Caracterización in vitro de propiedades probióticas de Lactobacillus ssp. aislados del tracto digestivo de abejas

Contenido principal del artículo

José Antonio Rodríguez Díaz
Juan Emilio Hernández García
Laureano Sebastián Frizzo
Ken Jact Fernández León
Lilian Sánchez
Yovanni Solenzal Valdivia

Resumen

El presente trabajo tuvo como objetivo caracterizar in vitro bacterias ácido lácticas (Fructobacillus fructosus SS66, Lactococcus garvieae SS79, Fructobacillus fructosus SS72, Lactobacillus kunkeei SS70, Lactobacillus rhamnosus SS73), aisladas del tracto digestivo de abejas Apis mellifera. Se evaluó su capacidad probiótica mediante pruebas enzimáticas, estabilidad de crecimiento a diferentes temperaturas (37 y 45°C) y a un rango de pH (3,5; 4,5; 5,5; 6,5), tolerancia a jugo gástrico artificial (JGA), sales biliares (0,3, 05 y 1 %); pruebas de adherencia como agregación, autoagregación e hidrofobicidad y antagonismo microbiano. Los resultados mostraron que todas las cepas crecieron a 37°C a pH ácido 6,5 y 5,5; no crecieron a pH 4,5, produjeron peróxido de hidrógeno y no revelaron actividad hemolítica. Las cepas soportaron el JGA pH 3 durante 3 h a 37°C y a las sales biliares hasta 1 %. Ninguna cepa mostró poder de autoagregación y solo dos (L. rhamnosus SS73 y L. kunkeei SS70) produjeron coagregación contra Escherichia coli. La hidrofobicidad fue variable entre las cepas, F. fructosus SS72 exhibió un valor alto, L. rhamnosus SS73 y L. kunkeei SS70 medio y L. garvieae SS79 y F. fructosus SS66 bajo. Todas las cepas presentaron amplio espectro de actividad antimicrobiana y efecto inhibitorio frente a Paenibacillus larvae y otros patógenos humanos y animales. Las cepas que mejor comportamiento mostraron corresponden a L. kunkeei SS70 y L rhamnosus SS73; fueron susceptibles a los agentes antimicrobianos utilizados con excepción de la Sulfonamida y Vancomicina y, a partir de estos resultados, se podrán incorporar en un inóculo probiótico para evaluar su efecto in vivo.

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Cómo citar
Rodríguez Díaz, J. A., Hernández García, J. E., Sebastián Frizzo, L., Fernández León, K. J., Sánchez, L., & Solenzal Valdivia, Y. (2021). Caracterización in vitro de propiedades probióticas de Lactobacillus ssp. aislados del tracto digestivo de abejas. Revista De Salud Animal, 43(2). Recuperado a partir de http://revistas.censa.edu.cu/index.php/RSA/article/view/1162
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Hudson JA, Frewer LJ, Jones G, Brereton PA, Whittingham MJ, Stewart G. The agri-food chain and antimicrobial resistance. Trends in Food Science and Technology. 2017.

Aidara-Kane A, Angulo FJ, Conly JM, Minato Y, Silbergeld EK, McEwen SA, et al. World Health Organization (WHO) guidelines on use of medically important antimicrobials in food-producing animals. Antimicrobial Resistance & Infection Control. 2018;7(1):7.

Gao P, Ma C, Sun Z, Wang L, Huang S, Su X, et al. Feed-additive probiotics accelerate yet antibiotics delay intestinal microbiota maturation in broiler chicken. Microbiome. 2017;5(1):91.

Tonello NV. Caracterización de nuevos medicamentos no contaminantes para el tratamiento de enfermedades apícolas [Doctoral]. Argentina: Universidad Nacional de Rio Cuarto; 2019.

Bonilla-Rosso G, Engel P. Functional roles and metabolic niches in the honey bee gut microbiota. Current opinion in microbiology. 2018;43:69-76.

Zheng H, Powell JE, Steele MI, Dietrich C, Moran NA. Honeybee gut microbiota promotes host weight gain via bacterial metabolism and hormonal signaling. PNAS. 2017;114(18):4775–80.

Kwong WK, Mancenido AL, Moran NA. Immune system stimulation by the native gut microbiota of honey bees. R Soc open sci. 2017;4:1-9.

Engel P, Moran NA. The gut microbiota of insects – diversity in structure and function. FEMS Microbiol Ecol. 2013;37:699-735.

Budge GE, Adams I, Thwaites R, Pietravalle S, Drew GC, Hurst GDD, et al. Identifying bacterial predictors of honey bee health. Journal of Invertebrate Pathology. 2016:1-19.

Engel P, Kwong WK, McFrederick Q, Anderson KE, Barribeau SM, Chandler JA, et al. The Bee Microbiome: Impact on bee health and model for evolution and ecology of host-microbe interactions. Mbioasmorg. 2016;7(2):1-9.

Khalafalla GM, Sadik MW, Ali MAM, Mohamed RS. Novel potential probiotics from gut microbiota of honeybees (Apis mellifera) in clover feeding season in Egypt. Plant Archives. 2019;19(2):3381-3389.

Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, et al. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nature reviews Gastroenterology & hepatology. 2014;11(8):506.

Markowiak P, Śliżewska K. The role of probiotics, prebiotics and synbiotics in animal nutrition. Gut pathogens. 2018;10(1):21.

Miranda-Yuquilema JE, Marin-Cárdenas A, Sánchez-Macías D, García-Hernández Y. Obtención, caracterización y evaluación de dos preparados candidatos a probióticos desarrollados con residuos agroindustriales. Revista MVZ Córdoba. 2018:6487-6499.

Yao W, Yang L, Shao Z, Xie L, Chen L. Identification of salt tolerance-related genes of Lactobacillus plantarum D31 and T9 strains by genomic analysis. Annals of Microbiology. 2020;70(1):1-14.

Alberoni D, Baffoni L, Gaggìa F, Ryan P, Murphy K, Ross P, et al. Impact of beneficial bacteria supplementation on the gut microbiota, colony development and productivity of Apis mellifera L. Beneficial microbes. 2018;9(2):269-278.

Khare A, Thorat G, Bhimte A, Yadav V. Mechanism of action of prebiotic and probiotic. immunity (Choct, 2009; Williams et al, 2001). 2018;3:27.

Sánchez L, Omura M, Lucas A, Pérez T, Llanes M, Ferreira C. Cepas de Lactobacillus spp. con capacidades probióticas aisladas del tracto intestinal de terneros neonatos. Rev Salud Anim. 2015;32(2):11.

Thakur N, Rokana N, Panwar H. Probiotics, Selection criteria, safety and role in health and. Journal of Innovative Biology January. 2016;3(1):259-270.

FAO/WHO. WHO works group report on drafting guidelines for the evaluation of probiotics in food London. Ontario, Canada, April. 2002;30.

Audisio MC. Gram-Positive bacteria with probiotic potential for the Apis mellifera L. honey bee: The Experience in the Northwest of Argentina. Probiotics & Antimicro Prot. 2016:1-10.

Daisley BA, Pitek AP, Chmiel JA, Al KF, Chernyshova AM, Faragalla KM, et al. Novel probiotic approach to counter Paenibacillus larvae infection in honey bees. The ISME journal. 2020 14(2):476-491.

Hernández García JE, Rodríguez Díaz JA, Sebastián Frizzo L, Fernández León KJ, Solenzal Y, Paola Soto L, et al. Aislamiento e identificación de bacterias ácido lácticas del tracto digestivo de abejas adultas Apis mellifera. Rev Salud Anim. 2020;42(2):9.

Harrigan WF. Laboratory methods in food microbiology: Gulf professional publishing; 1998.

Mclean NW, Rosenstein IJ. Characterisation and selection of a Lactobacillus species to re-colonise the vagina of women with recurrent bacterial vaginosis. Journal of medical microbiology. 2000; 49(6):543-552.

Hernández-García JE, Sebastián-Frizzo L, Rodríguez-Fernández JC, Valdez-Paneca G, Virginia-Zbrun M, Calero-Herrera I. Evaluación in vitro del potencial probiótico de Lactobacillus acidophilus SS80 y Streptococcus thermophilus SS77. Rev Salud Anim. 2019;41(1).

Balamurugan R, Chandragunasekaran AS, Chellappan G, Rajaram K, Ramamoorthi G, Ramakrishna BS. Probiotic potential of lactic acid bacteria present in homemade curd in southern India. The Indian journal of medical research. 2014;140(3):345.

Mete A, Coşansu S, Demirkol O, Ayhan K. Amino acid decarboxylase activities and biogenic amine formation abilities of lactic acid bacteria isolated from shalgam. International Journal of Food Properties. 2017;20(1):171-178.

Uriot O, Denis S, Junjua M, Roussel Y, Dary-Mourot A, Blanquet-Diot S. Streptococcus thermophilus: From yogurt starter to a new promising probiotic candidate? Journal of Functional Foods. 2017;37:74-89.

Bao Y, Zhang Y, Zhang Y, Liu Y, Wang S, Dong X, et al. Screening of potential probiotic properties of Lactobacillus fermentum isolated from traditional dairy products. Food Control. 2010;21(5):695-701.

Reniero R, Coocconcelli P, Bottazzi V, MorellI L. High frequency of conjugation in Lactobacillus mediated by an aggregation-promoting factor. Journal of General Microbiology 1992;138:763-768.

Maldonado NC, Ficoseco CA, Mansilla FI, Melián C, Hébert EM, Vignolo GM, et al. Identification, characterization and selection of autochthonous lactic acid bacteria as probiotic for feedlot cattle. Livestock science. 2018;212:99-110.

Reid G, Bruce AW. Probiotics to prevent urinary tract infections: the rationale and evidence. World journal of urology. 2006;24(1):28-32.

Frizzo LS, Soto LP, Bertozz I, Sequeira G, Marti LE, Rosmini MR. Evaluación in vitro de las capacidades probióticas microbianas orientadas al diseño de inóculos probióticos multiespecie para ser utilizados en la crianza de terneros. Revista FAVE-Ciencias Veterinarias. 2006;5.

Nader-Macías MEF, Otero MC, Espeche MC, Maldonado NC. Advances in the design of probiotic products for the prevention of major diseases in dairy cattle. Journal of industrial microbiology and biotechnology. 2008;35(11):1387-1395.

Kajal A, Ankur G, Jagriti S. Isolation and identification of Lactobacilli bacteria from raw cow milk in local region of Agra. Int J Adv Res Biol Sci. 2017;4(11):98-102.

Fleming H, Etchells J, Costilow R. Microbial inhibition by an isolate of Pediococcus from cucumber brines. Applied Microbiology. 1975;30(6):1040-1042.

Iorizzo M, Testa B, Lombardi SJ, Ganassi S, Ianiro MFL, et al. Antimicrobial activity against Paenibacillus larvae and functional properties of Lactiplantibacillus plantarum strains: Potential benefits for honeybee health. Antibiotics. 2020;9(442):2-18.

Schillinger U. Antibacterial activity of Lactobacillus sake isolated from meat. Applied and environmental microbiology. 1989;55(8):1901-1906.

Charteris WP, Kelly PM, Morelli L, Collins JK. Antibiotic susceptibility of potentially probiotic Lactobacillus species. Journal of Food Protection. 1998;6(12):1636-1643.

Laurencio-Silva M, Arteaga F, Rondón-Castillo AJ, Ormaza J, Pinto J, Pazmiño D, et al. Potencial probiótico in vitro de cepas de Lactobacillus spp. procedentes de la vagina de vacas lecheras. Pastos y Forrajes. 2017;40(3):206-215.

Peres CM, Alves M, Hernandez-Mendoza A, Moreira L, Silva S, Bronze MR, et al. Novel isolates of lactobacilli from fermented Portuguese olive as potential probiotics. LWT-Food Science and Technology. 2014;59(1):234-246.

Matthews A, Grimaldi A, Walker M, Bartowsky E, Grbin P, Jiranek V. Lactic acid bacteria as a potential source of enzymes for use in vinification. Appl Environ Microbiol. 2004;70(10):5715-5731.

Aimutis WR. Bioactive properties of milk proteins with particular focus on anticariogenesis. The Journal of nutrition. 2004;134(4):989S-995S.

Ávila J, Ávila M, Tovar B, Brizuela M, Perazzo Y, Hernández H. Capacidad probiótica de cepas del género Lactobacillus extraídas del tracto intestinal de animales de granja. Revista Científica. 2010;20(2):161-169.

Landa-Salgado P, Caballero-Cervantes Y, Ramírez-Bribiesca E, Hernández-Anguiano AM, Ramírez-Hernández LM, Espinosa-Victoria D, et al. Aislamiento e identificación de bacterias ácido lácticas con potencial probiótico para becerros del altiplano mexicano. Revista mexicana de ciencias pecuarias. 2019;10(1):68-83.

Elenany Y, Sharaf El-Din H. Detection and Identification of novel bacterial strains isolated from fresh clover bee honey. Journal of Plant Protection and Pathology. 2019;10(1):49-52.

Iranmanesh M, Ezzatpanah H, Mojgani N. Antibacterial activity and cholesterol assimilation of lactic acid bacteria isolated from traditional Iranian dairy products. LWT-food Science and Technology. 2014;58(2):355-359.

De Vuyst L, Moreno MF, Revets H. Screening for enterocins and detection of hemolysin and vancomycin resistance in enterococci of different origins. Int J Food Microbiol. 2003;84(3):299-318.

Gutiérrez RLA, David RCA, Montoya COI, Betancur GE. Efecto de la inclusión en la dieta de probióticos microencapsulados sobre algunos parámetros zootécnicos en alevinos de tilapia roja (Oreochromis sp.). Rev Salud Anim. 2016;38(2):8.

Ruiz-Moyano S, Martín A, Benito MJ, Casquete R, Serradilla MJ, de Guía Córdoba M. Safety and functional aspects of pre-selected lactobacilli for probiotic use in Iberian dry-fermented sausages. Meat science. 2009;83(3):460-467.

Hazards EPoB. EFSA Panel on Biological Hazards (BIOHAZ). Scientific opinion on risk based control of biogenic amine formation in fermented foods. Efsa Journal. 2011;9(10):2393-2486.

Ladero Losada VM, Martín MC, Redruello B, Mayo Pérez B, Flórez García AB, Fernández García M, et al. Genetic and functional analysis of biogenic amine production capacity among starter and non-starter lactic acid bacteria isolated from artisanal cheeses. 2015.

Pereira C, Crespo MB, San Romao M. Evidence for proteolytic activity and biogenic amines production in Lactobacillus curvatus and L. homohiochii. Int J Food Microbiol. 2001;68(3):211-216.

Tarrah A, Castilhos J, Rochele Cassanta R R, Da Silva V D, Righetto D Z, Corich V, et al. In vitro probiotic potential and anti-cancer activity of newly isolated folate-producing Streptococcus thermophilus strains. Frontiers in Microbiology. 2018;9:1-11.

Gilliland S, Staley T, Bush L. Importance of bile tolerance of Lactobacillus acidophilus used as a dietary adjunct. Journal of dairy science. 1984;67(12):3045-3051.

Jurado-Gámez H, Martínez BJA, Chaspuengal TA, Calpa FY. Evaluation in vitro of the action of Lactobacillus plantarum with probiotic characteristics on Yersinia pseudotuberculos. Biotecnología en el Sector Agropecuario y Agroindustrial. 2014;12(2):49-59.

Kenfack CHM, Kaktcham PM, Ngoufack FZ, Wang YR, Yin L, Zhu T. Screening and characterization of putative probiotic Lactobacillus strains from honey bee gut (Apis mellifera). J Advances in Microbiology. 2018:1-18.

Meryandini A, Karyawati AT, Nuraida L, Lestari Y. Lactic Acid Bacteria from Apis dorsata hive possessed probiotic and Angiotensin-Converting Enzyme Inhibitor Activity. Makara Jof Science. 2020;24(1):7.

Tuo Y, Yu H, Ai L, Wu Z, Guo B, Chen W. Aggregation and adhesion properties of 22 Lactobacillus strains. J dairy science. 2013;96(7):4252-4257.

Goel A, Halami PM, Tamang JP. Genome Analysis of Lactobacillus plantarum isolated from some Indian fermented foods for Bacteriocin production and probiotic marker genes. Frontiers in microbiology. 2020;11.

TR K. Probiotic potency of Lactobacillus plantarum KX519413 and KX519414 isolated from honey bee gut. FEMS microbiology letters. 2018;365(4):285.

Dlamini ZC, Langa RL, Aiyegoro OA, Okoh AI. Safety evaluation and colonisation abilities of four lactic acid bacteria as future probiotics. Probiotics and antimicrobial proteins. 2019;11(2):397-402.

Elshaghabee FM, Rokana N, Gulhane RD, Sharma C, Panwar H. Bacillus as potential probiotics: status, concerns, and future perspectives. Frontiers in microbiology. 2017;8:1490.

Audisio MC, Torres MJ, Sabaté DC, Ibarguren C, Apella MC. Properties of different lactic acid bacteria isolated from Apis mellifera L. bee-gut. Microbiological research. 2011;166(1):1-13.

UĞRAŞ S. Isolation, identification and characterization of probiotic properties of bacterium from the honey stomachs of Yigilca honeybees in Turkey. Türkiye Entomoloji Dergisi. 2017;41(3):253-261.

Putri I, Jannah SN, Purwantisari S. Isolation and characterization of lactic acid bacteria from Apis mellifera and their potential as antibacterial using in vitro test against growth of Listeria monocytogenes and Escherichia coli. NICHE J of Tropical Biology. 2020;3(1):26-34.

Saleh G. Isolation and characterization of unique fructophilic lactic acid bacteria from different flower sources. Iraqi Journal of Agricultural Science. 2020;51(2):508-518.

Al-Ghamdi A, Al-Abbadi AA, Khan KA, Ghramh HA, Ahmed AM, Ansari MJ. In vitro antagonistic potential of gut bacteria isolated from indigenous honey bee race of Saudi Arabia against Paenibacillus larvae. Journal of Apicultural Research. 2020:1-9.

Yoshiyama M, Wu M, Sugimura Y, Takaya N, Kimoto-Nira H, Suzuki C. Inhibition of Paenibacillus larvae by lactic acid bacteria isolated from fermented materials. Journal of invertebrate pathology. 2013;112(1):62-67.

Janashia I, Choiset Y, Jozefiak D, Déniel F, Coton E, Moosavi-Movahedi AA, et al. Beneficial protective role of endogenous lactic acid bacteria against mycotic contamination of honeybee beebread. Probiotics and antimicrobial proteins. 2018;10(4):638-646.

Kačániová M, Kunová S, Ivanišová E, Terentjeva M, Gasper J. Antimicrobial effect of Lactobacillus kunkeei against pathogenic bacteria isolated from bees' gut. Scientific Papers: Animal Science & Biotechnologies/Lucrari Stiintifice: Zootehnie si Biotehnologii. 2019;52(2).

Olofsson TC, Vásquez A. Detection and identification of a novel lactic acid bacterial flora within the honey stomach of the honeybee Apis mellifera. Current microbiology. 2008;57(4):356-363.

Tajabadi N, Mardan M, Manap MYA, Shuhaimi M, Meimandipour A, Nateghi L. Detection and identification of Lactobacillus bacteria found in the honey stomach of the giant honeybee Apis dorsata. Apidologie. 2011;42(5):642.

Sánchez L, Omura M, Lucas A, Pérez T, Llanes M, Ferreira CdL. Cepas de Lactobacillus spp. con capacidades probióticas aisladas del tracto intestinal de terneros neonatos. Rev Salud Animal. 2015;37(2):94-104.

Gharehyakheh S, HosseinElhamirad A, Nateghi L, Varmira K. Evaluation of resistance to conventional antibiotics in medicine by 5 strains of Lactic Acid Bacteria isolated from the stomach of honey bee. Asian Journal of Biological and Life Sciences. 2017;6(3).

Anisimova EA, Yarullina DR. Antibiotic resistance of Lactobacillus strains. Current microbiology. 2019;76(12):1407-1416.

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