{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,13]],"date-time":"2026-01-13T08:14:10Z","timestamp":1768292050853,"version":"3.49.0"},"reference-count":30,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2022,1,14]],"date-time":"2022-01-14T00:00:00Z","timestamp":1642118400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2022,1,14]],"date-time":"2022-01-14T00:00:00Z","timestamp":1642118400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"Conacyt","award":["A1-S-21955"],"award-info":[{"award-number":["A1-S-21955"]}]},{"DOI":"10.13039\/100016928","name":"instituto nacional de pediatria","doi-asserted-by":"crossref","award":["2012\/013 and 2020\/039"],"award-info":[{"award-number":["2012\/013 and 2020\/039"]}],"id":[{"id":"10.13039\/100016928","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Vet Res"],"published-print":{"date-parts":[[2022,12]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:sec><jats:title>Background<\/jats:title><jats:p>Currently, more than 300 genotypes of<jats:italic>Toxoplasma gondii<\/jats:italic>(<jats:italic>T. gondii)<\/jats:italic>have been described throughout the world, demonstrating its wide genetic diversity. The<jats:italic>SAG3<\/jats:italic>locus is one of the genes included in the genotyping panel of this parasite. It is associated with its virulence since it participates during the invasion process of the host cells. Therefore, cloning, sequencing, and bioinformatic analysis were used to deepen the understanding of the<jats:italic>SAG3<\/jats:italic>locus genetic diversity of<jats:italic>T. gondii<\/jats:italic>in blood samples from feral cats.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>Six different<jats:italic>SAG3<\/jats:italic>sequences were detected, five of which were detected in one feline. Three sequences were first reported here; one of them was an intragenic recombinant. In the cladogram, four out of ten<jats:italic>SAG3<\/jats:italic>sequences did not share nodes with others reported worldwide.<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusions<\/jats:title><jats:p>Cloning and sequencing of samples with more than one restriction pattern by PCR-RFLP were very helpful tools to demonstrate the presence of more than three genotypes of<jats:italic>T. gondii<\/jats:italic>in the blood of feral cats from southeastern Mexico. This suggests a potential mixed infection of multiple<jats:italic>T. gondii<\/jats:italic>strains and high genetic diversity of the parasites in felines in this tropical region of Mexico.<\/jats:p><\/jats:sec>","DOI":"10.1186\/s12917-021-03129-9","type":"journal-article","created":{"date-parts":[[2022,1,14]],"date-time":"2022-01-14T06:18:08Z","timestamp":1642141088000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":7,"title":["SAG3 Toxoplasma gondii cloning reveals unexpected fivefold infection in the blood of feral cats in the Mexican Caribbean"],"prefix":"10.1186","volume":"18","author":[{"given":"Luis Fernando","family":"Valenzuela-Moreno","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sara Teresa","family":"M\u00e9ndez-Cruz","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Claudia Patricia","family":"Rico-Torres","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Carlos","family":"Cedillo-Pel\u00e1ez","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Dolores","family":"Correa","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4269-8251","authenticated-orcid":false,"given":"Heriberto","family":"Caballero-Ortega","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2022,1,14]]},"reference":[{"key":"3129_CR1","doi-asserted-by":"publisher","first-page":"e1006351","DOI":"10.1371\/journal.ppat.1006351","volume":"13","author":"OA Mendez","year":"2017","unstructured":"Mendez OA, Koshy AA. Toxoplasma gondii: Entry, association, and physiological influence on the central nervous system. PLoS Pathog. 2017;13:e1006351.","journal-title":"PLoS Pathog"},{"key":"3129_CR2","doi-asserted-by":"publisher","first-page":"82","DOI":"10.1186\/s13071-020-3954-1","volume":"13","author":"M Montazeri","year":"2020","unstructured":"Montazeri M, Mikaeili Galeh T, Moosazadeh M, Sarvi S, Dodangeh S, Javidnia J, et al. The global serological prevalence of Toxoplasma gondii in felids during the last five decades (1967\u20132017): a systematic review and meta-analysis. Parasit Vectors. 2020;13:82.","journal-title":"Parasit Vectors"},{"key":"3129_CR3","doi-asserted-by":"crossref","first-page":"51","DOI":"10.24425\/pjvs.2021.136792","volume":"1","author":"KM Ali","year":"2021","unstructured":"Ali KM, Abu-Seida AM, Abuowarda M. Feline ocular toxoplasmosis: Seroprevalence, diagnosis and treatment outcome of 60 clinical cases. Pol J Vet Sci. 2021;1:51\u201361.","journal-title":"Pol J Vet Sci"},{"key":"3129_CR4","doi-asserted-by":"publisher","first-page":"925","DOI":"10.1016\/j.ijpara.2009.02.005","volume":"39","author":"ME Grigg","year":"2009","unstructured":"Grigg ME, Sundar N. Sexual recombination punctuated by outbreaks and clonal expansions predicts Toxoplasma gondii population genetics. Int J Parasitol. 2009;39:925\u201333.","journal-title":"Int J Parasitol"},{"key":"3129_CR5","doi-asserted-by":"publisher","first-page":"587","DOI":"10.1007\/s00436-019-06523-3","volume":"119","author":"A Vilares","year":"2020","unstructured":"Vilares A, Borges V, Sampaio D, Ferreira I, Martins S, Vieira L, et al. Towards a rapid sequencing-based molecular surveillance and mosaicism investigation of Toxoplasma gondii. Parasitol Res. 2020;119:587\u201399.","journal-title":"Parasitol Res"},{"key":"3129_CR6","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1016\/j.ijpara.2018.11.004","volume":"49","author":"L Galal","year":"2019","unstructured":"Galal L, Schares G, Stragier C, Vignoles P, Brouat C, Cuny T, et al. Diversity of Toxoplasma gondii strains shaped by commensal communities of small mammals. Int J Parasitol. 2019a;49:267\u201375.","journal-title":"Int J Parasitol"},{"key":"3129_CR7","doi-asserted-by":"publisher","first-page":"199","DOI":"10.1016\/j.actatropica.2019.03.006","volume":"193","author":"LF Valenzuela-Moreno","year":"2019","unstructured":"Valenzuela-Moreno LF, Rico-Torres CP, Cedillo-Pel\u00e1ez C, Luna-Past\u00e9n H, M\u00e9ndez-Cruz ST, Lara-Mart\u00ednez G, et al. Mixed Toxoplasma gondii infection and new genotypes in feral cats of Quintana Roo, M\u00e9xico. Acta Trop. 2019;193:199\u2013205.","journal-title":"Acta Trop"},{"key":"3129_CR8","doi-asserted-by":"publisher","first-page":"85","DOI":"10.1016\/j.ijpara.2019.12.001","volume":"50","author":"LF Valenzuela-Moreno","year":"2020","unstructured":"Valenzuela-Moreno LF, Rico-Torres CP, Cedillo-Pel\u00e1ez C, Luna-Past\u00e9n H, M\u00e9ndez-Cruz ST, Reyes-Garc\u00eda ME, et al. Stray dogs in the tropical state of Chiapas, Mexico, harbour atypical and novel genotypes of Toxoplasma gondii. Int J Parasitol. 2020a;50:85\u201390.","journal-title":"Int J Parasitol"},{"key":"3129_CR9","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1016\/j.mib.2006.06.017","volume":"10","author":"V Carruthers","year":"2007","unstructured":"Carruthers V, Boothroyd JC. Pulling together: an integrated model of Toxoplasma cell invasion. Curr Opin Microbiol. 2007;10:83\u20139.","journal-title":"Curr Opin Microbiol"},{"key":"3129_CR10","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1128\/mBio.02280-14","volume":"6","author":"KD Jensen","year":"2015","unstructured":"Jensen KD, Camejo A, Melo M, Cordeiro C, Julien L, Grotenbreg G, et al. Toxoplasma gondii superinfection and virulence during secondary infection correlate with the exact ROP5\/ROP18 allelic combination. MBio. 2015;6:1\u201315.","journal-title":"MBio."},{"key":"3129_CR11","doi-asserted-by":"publisher","first-page":"124","DOI":"10.1016\/j.actatropica.2017.11.008","volume":"178","author":"CP Rico-Torres","year":"2018","unstructured":"Rico-Torres CP, Valenzuela-Moreno LF, Luna-Past\u00e9n H, Figueroa-Dami\u00e1n R, G\u00f3mez-Toscano V, Hern\u00e1ndez-Delgado L, et al. High heterogeneity, mixed infections and new genotypes in human congenital toxoplasmosis cases in the mega-metropolis of Central Mexico. Acta Trop. 2018;178:124\u20139.","journal-title":"Acta Trop"},{"key":"3129_CR12","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.ijppaw.2020.07.005","volume":"13","author":"LF Valenzuela-Moreno","year":"2020","unstructured":"Valenzuela-Moreno LF, Cedillo-Pel\u00e1ez C, Rico-Torres CP, Hern\u00e1ndez-Rodr\u00edguez MA, Carmona-Muci\u00f1o M Del C, Farf\u00e1n-Morales JE, et al. Toxoplasma gondii infection in European mouflons (Ovis musimon) and captive wild felines from Puebla, M\u00e9xico. Int J Parasitol Parasites Wildl. 2020b;13:1\u20136.","journal-title":"Int J Parasitol Parasites Wildl"},{"key":"3129_CR13","doi-asserted-by":"publisher","first-page":"463","DOI":"10.1016\/j.parint.2013.10.012","volume":"63","author":"V S\u00e1nchez","year":"2014","unstructured":"S\u00e1nchez V, De-la-Torre A, G\u00f3mez-Mar\u00edn JE. Characterization of ROP18 alleles in human toxoplasmosis. Parasitol Int. 2014;63:463\u20139.","journal-title":"Parasitol Int"},{"key":"3129_CR14","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1016\/S0020-7519(02)00230-8","volume":"33","author":"TV Aspinall","year":"2003","unstructured":"Aspinall TV, Guy EC, Roberts KE, Joynson DHM, Hyde JE, Sims PFG. Molecular evidence for multiple Toxoplasma gondii infections in individual patients in England and Wales: public health implications. Int J Parasitol. 2003;33:97\u2013103.","journal-title":"Int J Parasitol"},{"key":"3129_CR15","first-page":"191","volume":"14","author":"AI Cubas-Atienzar","year":"2018","unstructured":"Cubas-Atienzar AI, Hide G, Jim\u00e9nez-Coello M, Ortega-Pacheco A, Smith JE. Genotyping of Toxoplasma gondii from pigs in Yucatan, Mexico. Vet Parasitol Reg Stud Reports. 2018;14:191\u20139.","journal-title":"Vet Parasitol Reg Stud Reports"},{"key":"3129_CR16","doi-asserted-by":"publisher","first-page":"1114","DOI":"10.1093\/nar\/29.5.1114","volume":"29","author":"M Beaulieu","year":"2001","unstructured":"Beaulieu M, Larson GP, Geller L, Flanagan SD, Krontiris TG. PCR candidate region mismatch scanning: Adaptation to quantitative, high-throughput genotyping. Nucleic Acids Res. 2001;29:1114\u201324.","journal-title":"Nucleic Acids Res"},{"key":"3129_CR17","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1016\/j.gene.2008.09.013","volume":"427","author":"TL Lenz","year":"2008","unstructured":"Lenz TL, Becker S. Simple approach to reduce PCR artefact formation leads to reliable genotyping of MHC and other highly polymorphic loci \u2014 Implications for evolutionary analysis. Gene. 2008;427:117\u201323.","journal-title":"Gene."},{"key":"3129_CR18","doi-asserted-by":"publisher","first-page":"857","DOI":"10.2144\/000113219","volume":"47","author":"DJG Lahr","year":"2009","unstructured":"Lahr DJG, Katz LA. Reducing the impact of PCR-mediated recombination in molecular evolution and environmental studies using a new-generation high-fidelity DNA polymerase. Biotechniques. 2009;47:857\u201366.","journal-title":"Biotechniques."},{"key":"3129_CR19","doi-asserted-by":"publisher","first-page":"203","DOI":"10.1016\/j.mimet.2013.03.013","volume":"93","author":"JL Stevens","year":"2013","unstructured":"Stevens JL, Jackson RL, Olson JB. Slowing PCR ramp speed reduces chimera formation from environmental samples. J Microbiol Methods. 2013;93:203\u20135.","journal-title":"J Microbiol Methods"},{"key":"3129_CR20","doi-asserted-by":"crossref","unstructured":"Juliano JJ, Porter K, Mwapasa V, Sem R, Rogers WO, Ariey F, et al. Exposing malaria in-host diversity and estimating population diversity by capture-recapture using massively parallel pyrosequencing. Proc Natl Acad Sci U S A. 2010;107:20138\u201343.","DOI":"10.1073\/pnas.1007068107"},{"key":"3129_CR21","doi-asserted-by":"publisher","first-page":"9027","DOI":"10.1073\/pnas.0901415106","volume":"106","author":"WE Harrington","year":"2009","unstructured":"Harrington WE, Mutabingwa TK, Muehlenbachs A, Sorensen B, Bolla MC, Fried M, et al. Competitive facilitation of drug-resistant Plasmodium falciparum malaria parasites in pregnant women who receive preventive treatment. Proc Natl Acad Sci. 2009;106:9027\u201332.","journal-title":"Proc Natl Acad Sci"},{"key":"3129_CR22","doi-asserted-by":"publisher","first-page":"96","DOI":"10.1016\/j.vetpar.2011.07.018","volume":"182","author":"JM Wendte","year":"2011","unstructured":"Wendte JM, Gibson AK, Grigg ME. Population genetics of Toxoplasma gondii: new perspectives from parasite genotypes in wildlife. Vet Parasitol. 2011;182:96\u2013111.","journal-title":"Vet Parasitol"},{"key":"3129_CR23","first-page":"3","volume-title":"Toxoplasmosis - Recent Advances","author":"E Gilot-Fromont","year":"2012","unstructured":"Gilot-Fromont E, Dard\u00e9 MLM-L, Richomme C, Aubert D, Afonso E, Mercier A, et al. The Life Cycle of Toxoplasma gondii in the Natural Environment. In: Djurkovi\u0107-Djakovi\u0107 O, editor. Toxoplasmosis - Recent Advances: InTech; 2012. p. 3\u201336."},{"key":"3129_CR24","doi-asserted-by":"publisher","first-page":"16001","DOI":"10.1038\/nmicrobiol.2016.1","volume":"1","author":"C Konradt","year":"2016","unstructured":"Konradt C, Ueno N, Christian DA, Delong JH, Pritchard GH, Herz J, et al. Endothelial cells are a replicative niche for entry of Toxoplasma gondii to the central nervous system. Nat Microbiol. 2016;1:16001.","journal-title":"Nat Microbiol"},{"key":"3129_CR25","doi-asserted-by":"publisher","first-page":"e00052","DOI":"10.1016\/j.fawpar.2019.e00052","volume":"15","author":"L Galal","year":"2019","unstructured":"Galal L, Hamidovi\u0107 A, Dard\u00e9 ML, Mercier M. Diversity of Toxoplasma gondii strains at the global level and its determinants. Food Waterborne Parasitol. 2019b;15:e00052.","journal-title":"Food Waterborne Parasitol"},{"key":"3129_CR26","doi-asserted-by":"publisher","first-page":"611","DOI":"10.1016\/j.ijpara.2018.01.008","volume":"48","author":"T Jiang","year":"2018","unstructured":"Jiang T, Shwab EK, Martin RM, Gerhold RW, Rosenthal BM, Dubey JP, et al. A partition of Toxoplasma gondii genotypes across spatial gradients and among host species, and decreased parasite diversity towards areas of human settlement in North America. Int J Parasitol. 2018;48:611\u20139.","journal-title":"Int J Parasitol"},{"key":"3129_CR27","first-page":"21","volume":"9","author":"G Ceballos","year":"2012","unstructured":"Ceballos G, Arroyo-Cabrales J, Medell\u00edn R, Dom\u00ednguez-Castellanos Y. Lista actualizada de los mam\u00edferos de M\u00e9xico. Rev Mex Mastozoolog\u00eda. 2012;9:21\u201371.","journal-title":"Rev Mex Mastozoolog\u00eda"},{"key":"3129_CR28","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1017\/S0031182009991065","volume":"137","author":"C Su","year":"2010","unstructured":"Su C, Shwab EK, Zhou P, Zhu XQ, Dubey JP. Moving towards an integrated approach to molecular detection and identification of Toxoplasma gondii. Parasitology. 2010;137:1\u201311.","journal-title":"Parasitology."},{"key":"3129_CR29","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1109\/IPDPS.2002.1016585","volume-title":"Proceedings 16th International Parallel and Distributed Processing Symposium","author":"M Clement","year":"2002","unstructured":"Clement M, Snell Q, Walke P, Posada D, Crandall K. TCS: estimating gene genealogies. In: Proceedings 16th International Parallel and Distributed Processing Symposium: IEEE; 2002. p. 7."},{"key":"3129_CR30","doi-asserted-by":"publisher","first-page":"627","DOI":"10.1093\/bioinformatics\/btv636","volume":"32","author":"A M\u00farias dos Santos","year":"2016","unstructured":"M\u00farias dos Santos A, Cabezas MP, Tavares AI, Xavier R, Branco M. tcsBU: a tool to extend TCS network layout and visualization. Bioinformatics. 2016;32:627\u20138.","journal-title":"Bioinformatics."}],"container-title":["BMC Veterinary Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12917-021-03129-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s12917-021-03129-9\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12917-021-03129-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,9,16]],"date-time":"2024-09-16T07:52:38Z","timestamp":1726473158000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcvetres.biomedcentral.com\/articles\/10.1186\/s12917-021-03129-9"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,1,14]]},"references-count":30,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2022,12]]}},"alternative-id":["3129"],"URL":"https:\/\/doi.org\/10.1186\/s12917-021-03129-9","relation":{},"ISSN":["1746-6148"],"issn-type":[{"value":"1746-6148","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,1,14]]},"assertion":[{"value":"20 September 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"23 December 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"14 January 2022","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The animal study was reviewed and approved by the Review Board of the Instituto Nacional de Pediatr\u00eda of the Ministry of Health of M\u00e9xico (INP; IRB-NIH numbers IRB00008064 and IRB00008065), which includes the Research and Animal Care Committees (approved protocols 2012\/013 and 2020\/039). The owners of this private collection granted permission for the capture of the feral cats used in this work. These capture actions are part of the annual program for the control of undesired fauna of the eco-archaeological park conducted in accordance with the General Wildlife Law of Mexico (DOF 01-19-2018) and the Official Mexican Standard NOM-033-ZOO-1995.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"33"}}