteriophage infection, one of the most direct encounters with foreign DNA, remain unexplored. In Corynebacterium glutamicum, the Lsr2-like protein CgpS is encoded within the mobile genetic element CGP3 and is known to silence transcription of foreign DNA within this region. Here we show that CgpS also restricts infection by the AT-rich bacteriophage Jean Grey. Upon phage DNA injection, CgpS binds phage-derived AT-rich sequences and represses early phage gene transcription. This transcriptional bottleneck prevents efficient phage genome replication and delays progression of the viral program. The resulting temporal window enables activation of host stress and defense pathways, including LexA-regulated SOS genes and additional antiviral systems. Our findings reveal a novel antiviral function for an Lsr2-like silencer and suggest that xenogeneic silencers can act as regulatory barriers that modulate the outcome of phage infection in Actinomycetota.

INSTRUMENT(S):

ORGANISM(S): Corynebacterium Glutamicum Mb001

SUBMITTER: Konstantinos Kalogeropoulos

LAB HEAD: Konstantinos Kalogeropoulos

PROVIDER: PXD075760 | Pride | 2026-03-21

REPOSITORIES: Pride

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			Action	DRS
	20251211_MH_ELBE_KK_FAIMS_1CV_uPAC50_38min_1475_DIA_NP10.raw	Raw
	20251211_MH_ELBE_KK_FAIMS_1CV_uPAC50_38min_1475_DIA_NP10.raw.quant	Raw
	20251211_MH_ELBE_KK_FAIMS_1CV_uPAC50_38min_1475_DIA_NP11.raw	Raw
	20251211_MH_ELBE_KK_FAIMS_1CV_uPAC50_38min_1475_DIA_NP11.raw.quant	Raw
	20251211_MH_ELBE_KK_FAIMS_1CV_uPAC50_38min_1475_DIA_NP12.raw	Raw

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Project description:Bacteriophage infection of Lactococcus lactis strains used in the manufacture of fermented milk products is a major threat for the dairy industry. A greater understanding of the global molecular response of the bacterial host following phage infection has the potential to identify new targets for the design of phage control measures for biotechnological processes. In this study, we have used whole-genome oligonucleotide microarrays to gain insights into the genomic intelligence driving the instinctive response of L. lactis subsp. lactis IL1403 to the onset of a challenge with the lytic prolate-headed phage c2. Following phage adsorption, the bacterium differentially regulated the expression of 61 genes belonging to 14 functional categories, and mostly to cell envelope (12 genes), regulatory functions (11 genes), and carbohydrate metabolism (7 genes). The nature of the differentially regulated genes suggests the orchestration of a complex response involving induction of cell envelope stress proteins, D-alanylation of cell-wall lipoteichoic acids (LTAs), restoration of the proton motive force (PMF), and energy conservation. Increased D-alanylation of LTAs would act as an adsorption blocking mechanism, which we speculate may allow the survival of a small percent of the cell population when facing more realistic in vivo low titer-phage attacks. The modification of LTAs decoration in response to phage c2 adsorption also suggests these cell wall structures as possible primary receptors for this phage. Restoration of a physiological PMF is achieved by regulating the expression of genes affecting the two main components of the PMF, and serves to reverse a drastic depolarization of the host membrane caused by phage adsorption. Down-regulation of energy-consuming metabolic activities and a switch to anaerobic respiration helps the bacterium to save energy in order to sustain the PMF and the overall response to phage. We finally propose that the overall transcriptional response of L. lactis IL1403 to the phage stimuli is orchestrated by the concerted action of Phage Shock Proteins and of the bivalent transcriptional regulator SpxB following activation by the two-component system CesSR. To our knowledge, this represents the first detailed description in L. lactis, and probably in Gram-positive bacteria, of the molecular mechanisms involved in the host response to the membrane perturbation mediated by phage adsorption. Two-condition experiment: IL1403 vs. Bacteriophage c2-infected IL1403 cells. Biological replicates: 2 controls, 2 infected, independently grown and harvested. Two technical replicates per array.

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An Lsr2-like xenogeneic silencer confers immunity against AT-rich bacteriophage infection

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