Lytic Infection of Lactococcus lactis by Bacteriophages Tuc2009 and c2 Triggers Alternative Transcriptional Host Responses

Abstract

Here we present an entire temporal transcriptional profile of Lactococcus lactis subsp. cremoris UC509.9 undergoing lytic infection with two distinct bacteriophages, Tuc2009 and c2. Furthermore, corresponding high-resolution whole-phage genome tiling arrays of both bacteriophages were performed throughout lytic infection. Whole-genome microarrays performed at various time points postinfection demonstrated a rather modest impact on host transcription. The majority of changes in the host transcriptome occur during late infection stages; few changes in host gene transcription occur during the immediate and early infection stages. Alterations in the L. lactis UC509.9 transcriptome during lytic infection appear to be phage specific, with relatively few differentially transcribed genes shared between cells infected with Tuc2009 and those infected with c2. Despite the apparent lack of a coordinated general phage response, three themes common to both infections were noted: alternative transcription of genes involved in catabolic flux and energy production, differential transcription of genes involved in cell wall modification, and differential transcription of genes involved in the conversion of ribonucleotides to deoxyribonucleotides. The transcriptional profiles of both bacteriophages during lytic infection generally correlated with the findings of previous studies and allowed the confirmation of previously predicted promoter sequences. In addition, the host transcriptional response to lysogenization with Tuc2009 was monitored along with tiling array analysis of Tuc2009 in the lysogenic state. Analysis identified 44 host genes with altered transcription during lysogeny, 36 of which displayed levels of transcription significantly reduced from those for uninfected cells.

Stress Physiology of Lactic Acid Bacteria

“…This is believed to be orchestrated by the action of membrane-associated, phage shock-mediated protein C-like homologs, the global regulator SpxB, and the two-component regulatory system CesSR (572). Analysis of the host transcriptome response to infection by the lactococcal phages Tuc2009 and c2 revealed the induction of genes involved in metabolic flux and energy production, in cell wall modification, and in the conversion of ribonucleotides to deoxyribonucleotides (572,573).…”

Global Transcriptional Response of Clostridium difficile Carrying the ϕCD38-2 Prophage

“…coli and other species during a productive lytic infection, and multiple proteins have been shown to interfere with transcription, translation, or DNA replication (2,(21)(22)(23)(24)(25). On the other hand, phage-host interactions during lysogeny and the influence of prophages on host genes have not been investigated extensively (3,4,25,26).…”

“…Another good example is the botulinum toxin encoded by Clostridium botulinum phages CE␤ and CE␥ (17). Yet some phages express membrane-associated or periplasmic proteins, such as Imm encoded by the Escherichia coli phage T4 (18) or LTP encoded by the S. thermophilus phage TP-J34 (19), that function as phage superinfection exclusion systems (for a review, see reference 20).Phage-host interactions have been extensively studied for E.coli and other species during a productive lytic infection, and multiple proteins have been shown to interfere with transcription, translation, or DNA replication (2,(21)(22)(23)(24)(25). On the other hand, phage-host interactions during lysogeny and the influence of prophages on host genes have not been investigated extensively (3,4,25,26).…”

Lack of the host membrane protease FtsH hinders release of the Lactococcus lactis bacteriophage TP712

“…Clustered regularly interspaced short palindromic repeats (CRISPRs) located in the genomes of host bacteria together with a group of associated proteins can also confer resistance to phages (Labrie et al, 2010). Recently, the response to phage infection in L. lactis has been approached by genome-wide transcriptomics (Fallico et al, 2011;Ainsworth et al, 2013). L. lactis appears to sense bacteriophage infection as a perturbation of its cell envelope and mounts a response targeted to the cell wall, activating regulators of the cell envelope stress response such as the two-component system CesSR.…”