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The transcriptional regulator CtrA controls gene expression in Alphaproteobacteria phages: Evidence for a lytic deferment pathway

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dc.contributor.authorMascolo, Elia
dc.contributor.authorAdhikari, Satish
dc.contributor.authorCaruso, Steven M.
dc.contributor.authordeCarvalho, Tagide
dc.contributor.authorSalvador, Anna Folch
dc.contributor.authorSerra-Sagristà, Joan
dc.contributor.authorYoung, Ry
dc.contributor.authorErill, Ivan
dc.contributor.authorCurtis, Patrick D.
dc.date.accessioned2023-04-11T19:50:23Z
dc.date.available2023-04-11T19:50:23Z
dc.date.issued2022-08-19
dc.description.abstractPilitropic and flagellotropic phages adsorb to bacterial pili and flagella. These phages have long been used to investigate multiple aspects of bacterial physiology, such as the cell cycle control in the Caulobacterales. Targeting cellular appendages for adsorption effectively constrains the population of infectable hosts, suggesting that phages may have developed strategies to maximize their infective yield. Brevundimonas phage vB_BsubS-Delta is a recently characterized pilitropic phage infecting the Alphaproteobacterium Brevundimonas subvibrioides. Like other Caulobacterales, B. subvibrioides divides asymmetrically and its cell cycle is governed by multiple transcriptional regulators, including the master regulator CtrA. Genomic characterization of phage vB_BsubS-Delta identified the presence of a large intergenic region with an unusually high density of putative CtrA-binding sites. A systematic analysis of the positional distribution of predicted CtrA-binding sites in complete phage genomes reveals that the highly skewed distribution of CtrA-binding sites observed in vB_BsubS-Delta is an unequivocal genomic signature that extends to other pilli- and flagellotropic phages infecting the Alphaproteobacteria. Moreover, putative CtrA-binding sites in these phage genomes localize preferentially to promoter regions and have higher scores than those detected in other phage genomes. Phylogenetic and comparative genomics analyses show that this genomic signature has evolved independently in several phage lineages, suggesting that it provides an adaptive advantage to pili/flagellotropic phages infecting the Alphaproteobacteria. Experimental results demonstrate that CtrA binds to predicted CtrA-binding sites in promoter regions and that it regulates transcription of phage genes in unrelated Alphaproteobacteria-infecting phages. We propose that this focused distribution of CtrA-binding sites reflects a fundamental new aspect of phage infection, which we term lytic deferment. Under this novel paradigm, pili- and flagellotropic phages exploit the CtrA transduction pathway to monitor the host cell cycle state and synchronize lysis with the presence of infectable cells.en_US
dc.description.sponsorshipPhylogenetic inference computations were performed using the UMBC High Performance Computing Facility (HPCF). The facility is supported by the US National Science Foundation through the MRI program (CNS-0821258, CNS-1228778 and OAC-1726023) and the SCREMS program (DMS-08215311), with additional support from the University of Maryland, Baltimore County (UMBC). Sequencing was carried out with support from the Center for Phage Technology, sponsored jointly by the Texas A&M AgriLife and the office of the Vice President for Research at Texas A&M University. Anurag Rijal provided critical aid to the phage EMSA experiments. This work was funded in part by the United States National Science Foundation CAREER program award 1552647 to PC, and by grant NIH R35 GM136396 to RY. EM was supported by the UMBC Department of Biological Sciences.en_US
dc.description.urihttps://www.frontiersin.org/articles/10.3389/fmicb.2022.918015/fullen_US
dc.format.extent21 pagesen_US
dc.genrejournal articlesen_US
dc.identifierdoi:10.13016/m2u6cu-zgsx
dc.identifier.citationMascolo E, Adhikari S, Caruso SM, deCarvalho T, Folch Salvador A, Serra-Sagristà J, Young R, Erill I and Curtis PD. "The transcriptional regulator CtrA controls gene expression in Alphaproteobacteria phages: Evidence for a lytic deferment pathway" Front. Microbiol. 13, 918015 (19 August, 2022). https://doi.org/10.3389/fmicb.2022.918015.en_US
dc.identifier.urihttps://doi.org/10.3389/fmicb.2022.918015
dc.identifier.urihttp://hdl.handle.net/11603/27585
dc.language.isoen_USen_US
dc.publisherFrontiersen_US
dc.relation.isAvailableAtThe University of Maryland, Baltimore County (UMBC)
dc.relation.ispartofUMBC Biological Sciences Department Collection
dc.relation.ispartofUMBC Keith R. Porter Imaging Facility
dc.relation.ispartofUMBC Faculty Collection
dc.relation.ispartofUMBC Student Collection
dc.relation.ispartofUMBC Computer Science and Electrical Engineering Department
dc.rightsThis item is likely protected under Title 17 of the U.S. Copyright Law. Unless on a Creative Commons license, for uses protected by Copyright Law, contact the copyright holder or the author.en_US
dc.rightsAttribution 4.0 International (CC BY 4.0)*
dc.rights.urihttps://creativecommons.org/licenses/by/4.0/*
dc.subjectUMBC High Performance Computing Facility (HPCF)
dc.titleThe transcriptional regulator CtrA controls gene expression in Alphaproteobacteria phages: Evidence for a lytic deferment pathwayen_US
dc.typeTexten_US
dcterms.creatorhttps://orcid.org/0000-0003-2977-7844en_US
dcterms.creatorhttps://orcid.org/0000-0001-9166-9137en_US
dcterms.creatorhttps://orcid.org/0000-0003-0774-3096en_US
dcterms.creatorhttps://orcid.org/0000-0002-7280-7191en_US

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