A survey of oenophages during wine making reveals a novel group with unusual genomic characteristics

Philippe, Cécile; Jaomanjaka, Féty; Claisse, Olivier; Laforgue, Rémi; Maupeu, Julie; Petrel, Melina; Marrec, Claire Le

doi:10.1016/j.ijfoodmicro.2017.06.014

Cited by 16 publications

(30 citation statements)

References 43 publications

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“…The same pattern applies to several other phages: Bacillus cereus phage BDRD‐cer4, Bacillus thuringiensis phage ATCC 10782, and Listeria monocytogenes phage A006, as identified examples. Phage OE33PA from Oenococcus oeni (Philippe et al, ) exhibits an insertion with another type of CBM, PDB ID 1GUI, corresponding to the CBM4 from Thermotoga maritima (Boraston et al, , fig. 10).…”

Section: Resultsmentioning

confidence: 99%

Functional carbohydrate binding modules identified in evolved dits from siphophages infecting various Gram‐positive bacteria

Hayes

Vincentelli

Mahony

et al. 2018

Molecular Microbiology

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With increasing numbers of 3D structures of bacteriophage components, combined with powerful in silico predictive tools, it has become possible to decipher the structural assembly and associated functionality of phage adhesion devices. Recently, decorations have been reported in the tail and neck passage structures of members of the so-called 936 group of lactococcal siphophages. In the current report, using bioinformatic analysis we identified a conserved carbohydrate binding module (CBM) among many of the virion baseplate Dit components, in addition to the CBM present in the 'classical' receptor binding proteins (RBPs). We observed that, within these so-called 'evolved' Dit proteins, the identified CBMs have structurally conserved folds, yet can be grouped into four distinct classes. We expressed such modules in fusion with GFP, and demonstrated their binding capability to their specific host using fluorescent binding assays with confocal microscopy. We detected evolved Dits in several phages infecting various Gram-positive bacterial species, including mycobacteria. The omnipresence of CBM domains in siphophages indicates their auxiliary role in infection, as they can assist in the specific recognition of and attachment to their host, thus ensuring a highly efficient and specific phage-host adhesion process as a prelude to DNA injection.

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Section: Resultsmentioning

confidence: 99%

Functional carbohydrate binding modules identified in evolved dits from siphophages infecting various Gram‐positive bacteria

Hayes

Vincentelli

Mahony

et al. 2018

Molecular Microbiology

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“…It should be pointed out that no IntC-type oenophage was available in our laboratory for this experiment. As a matter of fact, we were unsuccessful in isolating any IntC oenophage during our two past sampling campaigns targeting musts and wines (20,22). Moreover, no monolysogenic strain containing an IntC prophage was identified in the CRB Oeno collection.…”

Section: Resultsmentioning

confidence: 98%

“…The first hypothesis was ruled out by performing the lysogenization test in strain IOEBS277 using oenophages that integrate at other loci in the bacterial chromosome, such as attB B and attB D . Phage 10MC (IntB type) (28) and the IntD-type phages OE33SAG and 9805MC (20,22) were chosen. It should be pointed out that no IntC-type oenophage was available in our laboratory for this experiment.…”

Section: Resultsmentioning

confidence: 99%

“…They are inserted at tRNA sites and are so far clustered into four integrase gene sequence groups (IntA to IntD), which are also related to the chromosomal integration site. Members of the IntA group are the most prevalent prophages identified in oenococcal genomes (19,20) and also as replicating phages associated with wines and wine making production facilities, as reported in recent surveys (20,22). Lysogeny is frequent among commercial strains.…”

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confidence: 94%

“…The pervasiveness of prophages has been long recognized in the O. oeni species (17)(18)(19)(20)(21)(22). Prophages belong to the Siphoviridae family and are typically mosaic (19).…”

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confidence: 99%

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Lysogeny in the Lactic Acid Bacterium Oenococcus oeni Is Responsible for Modified Colony Morphology on Red Grape Juice Agar

Chaïb

Philippe

Jaomanjaka

et al. 2019

Appl Environ Microbiol

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Oenococcus oeni is the lactic acid bacterium (LAB) that most commonly drives malolactic fermentation in wine. Although oenococcal prophages are highly prevalent, their implications on bacterial fitness have remained unexplored and more research is required in this field. An important step toward achieving this goal is the ability to produce isogenic pairs of strains that differ only by the lysogenic presence of a given prophage, allowing further comparisons of different phenotypic traits. A novel protocol for the rapid isolation of lysogens is presented. Bacteria were first picked from the center of turbid plaques produced by temperate oenophages on a sensitive nonlysogenic host. When streaked onto an agar medium containing red grape juice (RGJ), cells segregated into white and red colonies. PCR amplifications with phage-specific primers demonstrated that only lysogens underwent white-red morphotypic switching. The method proved successful for various oenophages irrespective of their genomic content and attachment site used for site-specific recombination in the bacterial chromosome. The color switch was also observed when a sensitive nonlysogenic strain was infected with an exogenously provided lytic phage, suggesting that intracolonial lysis triggers the change. Last, lysogens also produced red colonies on white grape juice agar supplemented with polyphenolic compounds. We posit that spontaneous prophage excision produces cell lysis events in lysogenic colonies growing on RGJ agar, which, in turn, foster interactions between lysed materials and polyphenolic compounds to yield colonies easily distinguishable by their red color. Furthermore, the technique was used successfully with other species of LAB. IMPORTANCE The presence of white and red colonies on red grape juice (RGJ) agar during enumeration of Oenococcus oeni in wine samples is frequently observed by stakeholders in the wine industry. Our study brings an explanation for this intriguing phenomenon and establishes a link between the white-red color switch and the lysogenic state of O. oeni. It also provides a simple and inexpensive method to distinguish between lysogenic and nonlysogenic derivatives in O. oeni with a minimum of expended time and effort. Noteworthy, the protocol could be adapted to two other species of LAB, namely, Leuconostoc citreum and Lactobacillus plantarum. It could be an effective tool to provide genetic, ecological, and functional insights into lysogeny and aid in improving biotechnological processes involving members of the lactic acid bacterium (LAB) family.

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Measures to improve wine malolactic fermentation

Sumby

Bartle

Grbin

et al. 2019

Appl Microbiol Biotechnol

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peer review but prior to copyediting and typesetting that can be made available under the following conditions:(i) Author(s) retain the right to make an AAM of their Article available on their own personal, selfmaintained website immediately on acceptance, (ii) Author(s) retain the right to make an AAM of their Article available for public release on any of the following 12 months after first publication ("Embargo Period"): their employer's internal website; their institutional and/or funder repositories. AAMs may also be deposited in such repositories immediately on acceptance, provided that they are not made publicly available until after the Embargo Period.

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A survey of oenophages during wine making reveals a novel group with unusual genomic characteristics

Cited by 16 publications

References 43 publications

Functional carbohydrate binding modules identified in evolved dits from siphophages infecting various Gram‐positive bacteria

Functional carbohydrate binding modules identified in evolved dits from siphophages infecting various Gram‐positive bacteria

Lysogeny in the Lactic Acid Bacterium Oenococcus oeni Is Responsible for Modified Colony Morphology on Red Grape Juice Agar

Measures to improve wine malolactic fermentation

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