{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,18]],"date-time":"2026-06-18T09:13:02Z","timestamp":1781773982760,"version":"3.54.5"},"reference-count":46,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2021,7,26]],"date-time":"2021-07-26T00:00:00Z","timestamp":1627257600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"This research was funded by Lombardy Region and European Regional Development Fund (ERDF) under grant: FoodTech Project","award":["(ID: 203370)"],"award-info":[{"award-number":["(ID: 203370)"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Limosilactobacillus reuteri and Lactiplantibacillus plantarum strains, previously isolated from weaned piglets, were considered for the evaluation of their adhesive characteristics. Lactobacilli were treated with LiCl in order to remove the surface protein layer, and probiotic activity was compared with those of untreated strains. The autoaggregation, co-aggregation to E. coli F18+, and adhesive abilities of LiCl-treated Limosilactobacillus reuteri and Lactiplantibacillus plantarum were significantly inhibited (p &lt; 0.05) compared with the respective untreated strain. The hydrophobic and basic phenotypes were observed due to the strong affinity to chloroform and low adherence to ethyl acetate. In particular, L. plantarum showed higher hydrophobicity compared to L. reuteri, which may reflect their different colonizing ability. After treatment with LiCl to remove surface proteins, the adherence capabilities of L. reuteri and L. casei on IPEC-J2 cells decreased significantly (p &lt; 0.001) and L. reuteri adhered more frequently. Sodium dodecyl sulphate-polyacrylamide gel electrophoresis (SDS-PAGE) showed that both L. reuteri and L. plantarum had several bands ranging from 20 to 100 kDa. Two-dimensional gel electrophoresis showed an acidic profile of the surface-layer polypeptides for both bacterial strains, and more studies are needed to characterize their profile and functions. The results confirm the pivotal role of surface proteins in the probiotic potential of L. reuteri and L. plantarum.<\/jats:p>","DOI":"10.3390\/microorganisms9081587","type":"journal-article","created":{"date-parts":[[2021,7,26]],"date-time":"2021-07-26T09:25:52Z","timestamp":1627291552000},"page":"1587","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":21,"title":["Evaluation of Adhesive Characteristics of L. plantarum and L. reuteri Isolated from Weaned Piglets"],"prefix":"10.3390","volume":"9","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-2171-864X","authenticated-orcid":false,"given":"Matteo","family":"Dell\u2019Anno","sequence":"first","affiliation":[{"name":"Department of Health, Animal Science and Food Safety \u201cCarlo Cantoni\u201d (VESPA), Universit\u00e0 Degli Studi di Milano, 26900 Lodi, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3717-5336","authenticated-orcid":false,"given":"Carlotta","family":"Giromini","sequence":"additional","affiliation":[{"name":"Department of Health, Animal Science and Food Safety \u201cCarlo Cantoni\u201d (VESPA), Universit\u00e0 Degli Studi di Milano, 26900 Lodi, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2136-1177","authenticated-orcid":false,"given":"Serena","family":"Reggi","sequence":"additional","affiliation":[{"name":"Department of Health, Animal Science and Food Safety \u201cCarlo Cantoni\u201d (VESPA), Universit\u00e0 Degli Studi di Milano, 26900 Lodi, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5296-4686","authenticated-orcid":false,"given":"Mariagrazia","family":"Cavalleri","sequence":"additional","affiliation":[{"name":"Department of Health, Animal Science and Food Safety \u201cCarlo Cantoni\u201d (VESPA), Universit\u00e0 Degli Studi di Milano, 26900 Lodi, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alessandra","family":"Moscatelli","sequence":"additional","affiliation":[{"name":"Department of Biosciences, Universit\u00e0 Degli Studi di Milano, 20133 Milan, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3724-4116","authenticated-orcid":false,"given":"Elisabetta","family":"Onelli","sequence":"additional","affiliation":[{"name":"Department of Biosciences, Universit\u00e0 Degli Studi di Milano, 20133 Milan, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Raffaella","family":"Rebucci","sequence":"additional","affiliation":[{"name":"Department of Health, Animal Science and Food Safety \u201cCarlo Cantoni\u201d (VESPA), Universit\u00e0 Degli Studi di Milano, 26900 Lodi, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tamil Selvi","family":"Sundaram","sequence":"additional","affiliation":[{"name":"Department of Health, Animal Science and Food Safety \u201cCarlo Cantoni\u201d (VESPA), Universit\u00e0 Degli Studi di Milano, 26900 Lodi, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Simona","family":"Coranelli","sequence":"additional","affiliation":[{"name":"Biotecnologie B.T. 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Appl. Microbiol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/srep09938","article-title":"Dynamic distribution of the gut microbiota and the relationship with apparent crude fiber digestibility and growth stages in pigs","volume":"5","author":"Niu","year":"2015","journal-title":"Sci. Rep."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s40104-015-0014-3","article-title":"Study and use of the probiotic Lactobacillus reuteri in pigs: A review","volume":"6","author":"Hou","year":"2015","journal-title":"J. Anim. Sci. Biotechnol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1080\/09540105.2017.1360254","article-title":"Effects of microencapsulated Lactobacillus plantarum and fructooligosaccharide on growth performance, blood immune parameters, and intestinal morphology in weaned piglets","volume":"29","author":"Wang","year":"2017","journal-title":"Food Agric. Immunol."},{"key":"ref_5","unstructured":"(2003). Regulation EC 1831\/2003. of the European Parliament and of the Council, of 22 September 2003 on Additives for Use in Animal Nutrition (Text with EEA Relevance), Official Journal of the European Union."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"4985","DOI":"10.1128\/AEM.00753-08","article-title":"Ecological Role of Lactobacilli in the Gastrointestinal Tract: Implications for Fundamental and Biomedical Research","volume":"74","author":"Walter","year":"2008","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1016\/j.ifset.2008.10.007","article-title":"Growth and survival of Lactobacillus reuteri RC-14 and Lactobacillus rhamnosus GR-1 in yogurt for use as a functional food","volume":"10","author":"Hekmat","year":"2009","journal-title":"Innov. Food Sci. Emerg. Technol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"613","DOI":"10.3390\/nu3050613","article-title":"Lactobacillus Adhesion to Mucus","volume":"3","author":"Miller","year":"2011","journal-title":"Nutrients"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s41110-016-0007-9","article-title":"Cell surface proteins play an important role in probiotic activities of Lactobacillus reuteri","volume":"41","author":"Singh","year":"2016","journal-title":"Nutrire"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Dell\u2019Anno, M., Callegari, M.L., Reggi, S., Caprarulo, V., Giromini, C., Spalletta, A., Coranelli, S., Rossi, C.A.S., and Rossi, L. (2021). Lac-tobacillus plantarum and Lactobacillus reuteri as Functional Feed Additives to Prevent Diarrhoea in Weaned Piglets. Animals, 11.","DOI":"10.3390\/ani11061766"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1080\/1828051X.2019.1703563","article-title":"In vitro evaluation of antimicrobial and antioxidant activities of algal extracts","volume":"19","author":"Sotira","year":"2020","journal-title":"Ital. J. Anim. Sci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"981","DOI":"10.1046\/j.1365-2672.2003.01915.x","article-title":"Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92","volume":"94","author":"Kos","year":"2003","journal-title":"J. Appl. Microbiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/0927-7765(96)01272-6","article-title":"Microbial adhesion to solvents: A novel method to determine the electron-donor\/electron-acceptor or Lewis acid-base properties of microbial cells","volume":"7","author":"Rault","year":"1996","journal-title":"Colloids Surf. B Biointerfaces"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1016\/j.anaerobe.2013.06.005","article-title":"Adhesive ability means inhibition activities for lactobacillus against pathogens and S-layer protein plays an important role in adhesion","volume":"22","author":"Zhang","year":"2013","journal-title":"Anaerobe"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"24234","DOI":"10.1039\/D0RA03517C","article-title":"In vitro studies of adhesion prop-erties of six lactic acid bacteria isolated from the longevous population of China","volume":"10","author":"Guan","year":"2020","journal-title":"RSC Adv."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"486","DOI":"10.3389\/fmicb.2017.00486","article-title":"Antagonistic activity of Lactobacillus reuteri strains on the adhesion characteristics of selected pathogens","volume":"8","author":"Singh","year":"2017","journal-title":"Front. Microbiol."},{"key":"ref_17","unstructured":"Bonjoch, N.P., and Tamayo, P.R. (2006). Protein Content Quantification by Bradford Method. Handbook of Plant Ecophysiology Techniques, Springer."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"378","DOI":"10.1242\/bio.201410249","article-title":"Characterisation of detergent-insoluble membranes in pollen tubes of Nicotiana tabacum (L.)","volume":"4","author":"Moscatelli","year":"2015","journal-title":"Biol. Open"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"680","DOI":"10.1038\/227680a0","article-title":"Cleavage of structural proteins during the assembly of the head of bacteriophage T4","volume":"227","author":"Laemmli","year":"1970","journal-title":"Nature"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"835","DOI":"10.1002\/1615-9861(200107)1:7<835::AID-PROT835>3.0.CO;2-2","article-title":"A new silver staining apparatus and procedure for matrix-assisted laser desorption\/ionization-time of flight analysis of proteins after two-dimensional electrophoresis","volume":"1","author":"Sinha","year":"2001","journal-title":"Proteomics Int. Ed."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Sotira, S., Dell\u2019Anno, M., Caprarulo, V., Hejna, M., Pirrone, F., Callegari, M.L., Tucci, T.V., and Rossi, L. (2020). Effects of Tributyrin Supplementation on Growth Performance, Insulin, Blood Metabolites and Gut Microbiota in Weaned Piglets. Animals, 10.","DOI":"10.3390\/ani10040726"},{"key":"ref_22","first-page":"81","article-title":"Monitoring of goats\u2019 health status by on-line analysis of milk electrical conductivity","volume":"21","author":"Zaninelli","year":"2015","journal-title":"Large Anim. Rev."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"114519","DOI":"10.1016\/j.anifeedsci.2020.114519","article-title":"Evaluation of leonardite as a feed additive on lipid metabolism and growth of weaned piglets","volume":"266","author":"Hejna","year":"2020","journal-title":"Anim. Feed Sci. Technol."},{"key":"ref_24","unstructured":"FAO, and WHO (2001). Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Prevention, 5, 1\u201310."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1007\/s00203-008-0436-9","article-title":"Adhesion proper-ties of Lactobacillus casei strains to resected intestinal fragments and components of the extracellular matrix","volume":"191","author":"Llopis","year":"2009","journal-title":"Arch. Microbiol."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"\u015ali\u017cewska, K., Chlebicz-W\u00f3jcik, A., and Nowak, A. (2020). Probiotic Properties of New Lactobacillus strains Intended to Be Used as Feed Additives for Monogastric Animals. Probiotics and Antimicrobial Proteins, Springer.","DOI":"10.1007\/s12602-020-09674-3"},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Krausova, G., Hyrslova, I., and Hynstova, I. (2019). In Vitro Evaluation of Adhesion Capacity, Hydrophobicity, and Auto-Aggregation of Newly Isolated Potential Probiotic Strains. Fermentation, 5.","DOI":"10.3390\/fermentation5040100"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1","DOI":"10.4236\/ojvm.2012.21001","article-title":"Experimental Induction of Escherichia coli Diarrhoea in Weaned Piglets","volume":"2","author":"Rossi","year":"2012","journal-title":"Open J. Veter.-Med."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"2939","DOI":"10.4081\/ijas.2014.2939","article-title":"Plant bioreactors for the antigenic hook-associated flgK protein expression","volume":"13","author":"Rossi","year":"2014","journal-title":"Ital. J. Anim. Sci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1007\/s11259-013-9583-9","article-title":"Protective effect of oral administration of transgenic tobacco seeds against verocytotoxic Escherichia coli strain in piglets","volume":"38","author":"Rossi","year":"2014","journal-title":"Veter. Res. Commun."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"4252","DOI":"10.3168\/jds.2013-6547","article-title":"Aggregation and adhesion properties of 22 Lactobacillus strains","volume":"96","author":"Tuo","year":"2013","journal-title":"J. Dairy Sci."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Reggi, S., Giromini, C., Dell\u2019Anno, M., Baldi, A., Rebucci, R., and Rossi, L. (2020). In Vitro Digestion of Chestnut and Quebracho Tannin Extracts: Antimicrobial Effect, Antioxidant Capacity and Cytomodulatory Activity in Swine Intestinal IPEC-J2 Cells. Animals, 10.","DOI":"10.3390\/ani10020195"},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Vergauwen, H., Tambuyzer, B., Jennes, K., DeGroote, J., Wang, W., De Smet, S., Michiels, J., and Van Ginneken, C. (2015). Trolox and Ascorbic Acid Reduce Direct and Indirect Oxidative Stress in the IPEC-J2 Cells, an In Vitro Model for the Porcine Gastrointestinal Tract. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0120485"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1016\/j.vetmic.2011.10.017","article-title":"Porcine IPEC-J2 intestinal epithelial cells in microbiological investigations","volume":"156","author":"Brosnahan","year":"2012","journal-title":"Veter. Microbiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"442","DOI":"10.1111\/j.1365-2672.2006.03086.x","article-title":"Strain-and matrix-dependent adhesion of Lactobacillus plantarum is mediated by proteinaceous bacterial compounds","volume":"102","author":"Tallon","year":"2007","journal-title":"J. Appl. Microbiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1038\/nrmicro2297","article-title":"Host interactions of probiotic bacterial surface molecules: Comparison with commensals and pathogens","volume":"8","author":"Lebeer","year":"2010","journal-title":"Nat. Rev. Genet."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1016\/j.anaerobe.2009.08.002","article-title":"Probiotic properties of Lactobacillus isolates originating from porcine intestine and feces","volume":"16","author":"Malinen","year":"2010","journal-title":"Anaerobe"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"12182","DOI":"10.1021\/jf1035756","article-title":"Expression of Lactobacillus reuteri Pg4 Collagen-Binding Protein Gene in Lactobacillus casei ATCC 393 Increases Its Adhesion Ability to Caco-2 Cells","volume":"58","author":"Hsueh","year":"2010","journal-title":"J. Agric. Food Chem."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"723","DOI":"10.1016\/j.idairyj.2004.01.007","article-title":"Assessment of novel probiotic Lactobacillus casei strains for the production of functional dairy foods","volume":"14","author":"Minelli","year":"2004","journal-title":"Int. Dairy J."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1640","DOI":"10.1016\/j.lwt.2009.05.025","article-title":"In vitro comparison of probiotic properties of Lactobacillus casei Zhang, a potential new probiotic, with selected probiotic strains","volume":"42","author":"Guo","year":"2009","journal-title":"LWT"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"2858","DOI":"10.3389\/fmicb.2018.02858","article-title":"A surface protein from Lactobacillus plantarum increases the adhe-sion of lactobacillus strains to human epithelial cells","volume":"9","author":"Wang","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"5225","DOI":"10.1007\/s00253-013-4962-2","article-title":"Lactobacillus surface layer proteins: Structure, function and applications","volume":"97","author":"Palva","year":"2013","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1471-2164-7-126","article-title":"Lactobacillus plantarum gene clusters encoding putative cell-surface protein complexes for carbohydrate utilization are conserved in specific gram-positive bacteria","volume":"7","author":"Siezen","year":"2006","journal-title":"BMC Genom."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"6128","DOI":"10.1128\/JB.187.17.6128-6136.2005","article-title":"Biodiversity-based identification and functional characterization of the mannose-specific adhesin of Lactobacillus plantarum","volume":"187","author":"Pretzer","year":"2005","journal-title":"J. Bacteriol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"671","DOI":"10.1099\/mic.0.073551-0","article-title":"Role of Lactobacillus reuteri cell and mucus-binding protein A (CmbA) in adhesion to intestinal epithelial cells and mucus in vitro","volume":"160","author":"Jensen","year":"2014","journal-title":"Microbiology"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1007\/s00284-008-9148-2","article-title":"Identification of a Surface Protein from Lactobacillus reuteri JCM1081 That Adheres to Porcine Gastric Mucin and Human Enterocyte-Like HT-29 Cells","volume":"57","author":"Wang","year":"2008","journal-title":"Curr. Microbiol."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/9\/8\/1587\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T06:35:04Z","timestamp":1760164504000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/9\/8\/1587"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,7,26]]},"references-count":46,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2021,8]]}},"alternative-id":["microorganisms9081587"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms9081587","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,7,26]]}}}