Analysis of six prophages in Lactococcus lactis IL1403: different genetic structure of temperate and virulent phage populations

Chopin, Alain; Bolotin, Alexander; Sorokin, Alexeï; Ehrlich, S. Dusko; Chopin, Marie-Christine

doi:10.1093/nar/29.3.644

Cited by 161 publications

(150 citation statements)

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“…bIL170 belongs to the 936 group of lactococcal phages, known to contain only virulent phages that are closely related as observed by DNA hybridization experiments (Jarvis et al, 1991). The c2 group has the same features, whereas the P335 group A.-M. Crutz-Le Coq and others contains mainly temperate phages that are not necessarily closely related at the DNA sequence level (Chopin et al, 2001). In the 936 group, only a few genomic segments (essentially encoding the holin, lysin, major structural protein, structure-specific endonuclease and ori fragment) have been studied experimentally (Bidnenko et al, 1998 ;Chandry et al, 1997 ;Chung et al, 1991 ;Kim & Batt, 1991a).…”

Section: Phages Ofmentioning

confidence: 99%

“…gpl12 is also related, but only by its V domain, to other putative fibres (family III) from streptococcal and P335-type lactococcal phages, as well as to minor structural proteins (not localized) from lactococcal phages of the c2 group (Lubbers et al, 1995). Family III is the most heterogeneous and comprises large multi-domain proteins with collagen-type motifs (repetitions of GXX), reminiscent of the long tail fibres of coliphages by their mosaic organization and assumed to be involved in host specificity (Boyce et al, 1995 ;Chopin et al, 2001 ;Lucchini et al, 1999 ;Tremblay & Moineau, 1999). Whether they are indeed fibres remains to be determined experimentally but their direct involvement in hostrange determination was recently demonstrated for gp18 of phage DT1 (Duplessis & Moineau, 2001).…”

Section: Modular Structural Proteinsmentioning

confidence: 99%

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Sequence analysis of the lactococcal bacteriophage bIL170: insights into structural proteins and HNH endonucleases in dairy phages The GenBank/EMBL/DDBJ accession numbers for the sequences reported in this paper are bIL170, AF009630; bIL120, AY054975; bIL15, AY054976; bIL191, AY054977; bIL77, AY054978.

et al. 2002

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The complete 31 754 bp genome of bIL170, a virulent bacteriophage of Lactococcus lactis belonging to the 936 group, was analysed. Sixty-four ORFs were predicted and the function of 16 of them was assigned by significant homology to proteins in databases. Three putative homing endonucleases of the HNH family were found in the early region. An HNH endonuclease with zinc-binding motif was identified in the late cluster, potentially being part of the same functional module as terminase. Three putative structural proteins were analysed in detail and show interesting features among dairy phages. Notably, gpl12 (putative fibre) and gpl20 (putative baseplate protein) of bIL170 are related by at least one of their domains to a number of multidomain proteins encoded by lactococcal or streptococcal phages. A 110-to 150-aa-long hypervariable domain flanked by two conserved motifs of about 20 aa was identified. The analysis presented here supports the participation of some of these proteins in host-range determination and suggests that specific adsorption to the host may involve a complex multi-component system. Divergences in the genome of phages of the 936 group, that may have important biological properties, were noted. Insertions/deletions of units of one or two ORFs were the main source of divergence in the early clusters of the two entirely sequenced phages, bIL170 and sk1. An exchange of fragments probably affected the regions containing the putative origin of replication. It led to the absence in bIL170 of the direct repeats recognized in sk1 and to the presence of different ORFs in the ori region. Shuffling of protein domains affected the endolysin (putative cell-wall binding part), as well as gpl12 and gpl20.

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Section: Phages Ofmentioning

confidence: 99%

Section: Modular Structural Proteinsmentioning

confidence: 99%

Sequence analysis of the lactococcal bacteriophage bIL170: insights into structural proteins and HNH endonucleases in dairy phages The GenBank/EMBL/DDBJ accession numbers for the sequences reported in this paper are bIL170, AF009630; bIL120, AY054975; bIL15, AY054976; bIL191, AY054977; bIL77, AY054978.

et al. 2002

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“…These modules typically specify a single strand binding protein and a putative replisome organizer (bIL285, BK5-T, TP901-1, and Tuc2009), a DnaC analog and a putative replisome organizer (r1t and bIL309), or all three genes (bIL286). They are located in the same region within the genomes of these temperate bacteriophages (7,10). Most putative replisome organizers described in lactococcal bacteriophages contain a set of direct repeats structurally similar to iteron-containing origins of replication.…”

Section: Vol 76 2002mentioning

confidence: 99%

Characterization of the Putative Replisome Organizer of the Lactococcal Bacteriophage r1t

Zúñiga

Franke-Fayard

Venema

et al. 2002

J Virol

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Analysis of the nucleotide sequence of the genome of the lactococcal bacteriophage r1t showed that it may encode at least two proteins involved in DNA replication. On the basis of its similarity with the G38P protein encoded by the Bacillus subtilis phage SPP1, the product of orf11 (Pro11) is thought to be involved in the initiation of phage DNA replication. This protein was overexpressed in Lactococcus lactis and partially purified. Gel retardation analysis using various r1t DNA fragments indicates that Pro11 specifically binds to a sequence located within its cognate gene. DNase I footprinting showed that Pro11 protects a stretch of DNA of 47 bp. This region spans four 6-bp short direct repeats, which suggests that the region contains four binding sites for Pro11. 1,10-Phenanthroline-copper footprinting confirmed the protection of the hexamers. An asymmetric protection pattern of each strand was observed, suggesting that Pro11 contacts each DNA strand separately at contiguous hexamers. We propose a model for the binding of Pro11 to its target sites that may account for the torsion strain required for strand opening at the origin of replication.

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“…To investigate this possibility in more detail for Sfi21-like Siphoviridae, we included further Sfi21-like phage genome sequences (S. thermophilus phage 7201 [51], Lactobacillus casei phage A2 [27,28,33,46], and three L. lactis prophages [16]) into the comparative analysis. The analysis corroborated the proposal of a new Sfi21-like phage genus in lactic acid bacteria, yet the trend for a coevolution of phages and their host bacteria was not confirmed.…”

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confidence: 99%

The Dilemma of Phage Taxonomy Illustrated by Comparative Genomics of Sfi21-LikeSiphoviridaein Lactic Acid Bacteria

et al. 2002

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The complete genome sequences of two dairy phages, Streptococcus thermophilus phage 7201 and Lactobacillus casei phage A2, are reported. Comparative genomics reveals that both phages are members of the recently proposed Sfi21-like genus of Siphoviridae, a widely distributed phage type in low-GC-content gram-positive bacteria. Graded relatedness, the hallmark of evolving biological systems, was observed when different Sfi21-like phages were compared. Across the structural module, the graded relatedness was represented by a high level of DNA sequence similarity or protein sequence similarity, or a shared gene map in the absence of sequence relatedness. This varying range of relatedness was found within Sfi21-like phages from a single species as demonstrated by the different prophages harbored by Lactococcus lactis strain IL1403. A systematic dot plot analysis with 11 complete L. lactis phage genome sequences revealed a clear separation of all temperate phages from two classes of virulent phages. The temperate lactococcal phages share DNA sequence homology in a patchwise fashion over the nonstructural gene cluster. With respect to structural genes, four DNA homology groups could be defined within temperate L. lactis phages. Closely related structural modules for all four DNA homology groups were detected in phages from Streptococcus or Listeria, suggesting that they represent distinct evolutionary lineages that have not uniquely evolved in L. lactis. It seems reasonable to base phage taxonomy on data from comparative genomics. However, the peculiar modular nature of phage evolution creates ambiguities in the definition of phage taxa by comparative genomics. For example, depending on the module on which the classification is based, temperate lactococcal phages can be classified as a single phage species, as four distinct phage species, or as two if not three different phage genera. We propose to base phage taxonomy on comparative genomics of a single structural gene module (head or tail genes). This partially phylogeny-based taxonomical system still mirrors some aspects of the current International Committee on Taxonomy in Virology classification system. In this system the currently sequenced lactococcal phages would be grouped into five genera: c2-, sk1, Sfi11-, r1t-, and Sfi21-like phages.Due to their economic impact on industrial milk fermentation, bacteriophages attacking dairy starter bacteria (Streptococcus thermophilus, Lactococcus lactis, and various species of Lactobacillus) became the focus of substantial research efforts which made them the best-investigated phage group with respect to complete genome sequences (10). Dairy phages are therefore a suitable test case for hypotheses on phage evolution and for a genomics-based phage taxonomy. The comparative analysis of S. thermophilus phage genomes has revealed a rather homogeneous group of phages with substantial DNA sequence sharing between all investigated temperate and virulent phage isolates (11). On the basis of the DNA packaging mechanisms two groups m...

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Analysis of six prophages in Lactococcus lactis IL1403: different genetic structure of temperate and virulent phage populations

Cited by 161 publications

References 36 publications

Characterization of the Putative Replisome Organizer of the Lactococcal Bacteriophage r1t

The Dilemma of Phage Taxonomy Illustrated by Comparative Genomics of Sfi21-LikeSiphoviridaein Lactic Acid Bacteria

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