Genome diversity in temperate bacteriophages of Oenococcus oeni

Santos, Romana; São-José, Carlos; Vieira, G.; Paveia, H.; Santos, Mário A.

doi:10.1007/s007050050308

Cited by 17 publications

(5 citation statements)

References 21 publications

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“…The significant contribution of phage-related sequences to the dispensable gene reservoir of O. oeni is consistent with numerous reports of a high incidence of lysogeny in the species (1,34). However, these findings contrast with the situation recently described in the genomes of the ATCC BAA-1163 and PSU-1 strains, which do not contain any intact temperate bacteriophages or large tracts (Ͼ10 kb) of obvious bacteriophage origin (27,37,38 oeni. An assessment of the stability of phage-related sequences during the prolonged cultivation of bacterial strains on synthetic media, in the absence of any phage pressure, is now required.…”

Section: Discussioncontrasting

confidence: 99%

Oenococcus oeni Genome Plasticity Is Associated with Fitness

Bon

Delaherche

Bilhere

et al. 2009

Appl Environ Microbiol

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Oenococcus oeni strains are well-known for their considerable phenotypic variations in terms of tolerance to harsh wine conditions and malolactic activity. Genomic subtractive hybridization (SH) between two isolates with differing enological potentials was used to elucidate the genetic bases of this intraspecies diversity and identify novel genes involved in adaptation to wine. SH revealed 182 tester-specific fragments corresponding to 126 open reading frames (ORFs). A large proportion of the chromosome-related ORFs resembled genes involved in carbohydrate transport and metabolism, cell wall/membrane/envelope biogenesis, and replication, recombination, and repair. Six regions of genomic plasticity were identified, and their analysis suggested that both limited recombination and insertion/deletion events contributed to the vast genomic diversity observed in O. oeni. The association of selected sequences with adaptation to wine was further assessed by screening a large collection of strains using PCR. No sequences were found to be specific to highly performing (HP) strains alone. However, there was a statistically significant positive association between HP strains and the presence of eight gene sequences located on regions 2, 4, and 5. Gene expression patterns were significantly modified in HP strains, following exposure to one or more of the common stresses in wines. Regions 2 and 5 showed no traces of mobile elements and had normal GC content. In contrast, region 4 had the typical hallmarks of horizontal transfer, suggesting that the strategy of acquiring genes from other bacteria enhances the fitness of O. oeni strains.

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Section: Discussioncontrasting

confidence: 99%

Oenococcus oeni Genome Plasticity Is Associated with Fitness

Bon

Delaherche

Bilhere

et al. 2009

Appl Environ Microbiol

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“…O. oeni strain ML34-C10 (30) was used for phage fOg44 propagation. Preparation of fOg44 lysates was as previously described (29). Phage CE6 (Sam7 cI857 int::T7 gene 1; Stratagene) was propagated in E. coli LE392 as described by the supplier.…”

Section: Methodsmentioning

confidence: 99%

The N-Terminal Region of the Oenococcus oeni Bacteriophage fOg44 Lysin Behaves as a Bona Fide Signal Peptide in Escherichia coli and as a cis -Inhibitory Element, Preventing Lytic Activity on Oenococcal Cells

et al. 2000

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The function of the N-terminal region of the Oenococcus oeni phage fOg44 lysin (Lys44) as an export signal was investigated. We observed that when induced in Escherichia coli, Lys44 was cleaved between residues 27 and 28 in a SecA-dependent manner. Lys44 processing could be blocked by a specific signal peptidase inhibitor and was severely reduced by modification of the cleavage site. The lethal effect of Lys44 expression observed in E. coli was ascribed to the presence of its N-terminal 27-residue sequence, as its deletion resulted in the production of a nontoxic, albeit active, product. We have further established that lytic activity in oenococcal cells was dependent on Lys44 processing. An active protein with the molecular mass expected for the cleaved enzyme was detected in extracts from O. oeni-infected cells. The temporal pattern of its appearance suggests that synthesis and export of Lys44 in the infected host progress along with phage maturation. Overall, these results provide, for the first time, experimental evidence for the presence of a signal peptide in a bacteriophage lysin. Database searches and alignment of protein sequences support the prediction that other known O. oeni and Lactococcus lactis phages also encode secretory lysins. The evolutionary significance of a putative phage lysis mechanism relying on secretory lytic enzymes is tentatively discussed, on the basis of host cell wall structure and autolytic capacity.All tailed bacteriophages with double-stranded DNA genomes appear to accomplish lysis of the host cell by the concerted action of a peptidoglycan hydrolase (referred to as endolysin or lysin) and a small hydrophobic protein (holin) presumed to form nonspecific lesions upon oligomerization in the membrane (for a review, see reference 41). The latter function seems essential to allow access of the lytic enzyme to the cell wall compartment since in the phage lysins examined so far, the presence of a signal peptide (SP) that would target them to the translocase of the general secretion pathway (GSP) has never been demonstrated.We have recently described the sequences of the lysin and holin genes from the Oenococcus oeni bacteriophage fOg44 and noted that the N-terminal region of its putative lysin (Lys44) was highly hydrophobic (23). A similar observation was made earlier concerning a related enzyme from the lactococcal phage Tuc2009 (2). In spite of its hydrophobic character, the function of the N-terminal sequence of the Tuc2009 lysin as a possible SP was not considered, presumably because the presence of a holin gene upstream of lys argued for a standard holin-dependent lysin export mechanism. This assumption was strengthened by the observation that the expression of an almost identical lysin in Escherichia coli (LysB from the Lactococcus lactis phage LC3) did not result in a decrease in culture absorbance unless the corresponding holin was simultaneously induced (3).Interestingly, however, during an attempt to overproduce Lys44 in an easily purifiable form (as a histidine-tagged fusi...

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“…Incubation of tailed phages at high temperatures combined with chelating agents such as EDTA was early recognized to disrupt tailed phage particles with concomitant release of the viral DNA. Virion sensitivity correlated with the amount of DNA inside the phage capsid (Graham et al, 1979;Parkinson and Huskey, 1971;Santos et al, 1998). However, the TEB treatment proved effective to disrupt viral particles partially filled with as low as 50% of their DNA content (Fig.…”

Section: Discussionmentioning

confidence: 95%

A non-invasive method for studying viral DNA delivery to bacteria reveals key requirements for phage SPP1 DNA entry in Bacillus subtilis cells

et al. 2016

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Bacteriophages use most frequently a tail apparatus to create a channel across the entire bacterial cell envelope to transfer the viral genome to the host cell cytoplasm, initiating infection. Characterization of this critical step remains a major challenge due to the difficulty to monitor DNA entry in the bacterium and its requirements. In this work we developed a new method to study phage DNA entry that has the potential to be extended to many tailed phages. Its application to study genome delivery of bacteriophage SPP1 into Bacillus subtilis disclosed a key role of the host cell membrane potential in the DNA entry process. An energized B. subtilis membrane and a millimolar concentration of calcium ions are shown to be major requirements for SPP1 DNA entry following the irreversible binding of phage particles to the receptor YueB.

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Genome diversity in temperate bacteriophages of Oenococcus oeni

Cited by 17 publications

References 21 publications

Oenococcus oeni Genome Plasticity Is Associated with Fitness

Oenococcus oeni Genome Plasticity Is Associated with Fitness

The N-Terminal Region of the Oenococcus oeni Bacteriophage fOg44 Lysin Behaves as a Bona Fide Signal Peptide in Escherichia coli and as a cis -Inhibitory Element, Preventing Lytic Activity on Oenococcal Cells

A non-invasive method for studying viral DNA delivery to bacteria reveals key requirements for phage SPP1 DNA entry in Bacillus subtilis cells

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