{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T02:10:51Z","timestamp":1791252651705,"version":"4.1.0"},"reference-count":45,"publisher":"Oxford University Press (OUP)","issue":"1","license":[{"start":{"date-parts":[[2013,1,1]],"date-time":"2013-01-01T00:00:00Z","timestamp":1356998400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2013,1,1]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>In this study we report for the first time a rapid, efficient and cost-effective method for the enumeration of lactic acid bacteria (LAB) in wine. Indeed, up to now, detection of LAB in wine, especially red wine, was not possible. Wines contain debris that cannot be separated from bacteria using flow cytometry (FCM). Furthermore, the dyes tested in previous reports did not allow an efficient staining of bacteria. Using FCM and a combination of BOX\/PI dyes, we were able to count bacteria in wines. The study was performed in wine inoculated with Oenococcus oeni (106\u00a0CFU\u00a0ml\u22121) stained with either FDA or BOX\/PI and analyzed by FCM during the malolactic fermentation (MLF). The analysis show a strong correlation between the numbers of BOX\/PI-stained cells determined by FCM and the cell numbers determined by plate counts (red wine: R2\u00a0\u2265\u00a00.97, white wine R2\u00a0\u2265\u00a00.965). On the other hand, we found that the enumeration of O. oeni labeled with FDA was only possible in white wine (R2\u00a0\u2265\u00a00.97). Viable yeast and LAB populations can be rapidly discriminated and quantified in simultaneous malolactic-alcoholic wine fermentations using BOX\/PI and scatter parameters in a one single measurement. This rapid procedure is therefore a suitable method for monitoring O. oeni populations during winemaking, offers a detection limit of &amp;lt;104\u00a0CFU\u00a0ml\u22121 and can be considered a useful method for investigating the dynamics of microbial growth in wine and applied for microbiological quality control in wineries.<\/jats:p>","DOI":"10.1007\/s10295-012-1200-3","type":"journal-article","created":{"date-parts":[[2012,10,18]],"date-time":"2012-10-18T19:15:00Z","timestamp":1350587700000},"page":"63-73","source":"Crossref","is-referenced-by-count":24,"title":["Cytofluorometric detection of wine lactic acid bacteria: application of malolactic fermentation to the monitoring"],"prefix":"10.1093","volume":"40","author":[{"given":"Mohammad","family":"Salma","sequence":"first","affiliation":[{"name":"grid.5613.1 0000000122989313 UMR 02102 PAM Universit\u00e9 de Bourgogne-AgroSup Dijon Laboratoire VALMIS Institut Universitaire de la Vigne et du Vin Jules Guyot Universit\u00e9 de Bourgogne 21078 Dijon Cedex France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sandrine","family":"Rousseaux","sequence":"additional","affiliation":[{"name":"grid.5613.1 0000000122989313 UMR 02102 PAM Universit\u00e9 de Bourgogne-AgroSup Dijon Laboratoire VALMIS Institut Universitaire de la Vigne et du Vin Jules Guyot Universit\u00e9 de Bourgogne 21078 Dijon Cedex France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anabelle","family":"Sequeira-Le Grand","sequence":"additional","affiliation":[{"name":"grid.5613.1 0000000122989313 Plateforme de Cytom\u00e9trie, Structure F\u00e9d\u00e9rative de Recherche Sant\u00e9 STIC, Fac. M\u00e9decine Universit\u00e9 de Bourgogne 7, Bd Jeanne D\u2019Arc 21000 Dijon France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Herv\u00e9","family":"Alexandre","sequence":"additional","affiliation":[{"name":"grid.5613.1 0000000122989313 UMR 02102 PAM Universit\u00e9 de Bourgogne-AgroSup Dijon Laboratoire VALMIS Institut Universitaire de la Vigne et du Vin Jules Guyot Universit\u00e9 de Bourgogne 21078 Dijon Cedex France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2013,1,1]]},"reference":[{"key":"2021033103203436600_CR1","first-page":"289","article-title":"Malolactic fermentation","volume-title":"Wine microbiology biotechnology","author":"Henick-Kling","year":"1993"},{"issue":"4","key":"2021033103203436600_CR2","doi-asserted-by":"crossref","first-page":"641","DOI":"10.1128\/MR.60.4.641-696.1996","article-title":"Flow cytometry and cell sorting of heterogeneous microbial populations: the importance of single-cell analyses","volume":"60","author":"Davey","year":"1996","journal-title":"Microbiol Rev"},{"issue":"3","key":"2021033103203436600_CR3","doi-asserted-by":"publisher","first-page":"1228","DOI":"10.1128\/AEM.66.3.1228-1232.2000","article-title":"A flow cytometry method for rapid detection and enumeration of total bacteria in milk","volume":"66","author":"Gunasekera","year":"2000","journal-title":"Appl Environ Microbiol"},{"issue":"4","key":"2021033103203436600_CR4","doi-asserted-by":"publisher","first-page":"640","DOI":"10.1016\/S0723-2020(97)80036-7","article-title":"Rapid identification and detection of Lactobacillus sanfrancisco in sourdough by species-specific PCR with 16S rRNA-targeted primers","volume":"20","author":"Zapparoli","year":"1997","journal-title":"Syst Appl Microbiol"},{"issue":"5","key":"2021033103203436600_CR5","doi-asserted-by":"publisher","first-page":"243","DOI":"10.1046\/j.1472-765X.1998.00448.x","article-title":"Design and evaluation of malolactic enzyme gene targeted primers for rapid identification and detection of Oenococcus oeni in wine","volume":"27","author":"Zapparoli","year":"1998","journal-title":"Lett Appl Microbiol"},{"issue":"2","key":"2021033103203436600_CR6","doi-asserted-by":"publisher","first-page":"118","DOI":"10.1111\/j.1472-765X.2003.01462.x","article-title":"Rapid detection of Oenococcus oeni in wine by real-time quantitative PCR","volume":"38","author":"Pinzani","year":"2004","journal-title":"Lett Appl Microbiol"},{"issue":"1\u20132","key":"2021033103203436600_CR7","doi-asserted-by":"publisher","first-page":"119","DOI":"10.1016\/S0168-1605(99)00081-1","article-title":"Methodology for detection and typing of foodborne microorganisms","volume":"50","author":"De Boer","year":"1999","journal-title":"Int J Food Microbiol"},{"key":"2021033103203436600_CR8"},{"issue":"2","key":"2021033103203436600_CR9","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1080\/87559129609541073","article-title":"Automated direct and indirect methods in food microbiology: a literature review","volume":"12","author":"Karwoski","year":"1996","journal-title":"Food Rev Int"},{"issue":"1","key":"2021033103203436600_CR10","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/S1567-1356(02)00125-3","article-title":"A flow-cytometric method for determination of yeast viability and cell number in a brewery","volume":"3","author":"Boyd","year":"2003","journal-title":"FEMS Yeast Res"},{"issue":"6","key":"2021033103203436600_CR11","doi-asserted-by":"publisher","first-page":"4163","DOI":"10.1128\/AEM.02283-05","article-title":"Improved enumeration of lactic acid bacteria in mesophilic dairy starter cultures by using multiplex quantitative real-time PCR and flow cytometry-fluorescence in situ hybridization","volume":"72","author":"Friedrich","year":"2006","journal-title":"Appl Environ Microbiol"},{"issue":"10","key":"2021033103203436600_CR12","doi-asserted-by":"publisher","first-page":"6725","DOI":"10.1128\/AEM.01183-06","article-title":"Use of flow cytometry to follow the physiological states of microorganisms in cider fermentation processes","volume":"72","author":"Herrero","year":"2006","journal-title":"Appl Environ Microbiol"},{"issue":"15","key":"2021033103203436600_CR13","doi-asserted-by":"publisher","first-page":"5088","DOI":"10.1128\/AEM.02932-09","article-title":"Specific and rapid enumeration of viable but nonculturable and viable-culturable gram-negative bacteria by using flow cytometry","volume":"76","author":"Khan","year":"2010","journal-title":"Appl Environ Microbiol"},{"key":"2021033103203436600_CR14","doi-asserted-by":"publisher","first-page":"489","DOI":"10.1016\/S0091-679X(08)61092-4","article-title":"Detection of specific microorganisms in environmental samples using flow cytometry","volume":"42 Pt B","author":"Vesey","year":"1994","journal-title":"Met Cell Biol"},{"key":"2021033103203436600_CR15","doi-asserted-by":"publisher","first-page":"253","DOI":"10.1007\/978-1-61779-806-1_13","article-title":"Detection of specific strains of viable bacterial pathogens by using RNA bead assays and flow cytometry with 2100 Bioanalyzer","volume":"875","author":"Butterworth","year":"2012","journal-title":"Meth Mol Biol"},{"issue":"8","key":"2021033103203436600_CR16","doi-asserted-by":"publisher","first-page":"815","DOI":"10.1111\/j.1364-3703.2011.00711.x","article-title":"Applications of flow cytometry in plant pathology for genome size determination, detection and physiological status","volume":"12","author":"D\u2019Hondt","year":"2011","journal-title":"Mol Plant Pathol"},{"issue":"3","key":"2021033103203436600_CR17","doi-asserted-by":"crossref","first-page":"264","DOI":"10.1002\/cyto.a.20858","article-title":"Rapid and quantitative detection of Legionella pneumophila applying immunomagnetic separation and flow cytometry","volume":"77","author":"F\u00fcchslin","year":"2010","journal-title":"Cytom Part A"},{"key":"2021033103203436600_CR18"},{"issue":"4","key":"2021033103203436600_CR19","doi-asserted-by":"crossref","first-page":"576","DOI":"10.1128\/CMR.7.4.576","article-title":"Uses of flow cytometry in virology","volume":"7","author":"McSharry","year":"1994","journal-title":"Clin Microbiol Rev"},{"issue":"6","key":"2021033103203436600_CR20","doi-asserted-by":"publisher","first-page":"343","DOI":"10.1111\/j.1472-765X.1994.tb00885.x","article-title":"Use of flow cytometry in oenology to analyse yeasts","volume":"18","author":"Bruetschy","year":"1994","journal-title":"Lett Appl Microbiol"},{"issue":"6","key":"2021033103203436600_CR21","doi-asserted-by":"publisher","first-page":"466","DOI":"10.1111\/j.1472-765X.2005.01713.x","article-title":"The vinification of partially dried grapes: a comparative fermentation study of Saccharomyces cerevisiae strains under high sugar stress","volume":"40","author":"Malacrin\u00f2","year":"2005","journal-title":"Lett Appl Microbiol"},{"issue":"2","key":"2021033103203436600_CR22","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1016\/S0167-7012(01)00243-3","article-title":"Rapid detection of viable yeasts and bacteria in wine by flow cytometry","volume":"45","author":"Malacrin\u00f2","year":"2001","journal-title":"J Microbiol Meth"},{"issue":"1","key":"2021033103203436600_CR23","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1111\/j.1472-765X.2007.02265.x","article-title":"Use of flow cytometry with fluorescent antibodies in real-time monitoring of simultaneously inoculated alcoholic-malolactic fermentation of Chardonnay","volume":"46","author":"Rodriguez","year":"2008","journal-title":"Lett Appl Microbiol"},{"issue":"11","key":"2021033103203436600_CR24","doi-asserted-by":"publisher","first-page":"787","DOI":"10.1023\/A:1008974419342","article-title":"Evaluation of cell numbers and viability of Saccharomyces cerevisiae by different counting methods","volume":"13","author":"Fiala","year":"1999","journal-title":"Biotech Tech"},{"issue":"2","key":"2021033103203436600_CR25","doi-asserted-by":"publisher","first-page":"221","DOI":"10.1111\/j.1365-2672.1994.tb03067.x","article-title":"The use of fluorogenic esters to detect viable bacteria by flow cytometry","volume":"77","author":"Diaper","year":"1994","journal-title":"J Appl Microbiol"},{"issue":"5","key":"2021033103203436600_CR26","doi-asserted-by":"publisher","first-page":"487","DOI":"10.1023\/A:1018312714761","article-title":"Enhancement of apparent resistance to ethanol in Lactobacillus hilgardii","volume":"19","author":"Ant\u00f3nio Couto","year":"1997","journal-title":"Biotechnol Lett"},{"issue":"10","key":"2021033103203436600_CR27","doi-asserted-by":"publisher","first-page":"5826","DOI":"10.1128\/AEM.69.10.5826-5832.2003","article-title":"Membrane fluidity adjustments in ethanol-stressed Oenococcus oeni cells","volume":"69","author":"Silveira","year":"2003","journal-title":"Appl Environ Microbiol"},{"issue":"1","key":"2021033103203436600_CR28","doi-asserted-by":"publisher","first-page":"146","DOI":"10.1007\/s00248-001-0036-6","article-title":"Lactobacillic acid accumulation in the plasma membrane of Oenococcus oeni: a response to ethanol stress","volume":"43","author":"Teixeira","year":"2002","journal-title":"Microb Ecol"},{"issue":"3","key":"2021033103203436600_CR29","doi-asserted-by":"publisher","first-page":"426","DOI":"10.1021\/ac60147a030","article-title":"Use of dinitrosalicylic acid reagent for determination of reducing sugar","volume":"31","author":"Miller","year":"1959","journal-title":"Anal Chem"},{"issue":"8","key":"2021033103203436600_CR30","doi-asserted-by":"publisher","first-page":"2015","DOI":"10.1099\/mic.0.26312-0","article-title":"Effect of EDTA on Salmonella enterica serovar Typhimurium involves a component not assignable to lipopolysaccharide release","volume":"149","author":"Alakomi","year":"2003","journal-title":"Microbiology"},{"issue":"1","key":"2021033103203436600_CR31","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1111\/j.1365-2818.1995.tb03612.x","article-title":"Viability assessment of bacteria in mixed populations using flow cytometry","volume":"179","author":"Caron","year":"1995","journal-title":"J Microscopy"},{"issue":"2\u20133","key":"2021033103203436600_CR32","doi-asserted-by":"publisher","first-page":"251","DOI":"10.1016\/S0168-1656(99)00168-6","article-title":"The use of multi-parameter flow cytometry to compare the physiological response of Escherichia coli W3110 to glucose limitation during batch, fed-batch and continuous culture cultivations","volume":"75","author":"Hewitt","year":"1999","journal-title":"J Biotechnol"},{"issue":"6","key":"2021033103203436600_CR33","doi-asserted-by":"publisher","first-page":"705","DOI":"10.1002\/(SICI)1097-0290(19990620)63:6&lt;705::AID-BIT8&gt;3.0.CO;2-M","article-title":"Use of multi-staining flow cytometry to characterise the physiological state of Escherichia coli W3110 in high cell density fed-batch cultures","volume":"63","author":"Hewitt","year":"1999","journal-title":"Biotechnol Bioeng"},{"issue":"3","key":"2021033103203436600_CR34","doi-asserted-by":"publisher","first-page":"179","DOI":"10.1002\/1097-0320(20010701)44:3&lt;179::AID-CYTO1110&gt;3.0.CO;2-D","article-title":"An industrial application of multiparameter flow cytometry: assessment of cell physiological state and its application to the study of microbial fermentations","volume":"44","author":"Hewitt","year":"2001","journal-title":"Cytom Part A"},{"issue":"1","key":"2021033103203436600_CR35","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1016\/S0167-7012(00)00181-0","article-title":"Analysis of bacterial function by multi-colour fluorescence flow cytometry and single cell sorting","volume":"42","author":"Nebe-von-Caron","year":"2000","journal-title":"J Microbiol Meth"},{"issue":"2","key":"2021033103203436600_CR36","doi-asserted-by":"publisher","first-page":"144","DOI":"10.1016\/j.ijfoodmicro.2009.07.031","article-title":"Cell membrane damage induced by phenolic acids on wine lactic acid bacteria","volume":"135","author":"Campos","year":"2009","journal-title":"Int J Food Microbiol"},{"issue":"2","key":"2021033103203436600_CR37","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1080\/10408410600709800","article-title":"Environmental stress response in wine lactic acid bacteria: beyond Bacillus subtilis","volume":"32","author":"Spano","year":"2006","journal-title":"Crit Rev Microbiol"},{"issue":"6","key":"2021033103203436600_CR38","doi-asserted-by":"publisher","first-page":"1015","DOI":"10.1046\/j.1365-2672.2003.01923.x","article-title":"Membrane damage to bacteria caused by single and combined biocides","volume":"94","author":"Johnston","year":"2003","journal-title":"J Appl Microbiol"},{"issue":"6","key":"2021033103203436600_CR39","doi-asserted-by":"publisher","first-page":"497","DOI":"10.1002\/cyto.a.20861","article-title":"Specific identification and quantification of the spoilage microorganism Brettanomyces in wine by flow cytometry: a useful tool for winemakers","volume":"77A","author":"Serpaggi","year":"2010","journal-title":"Cytom Part A"},{"issue":"8","key":"2021033103203436600_CR40","doi-asserted-by":"publisher","first-page":"999","DOI":"10.1007\/s10295-009-0608-x","article-title":"Flow cytometry applications in the food industry","volume":"36","author":"Comas-Riu","year":"2009","journal-title":"J Ind Microbiol Biotechnol"},{"key":"2021033103203436600_CR41"},{"issue":"2","key":"2021033103203436600_CR42","doi-asserted-by":"publisher","first-page":"136","DOI":"10.1016\/j.fm.2005.01.019","article-title":"Lactic acid bacteria evolution during winemaking: use of rpoB gene as a target for PCR-DGGE analysis","volume":"23","author":"Renouf","year":"2006","journal-title":"Food Microbiol"},{"issue":"2","key":"2021033103203436600_CR43","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1016\/j.ijfoodmicro.2003.10.013","article-title":"Saccharomyces cerevisiae-Oenococcus oeni interactions in wine: current knowledge and perspectives","volume":"93","author":"Alexandre","year":"2004","journal-title":"Int J Food Microbiol"},{"issue":"1","key":"2021033103203436600_CR44","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1016\/j.fm.2011.09.006","article-title":"The impact of co-inoculation with Oenococcus oeni on the trancriptome of Saccharomyces cerevisiae and on the flavour-active metabolite profiles during fermentation in synthetic must","volume":"29","author":"Rossouw","year":"2012","journal-title":"Food Microbiol"},{"issue":"1\u20134","key":"2021033103203436600_CR45","doi-asserted-by":"publisher","first-page":"317","DOI":"10.1023\/A:1002088931106","article-title":"Lactic acid bacteria in the quality improvement and depreciation of wine","volume":"76","author":"Lonvaud-Funel","year":"1999","journal-title":"Antonie Leeuwenhoek"}],"container-title":["Journal of Industrial Microbiology and Biotechnology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s10295-012-1200-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1007\/s10295-012-1200-3\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/academic.oup.com\/jimb\/article-pdf\/40\/1\/63\/36803608\/jimb0063.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/jimb\/article-pdf\/40\/1\/63\/36803608\/jimb0063.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,4,30]],"date-time":"2024-04-30T11:35:38Z","timestamp":1714476938000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jimb\/article\/40\/1\/63\/5994739"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2013,1,1]]},"references-count":45,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2013,1,1]]}},"URL":"https:\/\/doi.org\/10.1007\/s10295-012-1200-3","relation":{},"ISSN":["1476-5535","1367-5435"],"issn-type":[{"value":"1476-5535","type":"electronic"},{"value":"1367-5435","type":"print"}],"subject":[],"published-other":{"date-parts":[[2013,1,1]]},"published":{"date-parts":[[2013,1,1]]}}}