{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,9]],"date-time":"2026-10-09T14:44:16Z","timestamp":1791557056005,"version":"4.3.4"},"reference-count":32,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2019,11,18]],"date-time":"2019-11-18T00:00:00Z","timestamp":1574035200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Seventh Framework Programme","award":["ERAfrica ERAFRICA IC-027, FP-226154"],"award-info":[{"award-number":["ERAfrica ERAFRICA IC-027, FP-226154"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Nutrients"],"abstract":"<jats:p>Folate deficiencies are widespread around the world. Promoting consumption of folate-rich foods could be a sustainable option to alleviate this problem. However, these foods are not always available. Cereals, being a staple food, could contribute to folate intake. They are fermented prior to consumption in many African countries, and fermentation can modify the folate content. In Ethiopia, injera is a widely consumed fermented flat bread. The main drivers of its fermentation are lactic acid bacteria (LAB). The aim of this work was to isolate and identify folate-producing LAB from injera fermented dough and to evaluate their ability to increase folate status after depletion in a rat model. Among the 162 strains isolated from 60 different fermentations, 19 were able to grow on a folate-free culture medium and produced 1 to 43 \u00b5g\/L (24 h, 30 \u00b0C incubation). The four highest folate producers belonged to the Lactobacillus plantarum species. The most productive strain was able to enhance folate status after depletion in a rat model, despite the relatively low folate content of the feed supplemented with the strain. Folate-producing L. plantarum strain has potential use as a commercial starter in injera production.<\/jats:p>","DOI":"10.3390\/nu11112819","type":"journal-article","created":{"date-parts":[[2019,11,18]],"date-time":"2019-11-18T11:18:48Z","timestamp":1574075928000},"page":"2819","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":47,"title":["Lactobacillus plantarum P2R3FA Isolated from Traditional Cereal-Based Fermented Food Increase Folate Status in Deficient Rats"],"prefix":"10.3390","volume":"11","author":[{"given":"Aynadis","family":"Tamene","sequence":"first","affiliation":[{"name":"Center for food science and nutrition, Addis Ababa University, Addis Ababa P.O. Box 150201, Ethiopia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kaleab","family":"Baye","sequence":"additional","affiliation":[{"name":"Center for food science and nutrition, Addis Ababa University, Addis Ababa P.O. Box 150201, Ethiopia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0207-2422","authenticated-orcid":false,"given":"Susanna","family":"Kariluoto","sequence":"additional","affiliation":[{"name":"Department of Food and Nutrition, University of Helsinki, P.O. Box 66, FIN-00014 Helsinki, Finland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Minnamari","family":"Edelmann","sequence":"additional","affiliation":[{"name":"Department of Food and Nutrition, University of Helsinki, P.O. Box 66, FIN-00014 Helsinki, Finland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fabrice","family":"Bationo","sequence":"additional","affiliation":[{"name":"D\u00e9partement de Technologie Alimentaire, IRSAT, CNRST, Ouagadougou B.P. 7047, Burkina Faso"},{"name":"UMR Nutripass, IRD, University of Montpellier\/Montpellier SupAgro, 34394 Montpellier, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nicolas","family":"Leconte","sequence":"additional","affiliation":[{"name":"UMR Nutripass, IRD, University of Montpellier\/Montpellier SupAgro, 34394 Montpellier, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9797-1625","authenticated-orcid":false,"given":"Christ\u00e8le","family":"Humblot","sequence":"additional","affiliation":[{"name":"UMR Nutripass, IRD, University of Montpellier\/Montpellier SupAgro, 34394 Montpellier, France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2019,11,18]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1002\/bdra.20504","article-title":"Update on prevention of folic acid-preventable spina bifida and anencephaly","volume":"85","author":"Bell","year":"2009","journal-title":"Birth Defects Res. Part A Clin. Mol. Teratol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1038\/sj.ejcn.1602923","article-title":"Which are the greatest recent discoveries and the greatest future challenges in nutrition?","volume":"63","author":"Katan","year":"2009","journal-title":"Eur. J. Clin. Nutr."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"i110","DOI":"10.1093\/ije\/dyq028","article-title":"Folic acid to reduce neonatal mortality from neural tube disorders","volume":"39","author":"Blencowe","year":"2010","journal-title":"Int. J. Epidemiol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"993","DOI":"10.1093\/ajcn\/83.5.993","article-title":"Folate and human reproduction","volume":"83","author":"Tamura","year":"2006","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1093\/bmb\/ldt015","article-title":"Meeting the challenges of micronutrient malnutrition in the developing world","volume":"106","author":"Bhutta","year":"2013","journal-title":"Br. Med. Bull."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"548","DOI":"10.1017\/S0029665107005873","article-title":"Folate and vitamin B12: Friendly or enemy nutrients for the elderly: Symposium on \u2018Micronutrients through the life cycle\u2019","volume":"66","author":"Cuskelly","year":"2007","journal-title":"Proc. Nutr. Soc."},{"key":"ref_7","unstructured":"FAO, and WHO (1998). (2004) Vitamin and Mineral Requirements in Human Nutrition, Joint FAO\/WHO Expert Consultation on Human Vitamin and Mineral Requirements. [2nd ed.]."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Bationo, F., Songr\u00e9-Ouattara, L.T., Hama-Ba, F., Baye, K., Hemery, Y.M., Parkouda, C., Lingani-Sawadogo, H., Diawara, B., and Humblot, C. (2019). Folate Status of Women and Children in Africa\u2013Current Situation and Improvement Strategies. Food Rev. Int., 1\u201314.","DOI":"10.1080\/87559129.2019.1608558"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"3894","DOI":"10.1080\/10408398.2016.1192986","article-title":"Lactic acid fermentation as a tool for increasing the folate content of foods","volume":"57","author":"Saubade","year":"2017","journal-title":"Crit. Rev. Food Sci. Nutr."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1109","DOI":"10.1111\/j.1365-2621.2012.02969.x","article-title":"Cereal-based fermented foods in developing countries: Ancient foods for modern research","volume":"47","author":"Guyot","year":"2012","journal-title":"Int. J. Food Sci. Technol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1016\/S0168-1605(01)00707-3","article-title":"Appropriate starter culture technologies for small-scale fermentation in developing countries","volume":"75","author":"Holzapfel","year":"2002","journal-title":"Int. J. Food Microbiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1016\/j.foodchem.2004.03.036","article-title":"The effect of fermentation and drying on the water-soluble vitamin content of tarhana, a traditional Turkish cereal food","volume":"90","year":"2005","journal-title":"Food Chem."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"100S","DOI":"10.1080\/07315724.2000.10718071","article-title":"Folates and dairy products: A critical update","volume":"19","author":"Jagerstad","year":"2000","journal-title":"J. Am. Coll. Nutr."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"118","DOI":"10.3390\/nu3010118","article-title":"Folate production by probiotic bacteria","volume":"3","author":"Rossi","year":"2011","journal-title":"Nutrients"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"430","DOI":"10.1016\/j.foodchem.2012.10.075","article-title":"Influence of flour blend composition on fermentation kinetics and phytate hydrolysis of sourdough used to make injera","volume":"138","author":"Baye","year":"2013","journal-title":"Food Chem."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"2881","DOI":"10.1007\/s13197-012-0745-5","article-title":"Teff (Eragrostis tef) as a raw material for malting, brewing and manufacturing of gluten-free foods and beverages: A review","volume":"51","author":"Gebremariam","year":"2014","journal-title":"J. Food Sci. Technol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1016\/j.jcs.2019.04.005","article-title":"Quantification of folate in the main steps of traditional processing of tef injera, a cereal based fermented staple food","volume":"87","author":"Tamene","year":"2019","journal-title":"J. Cereal Sci."},{"key":"ref_18","first-page":"S1","article-title":"The assessment of bioavailability of micronutrients: Introduction","volume":"51","author":"Jackson","year":"1997","journal-title":"Eur. J. Clin. Nutr."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1079\/NRR200126","article-title":"Bioavailability and bioefficacy of folate and folic acid in man","volume":"14","author":"Brouwer","year":"2001","journal-title":"Nutr. Res. Rev."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"2742","DOI":"10.1093\/jn\/137.12.2742","article-title":"Administration of folate-producing Bifidobacteria enhances folate status in Wistar rats","volume":"137","author":"Pompei","year":"2007","journal-title":"J. Nutr."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"835","DOI":"10.1016\/j.nut.2009.06.023","article-title":"Supplementation with engineered Lactococcus lactis improves the folate status in deficient rats","volume":"26","author":"LeBlanc","year":"2010","journal-title":"Nutrition"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"134","DOI":"10.1094\/CCHEM.2004.81.1.134","article-title":"Effect of baking method and fermentation on folate content of rye and wheat breads","volume":"81","author":"Kariluoto","year":"2004","journal-title":"Cereal Chem."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"8722","DOI":"10.1128\/AEM.05988-11","article-title":"Genetic screening of functional properties of lactic acid bacteria in a fermented pearl millet slurry and in the metagenome of fermented starchy foods","volume":"77","author":"Turpin","year":"2011","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"4801","DOI":"10.1073\/pnas.75.10.4801","article-title":"Complete nucleotide sequence of a 16S ribosomal RNA gene from Escherichia coli","volume":"75","author":"Brosius","year":"1978","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1016\/S0723-2020(00)80014-4","article-title":"Molecular diversity of Leuconostoc mesenteroides and Leuconostoc citreum isolated from traditional French cheeses as revealed by RAPD fingerprinting, 16S rDNA Sequencing and 16S rDNA fragment amplification","volume":"23","author":"Cibik","year":"2000","journal-title":"Syst. Appl. Microbiol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"697","DOI":"10.1128\/jb.173.2.697-703.1991","article-title":"16S ribosomal DNA amplification for phylogenetic study","volume":"173","author":"Weisburg","year":"1991","journal-title":"J. Bacteriol."},{"key":"ref_27","unstructured":"National Research Council (2011). Guide for the Care and Use of Laboratory Animals."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1023\/A:1008824500612","article-title":"Effect of heat treatment on the antimicrobial properties of tef dough, injera, kocho and aradisame and the fate of selected pathogens","volume":"14","author":"Nigatu","year":"1997","journal-title":"World J. Microbiol. Biotechnol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/S0733-5210(89)80027-X","article-title":"Lactic acid and volatile (C2-C6) fatty acid production in the fermentation and baking of tef (Eragrostis tef)","volume":"9","author":"Umeta","year":"1989","journal-title":"J. Cereal Sci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1016\/j.ijfoodmicro.2014.08.018","article-title":"Phytic acid degrading lactic acid bacteria in tef-injera fermentation","volume":"190","author":"Fischer","year":"2014","journal-title":"Int. J. Food Microbiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"911","DOI":"10.1093\/ajcn\/80.4.911","article-title":"Determining bioavailability of food folates in a controlled intervention study","volume":"80","author":"Armstrong","year":"2004","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1095","DOI":"10.1016\/j.foodchem.2006.03.009","article-title":"Retention of folates in cooked, stored and reheated peas, broccoli and potatoes for use in modern large-scale service systems","volume":"101","author":"Stea","year":"2007","journal-title":"Food Chem."}],"container-title":["Nutrients"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-6643\/11\/11\/2819\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T13:35:23Z","timestamp":1760189723000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-6643\/11\/11\/2819"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,11,18]]},"references-count":32,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2019,11]]}},"alternative-id":["nu11112819"],"URL":"https:\/\/doi.org\/10.3390\/nu11112819","relation":{},"ISSN":["2072-6643"],"issn-type":[{"value":"2072-6643","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,11,18]]}}}