Identification of four loci isolated from two<i>Streptococcus thermophilus</i>phage genomes responsible for mediating bacteriophage resistance

Stanley, Elizabeth; Walsh, Linda; Zwet, Anneke van der; Fitzgerald, Gerald F.; Sinderen, Douwe van

doi:10.1111/j.1574-6968.2000.tb08907.x

Cited by 53 publications

(11 citation statements)

References 25 publications

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“…An initial analysis of the DNA sequences revealed a high level of nucleotide identity (greater than 90% across approximately one-third of the length of their genomes) with phage ul36 (39), and also with Tuc2009, TP901-1, and the archetype P335, which are related phages, all belonging to P335 subgroup II (40,41). In contrast, the rightward end of each of the 9871-4 phage genomes appears to bear more similarity to S. thermophilus phage replication modules (42) (Fig. 1).…”

Section: Resultsmentioning

confidence: 99%

“…7B]) and the replication modules (comprising the lysin-encoding gene to the terminal ORF [ Fig. 7C]) of the 987 group with the relevant comparators, i.e., phages that also harbor group II/7201-like replication modules (42,66), show a clear difference in clustering, indicating the diverse lineage of these respective modules in the 987 group phages.…”

Section: Resultsmentioning

confidence: 99%

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Identification and Analysis of a Novel Group of Bacteriophages Infecting the Lactic Acid Bacterium Streptococcus thermophilus

McDonnell

Mahony

Neve

et al. 2016

Appl Environ Microbiol

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We present the complete genome sequences of four members of a novel group of phages infecting Streptococcus thermophilus, designated here as the 987 group. Members of this phage group appear to have resulted from genetic exchange events, as evidenced by their "hybrid" genomic architecture, exhibiting DNA sequence relatedness to the morphogenesis modules of certain P335 group Lactococcus lactis phages and to the replication modules of S. thermophilus phages. All four identified members of the 987 phage group were shown to elicit adsorption affinity to both their cognate S. thermophilus hosts and a particular L. lactis starter strain. The receptor binding protein of one of these phages (as a representative of this novel group) was defined using an adsorption inhibition assay. The emergence of a novel phage group infecting S. thermophilus highlights the continuous need for phage monitoring and development of new phage control measures. IMPORTANCEPhage predation of S. thermophilus is an important issue for the dairy industry, where viral contamination can lead to fermentation inefficiency or complete fermentation failure. Genome information and phage-host interaction studies of S. thermophilus phages, particularly those emerging in the marketplace, are an important part of limiting the detrimental impact of these viruses in the dairy environment. Streptococcus thermophilus is a globally employed dairy bacterium used in the production of a variety of cheeses and yoghurt. Having been safely consumed by humans for millennia, this bacterium is now a mainstay of the dairy industry due its favorable acidification and texturizing properties (1, 2). Despite advances in the available knowledge regarding dairy phage containment (3, 4) and S. thermophilus phage genetics and biology (5, 6), contamination of dairy production lines by S. thermophilus-infecting (bacterio)phages remains a persistent problem (for a review, see reference 7).Classification of phages of S. thermophilus (reviewed by Mahony and van Sinderen [8]) has long been based on (i) morphology, i.e., as Siphoviridae, corresponding to group B as defined by Bradley (9), and (ii) a combination of the mode of DNA packaging (i.e., cos or pac site-containing) and major structural protein content (10). A variable genomic region thought to be (at least in part) responsible for host determination (VR2 region [11]) can also be used to categorize the majority of isolated S. thermophilus phages (12). More recently, however, a morphologically distinct and genetically divergent S. thermophilus phage named 5093, containing neither cos-or pac-defining structural elements nor a confirmed antireceptor-encoding gene, was described (13), prompting the creation of a third S. thermophilus phage group (here termed the "5093 group"). The genomic content of phage 5093 (containing several genes of nondairy streptococcal phage origin) highlights the genetic plasticity of S. thermophilus phages, thus explaining the appearance of such diverse phage lineages.A total of 13 complete genom...

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Identification and Analysis of a Novel Group of Bacteriophages Infecting the Lactic Acid Bacterium Streptococcus thermophilus

McDonnell

Mahony

Neve

et al. 2016

Appl Environ Microbiol

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“…To date, the complete genomes of 20 phages infecting S. thermophilus have been published: O1205 (Stanley et al, 1997 ), Sfi19 and Sfi21 (Desiere et al, 1998 ), DT1 (Tremblay and Moineau, 1999 ), Sfi11 (Lucchini et al, 1999 ), 7201 (Stanley et al, 2000 ), 2972 (Levesque et al, 2005 ), 858 (Deveau et al, 2008 ), ALQ13.2 and Abc2 (Guglielmotti et al, 2009b ), 5093 (Mills et al, 2011 ), TP-J34L and TP-778L (Ali et al, 2014 ), 9871, 9872, 9873, and 9874 (McDonnell et al, 2016 ), and (very recently) CHPC577, CHPC926, and CHPC1151 (Szymczak et al, 2016 ). Their availability revealed that S. thermophilus phage genomes possess a modular structure, while it also allowed an analysis of their evolution and relatedness (Lucchini et al, 1999 ; Proux et al, 2002 ), thereby providing insights into some unusual genetic lineages (Mills et al, 2011 ; McDonnell et al, 2016 ; Szymczak et al, 2016 ; discussed further below).…”

Section: Introductionmentioning

confidence: 99%

Global Survey and Genome Exploration of Bacteriophages Infecting the Lactic Acid Bacterium Streptococcus thermophilus

et al. 2017

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Despite the persistent and costly problem caused by (bacterio)phage predation of Streptococcus thermophilus in dairy plants, DNA sequence information relating to these phages remains limited. Genome sequencing is necessary to better understand the diversity and proliferative strategies of virulent phages. In this report, whole genome sequences of 40 distinct bacteriophages infecting S. thermophilus were analyzed for general characteristics, genomic structure and novel features. The bacteriophage genomes display a high degree of conservation within defined groupings, particularly across the structural modules. Supporting this observation, four novel members of a recently discovered third group of S. thermophilus phages (termed the 5093 group) were found to be conserved relative to both phage 5093 and to each other. Replication modules of S. thermophilus phages generally fall within two main groups, while such phage genomes typically encode one putative transcriptional regulator. Such features are indicative of widespread functional synteny across genetically distinct phage groups. Phage genomes also display nucleotide divergence between groups, and between individual phages of the same group (within replication modules and at the 3′ end of the lysis module)—through various insertions and/or deletions. A previously described multiplex PCR phage detection system was updated to reflect current knowledge on S. thermophilus phages. Furthermore, the structural protein complement as well as the antireceptor (responsible for the initial attachment of the phage to the host cell) of a representative of the 5093 group was defined. Our data more than triples the currently available genomic information on S. thermophilus phages, being of significant value to the dairy industry, where genetic knowledge of lytic phages is crucial for phage detection and monitoring purposes. In particular, the updated PCR detection methodology for S. thermophilus phages is highly useful in monitoring particular phage group(s) present in a given whey sample. Studies of this nature therefore not only provide information on the prevalence and associated threat of known S. thermophilus phages, but may also uncover newly emerging and genomically distinct phages infecting this dairy starter bacterium.

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“…Although this genome structure is similar to that of phage 1706, the shared nucleotide identity with the latter genome is much lower (Fig. 3A), and they are thus classified as being distantly related to 1706 (34). We conducted an in silico analysis to compare phage CHPC971 with the four raw milk phages, choosing one of them, P094, as a reference.…”

Section: Resultsmentioning

confidence: 99%

A Specific Sugar Moiety in the Lactococcus lactis Cell Wall Pellicle Is Required for Infection by CHPC971, a Member of the Rare 1706 Phage Species

Marcelli

Jong

Karsens

et al. 2019

Appl Environ Microbiol

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Lactococcus lactis is a Gram-positive bacterium widely used as a starter culture for the production of different dairy products, especially a large variety of cheeses. Infection of lactococcal starter cultures by bacteriophages is one of the major causes of fermentation failure and often leads to production halt. Lactococcal bacteriophages belonging to the c2, 936, and P335 species are the most commonly isolated in dairy plants and have been extensively investigated in the past three decades. Information regarding bacteriophages belonging to less commonly isolated species is, on the other hand, less extensive, although these phages can also contribute to starter culture infection. Here, we report the nucleotide sequence of the newly isolated L. lactis phage CHPC971, belonging to the rare 1706 species of lactococcal phages. We investigated the nature of the host receptor recognized by the phage and collected evidence that strongly suggests that it binds to a specific sugar moiety in the cell wall pellicle of its host. An in silico analysis of the genome of phage CHPC971 identified the hypothetical genes involved in receptor binding. IMPORTANCE Gathering information on how lactococcal bacteriophages recognize their host and proliferate in the dairy environment is of vital importance for the establishment of proper starter culture rotation plans and to avoid fermentation failure and consequent great economic losses for dairy industries. We provide strong evidence on the type of receptor recognized by a newly isolated 1706-type lactococcal bacteriophage, increasing knowledge of phage-host interactions relevant to dairying. This information can help to prevent phage infection events that, so far, are hard to predict and avoid.

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Identification of four loci isolated from twoStreptococcus thermophilusphage genomes responsible for mediating bacteriophage resistance

Cited by 53 publications

References 25 publications

Identification and Analysis of a Novel Group of Bacteriophages Infecting the Lactic Acid Bacterium Streptococcus thermophilus

Identification and Analysis of a Novel Group of Bacteriophages Infecting the Lactic Acid Bacterium Streptococcus thermophilus

Global Survey and Genome Exploration of Bacteriophages Infecting the Lactic Acid Bacterium Streptococcus thermophilus

A Specific Sugar Moiety in the Lactococcus lactis Cell Wall Pellicle Is Required for Infection by CHPC971, a Member of the Rare 1706 Phage Species

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