Endolysin Regulation in Phage Mu Lysis

Chamblee, Jake S; Ramsey, Jolene; Chen, Yi; Maddox, Lori T; Ross, Curtis; To, Kam H.; Cahill, Jesse; Young, Ry

doi:10.1128/mbio.00813-22

Cited by 10 publications

(11 citation statements)

References 67 publications

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“…Endolysin belongs to a class of cell wall hydrolases encoded by double-stranded DNA phages. The expression of endolysin occurs in the later stages of phage infection and plays a role in the life history strategy of vB_SbaS_Y11, which involves lysing the host cell wall to release daughter phages ( 19 ). ORF22 is predicted to encode protease.…”

Section: Resultsmentioning

confidence: 99%

Shewanella phage encoding a putative anti-CRISPR-like gene represents a novel potential viral family

Wang,

Zheng,

Wang

et al. 2024

Microbiol Spectr

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Shewanella is a prevalent bacterial genus in deep-sea environments including marine sediments, exhibiting diverse metabolic capabilities that indicate its significant contributions to the marine biogeochemical cycles. However, only a few Shewanella phages were isolated and deposited in the NCBI database. In this study, we report the isolation and characterization of a novel Shewanella phage, vB_SbaS_Y11, that infects Shewanella KR11 and was isolated from the sewage in Qingdao, China. Transmission electron microscopy revealed that vB_SbaS_Y11 has an icosahedral head and a long tail. The genome of vB_SbaS_Y11 is a linear, double-stranded DNA with a length of 62,799 bp and a G+C content of 46.9%, encoding 71 putative open reading frames. No tRNA genes or integrase-related feature genes were identified. An uncharacterized anti-CRISPR AcrVA2 gene was detected in its genome. Phylogenetic analysis based on the amino acid sequences of whole genomes and comparative genomic analyses indicate that vB_SbaS_Y11 has a novel genomic architecture and shares low similarity to Pseudomonas virus H66 and Pseudomonas phage F116. vB_SbaS_Y11 represents a potential new family-level virus cluster with eight metagenomic assembled viral genomes named Ranviridae . IMPORTANCE The Gram-negative Shewanella bacterial genus currently includes about 80 species of mostly aquatic Gammaproteobacteria , which were isolated around the globe in a multitude of environments, such as freshwater, seawater, coastal sediments, and the deepest trenches. Here, we present a Shewanella phage vB_SbaS_Y11 that contains an uncharacterized anti-CRISPR AcrVA2 gene and belongs to a potential virus family, Ranviridae . This study will enhance the knowledge about the genome, diversity, taxonomic classification, and global distribution of Shewanella phage populations.

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Section: Resultsmentioning

confidence: 99%

Shewanella phage encoding a putative anti-CRISPR-like gene represents a novel potential viral family

Wang,

Zheng,

Wang

et al. 2024

Microbiol Spectr

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“…The lytic module of Phm3 belongs to Group I and contains four proteins, ORF41-ORF44 ( Figs 4B and S5A ). ORF41 encodes an endolysin protein that harbours a conserved EGGY motif near the N-terminus, and the glutamic acid within this motif is essential for catalytic activity [ 63 ]. Additionally, endolysins have no signal sequence ( Fig.…”

Section: Resultsmentioning

confidence: 99%

Active prophages in coral-associated Halomonas capable of lateral transduction

Liu,

Tang,

Zhou

et al. 2024

The ISME Journal

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Temperate phages can interact with bacterial hosts through lytic and lysogenic cycles via different mechanisms. Lysogeny has been identified as the major form of bacteria-phage interaction in the coral-associated microbiome. However, the lysogenic-to-lytic switch of temperate phages in ecologically important coral-associated bacteria and its ecological impact have not been extensively investigated. By studying the prophages in coral-associated Halomonas meridiana, we found that two prophages, Phm1 and Phm3, are inducible by the DNA-damaging agent mitomycin C and that Phm3 is spontaneously activated under normal cultivation conditions. Furthermore, Phm3 undergoes an atypical lytic pathway that can amplify and package adjacent host DNA, potentially resulting in lateral transduction. The induction of Phm3 triggered a process of cell-lysis accompanied by the formation of outer membrane vesicles (OMVs), and Phm3 attached to OMVs. This unique cell-lysis process was controlled by a four-gene lytic module within Phm3. Further analysis of the Tara Ocean dataset revealed that Phm3 represents a new group of temperate phages that are widely distributed and transcriptionally active in the ocean. Therefore, the combination of lateral transduction mediated by temperate phages and OMV transmission offers a versatile strategy for host-phage co-evolution in marine ecosystems.

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“…Instead, this phage employs a membrane-localized DUF2730 protein, which was accordingly designated releasin. The mechanism by which releasin acts is not completely clear but it is proposed that the protein directly or indirectly neutralizes the positive charges at the cytoplasmic face of the endolysin’s transmembrane domain, e. g., by removal through endolytic cleavage or formation of a hydrophylic channel (16). Lcc6 does not exhibit notable homologies to the Mu releasin gp25, does not have a DUF2730 domain and is also shorter.…”

Section: Discussionmentioning

confidence: 99%

“…Chamblee et al (16) recently identified the long missing protein that allows the SAR-endolysin of E. coli phage Mu to be released and activated, as this phage lacks a holin system. Instead, this phage employs a membrane-localized DUF2730 protein, which was accordingly designated releasin.…”

Section: Lcc6 a Novel Player In Phage-induced Lysismentioning

confidence: 99%

“…Some phages, such as E. coli phage Lambda (13), also produce antiholins, which can regulate timing of lysis initiation (14, 15). Some phages lack holins, such as Escherichia coli phage Mu, which instead uses a so-called releasin, a CM-tethered protein, to sever the association of the corresponding SAR endolysin with the membrane (16). Other phages lysing Gram-negatives do not possess apparent spanins.…”

Section: Introductionmentioning

confidence: 99%

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Identifying the components of theShewanellaphage LambdaSo lysis system

Thöneböhn,

Fischer,

Kreiling

et al. 2024

Preprint

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Phage-induced lysis of Gram-negative bacterial hosts usually requires a set of phage lysis proteins, a holin, an endopeptidase and a spanin system, to disrupt each of the three cell envelope layers. Genome annotations and previous studies identified a gene region in theShewanella oneidensisprophage LambdaSo, which comprises potential holin- and endolysin-encoding genes but lacks an obvious spanin system. By a combination of candidate approaches, mutant screening, characterization and microscopy we found that LambdaSo uses a pinholin/signal-anchor-release (SAR) endolysin system to induce proton-leakage and degradation of the cell wall. Between the corresponding genes we found that two extensively nested open reading frames encode a two-component spanin module Rz/Rz1. Unexpectedly, we identified another factor strictly required for LambdaSo-induced cell lysis, the phage protein Lcc6. Lcc6 is a transmembrane protein of 65 amino acid residues with hitherto unknown function, which acts at the level of holin in the cytoplasmic membrane to allow endolysin release. Thus, LambdaSo-mediated cell lysis requires at least four protein factors (pinholin, SAR-endolysin, spanin, Lcc6). The findings further extend the known repertoire of phage proteins involved in host lysis and phage egress.

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Endolysin Regulation in Phage Mu Lysis

Abstract: Host cell lysis is the terminal event of the bacteriophage infection cycle. In Gram-negative hosts, lysis requires proteins that disrupt each of the three cell envelope components, only one of which has been identified in Mu: the endolysin gp22.

Cited by 10 publications

References 67 publications

Shewanella phage encoding a putative anti-CRISPR-like gene represents a novel potential viral family

Shewanella phage encoding a putative anti-CRISPR-like gene represents a novel potential viral family

Active prophages in coral-associated Halomonas capable of lateral transduction

Identifying the components of theShewanellaphage LambdaSo lysis system

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