Transcriptome analyses of cells carrying the Type II Csp231I restriction–modification system reveal cross-talk between two unrelated transcription factors: C protein and the Rac prophage repressor

Alessandro Negri , Marcin Jąkalski , Aleksandra Szczuka , Leszek Pryszcz , Iwona Mruk

Abstract

Restriction-modification (R–M) systems represent an effective mechanism of defence against invading bacteriophages, and are widely spread among bacteria and archaea. In acquiring a Type II R–M system via horizontal gene transfer, the new hosts become more resistant to phage infection, through the action of a restriction endonuclease (REase), which recognizes and cleaves specific target DNAs. To protect the host cell's DNA, there is also a methyltransferase (MTase), which prevents DNA cleavage by the cognate REase. In some R–M systems, the host also accepts a cis-acting transcription factor (C protein), which regulates the counteracting activities of REase and MTase to avoid host self-restriction. Our study characterized the unexpected phenotype of Escherichia coli cells, which manifested as extensive cell filamentation triggered by acquiring the Csp231I R–M system from Citrobacter sp. Surprisingly, we found that the cell morphology defect was solely dependent on the C regulator. Our transcriptome analysis supported by in vivo and in vitro assays showed that C protein directly silenced the expression of the RacR repressor to affect the Rac prophage-related genes. The rac locus ydaST genes, when derepressed, exerted a toxicity indicated by cell filamentation through an unknown mechanism. These results provide an apparent example of transcription factor cross-talk, which can have significant consequences for the host, and may represent a constraint on lateral gene transfer.
Author Alessandro Negri (FB/DM)
Alessandro Negri,,
- Department of Microbiology
, Marcin Jąkalski (FB/DPTNC)
Marcin Jąkalski,,
- Department of Plant Taxonomy and Nature Conservation
, Aleksandra Szczuka (FB/DM)
Aleksandra Szczuka,,
- Department of Microbiology
, Leszek Pryszcz
Leszek Pryszcz,,
-
, Iwona Mruk (FB/DM)
Iwona Mruk,,
- Department of Microbiology
Journal seriesNucleic Acids Research, ISSN 0305-1048, (N/A 200 pkt)
Issue year2019
Vol47
No18
Pages9542-9556
Publication size in sheets0.70
Keywords in Englishrestriction-modification systems, transcription factor crosstalk, transcription regulation, cell filamentation
ASJC Classification1311 Genetics
DOIDOI:10.1093/nar/gkz665
URL https://doi.org/10.1093/nar/gkz665
Languageen angielski
LicenseJournal (articles only); published final; Uznanie Autorstwa - Użycie Niekomercyjne (CC-BY-NC); with publication
Score (nominal)200
Score sourcejournalList
ScoreMinisterial score = 200.0, 28-01-2020, ArticleFromJournal
Publication indicators WoS Citations = 0.000; Scopus SNIP (Source Normalised Impact per Paper): 2016 = 2.657; WoS Impact Factor: 2018 = 11.147 (2) - 2018=10.727 (5)
Citation count*1 (2020-07-28)
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