Abstract
Probiotics have emerged as biotherapeutic adjuncts to combat neonatal calf gastrointestinal disorders. Therefore, they are considered a suitable alternative to antibiotics for maintaining a healthy and balanced gut microbiota. Hence, the current investigation was carried out to evaluate the effect of autochthonous probiotics on Murrah buffalo calves. Sixteen calves (5-7 days of age) were randomly divided into four groups. Group I served as control (CT), fed a basal diet with no supplementation. Groups II (LR), III (LS), and IV (CS) were supplemented with Limosilactobacillus reuteri BF-E7, Ligilactobacillus salivarius BF-17, and a consortium of both probiotic strains at a rate of 1x108 CFU/g/calf per day along with the basal diet, respectively. Two previously isolated potential probiotic strains, Limosilactobacillus reuteri BF-E7 and Ligilactobacillus salivarius BF-17, were found to be compatible in vitro. Dietary supplementation of probiotics for sixty days significantly increased (P<0.05) dry matter intake (DMI, g/d), average daily gain (ADG, g/d), net body weight gain (kg), feed conversion efficiency (FCE), and structural growth measurements as compared to control. Furthermore, a considerable (P<0.05) increase in the abundance of beneficial intestinal microbiota (lactobacilli and bifidobacteria) was observed along with improvement in fecal biomarkers like lactate and ammonia, immune status, and reduced fecal score. Upon comparative analysis among treatment groups, the results were found to be better in the probiotic consortium fed group compared to the LR and LS treated groups. The present findings conclusively deduced that autochthonous probiotic consortium might serve as potential candidate for fostering performance, immunity, and gut health biomarkers in Murrah buffalo calves.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
All data generated or analysed during this study are included in this published article [and its supplementary information files].
References
Agazzi A, Tirloni E, Stella S, Maroccolo S, Ripamonti B, Bersani C, Caputo JM, Dell’Orto V, Rota N, Savoini G (2014) Effects of species-specific probiotic addition to milk replacer on calf health and performance during the first month of life. Ann Anim Sci 14:101–115. https://doi.org/10.2478/aoas-2013-0089
Alipour MJ, Jalanka J, Pessa-Morikawa T, Kokkonen T, Satokari R, Hynönen U, Iivanainen A, Niku M (2018) The composition of the perinatal intestinal microbiota in cattle. Sci Rep 8(1):1–14. https://doi.org/10.1038/s41598-018-28733-y
Amin N, Schwarzkopf S, Kinoshita A, Tröscher-Mußotter J, Dänicke S, Camarinha-Silva A, Huber K, Frahm J, Seifert J (2021) Evolution of rumen and oral microbiota in calves is influenced by age and time of weaning. Anim Microbiome 3(1):1–15. https://doi.org/10.1186/s42523-021-00095-3
AOAC, 1995. Official Method of Analysis, 16th edn, (AOAC International, Washington DC, USA)
Bayatkouhsar J, Tahmasebi AM, Naserian AA, Mokarram RR, Valizadeh R (2013) Effects of supplementation of lactic acid bacteria on growth performance, blood metabolites and fecal coliform and lactobacilli of young dairy calves. Anim Feed Sci Technol 186:1–11. https://doi.org/10.1016/j.anifeedsci.2013.04.015
Bi Y, Yang C, Diao Q, Tu Y (2017) Effects of dietary supplementation with two alternatives to antibiotics on intestinal microbiota of preweaned calves challenged with Escherichia coli K99. Sci Rep 7:1–12. https://doi.org/10.1038/s41598-017-05376-z
Celi P, Cowieson AJ, Fru-Nji F, Steinert RE, Kluenter AM, Verlhac V (2017) Gastrointestinal functionality in animal nutrition and health: new opportunities for sustainable animal production. Anim Feed Sci Technol 234:88–100. https://doi.org/10.1016/j.anifeedsci.2017.09.012
Collado MC, Isolauri E, Salminen S, Sanz Y (2009) The impact of probiotic on gut health. Curr Drug Metab 10:68–78. https://doi.org/10.2174/138920009787048437
Collado MC, Bäuerl C, Pérez-Martínez G (2012) Defining microbiota for developing new probiotics. Microb Ecol Health Dis 23(1):18579. https://doi.org/10.3402/mehd.v23i0.18579
Ellinger DK, Muller LD, Glantz PJ (1980) Influence of feeding fermented colostrum and Lactobacillus acidophilus on fecal flora of dairy calves. J Dairy Sci 63:478–482. https://doi.org/10.3168/jds.S0022-0302(80)82957-2
Fernández S, Fraga M, Silveyra E, Trombert AN, Rabaza A, Pla M, Zunino P (2018) Probiotic properties of native Lactobacillus spp. strains for dairy calves. Benef Microbes 9:613–624. https://doi.org/10.3920/BM2017.0131
Fernández S, Fraga M, Castells M, Colina R, Zunino P (2020) Effect of the administration of Lactobacillus spp. strains on neonatal diarrhoea, immune parameters and pathogen abundance in pre-weaned calves. Benef Microbes 11(5):477–488. https://doi.org/10.3920/BM2019.0167
Frizzo LS, Soto LP, Zbrun MV, Bertozzi E, Sequeira G, Armesto RR, Rosmini MR (2010) Lactic acid bacteria to improve growth performance in young calves fed milk replacer and spray-dried whey powder. Anim Feed Sci Technol 157(3-4):159–167. https://doi.org/10.1016/j.anifeedsci.2010.03.005
Fujisawa T, Sadatoshi A, Ohashi Y, Orihashi T, Sakai K, Sera K, Kanbe M (2010) Influences of Prebio SupportTM (mixture of fermented products of Lactobacillus gasseri OLL2716 and Propionibacterium freudenreichii ET-3) on the composition and metabolic activity of fecal microbiota in calves. Biosci Microflora 29:41–45. https://doi.org/10.12938/bifidus.29.41
Grasso F, Napolitano F, De Rosa G, Quarantelli T, Serpe L, Bordi A (1999) Effect of pen size on behavioral, endocrine, and immune responses of water buffalo (Bubalus bubalis) calves. J Anim Sci 77:2039–2046. https://doi.org/10.2527/1999.7782039x
Guo XH, Jong-Man K, Nam HM, Park SY, Jae-Myung K (2010) Screening lactic acid bacteria from swine origins for multistrain probiotics based on in vitro functional properties. Anaerobe 16:321–326. https://doi.org/10.1016/j.anaerobe.2010.03.006
Hemarajata P, Versalovic J (2013) Effects of probiotics on gut microbiota: mechanisms of intestinal immunomodulation and neuromodulation. Therap Adv Gastroenterol 6:39–51. https://doi.org/10.1177/1756283X12459294
Jiang X, Xu HJ, Cui ZQ, Zhang YG (2020) Effects of supplementation with Lactobacillus plantarum 299v on the performance, blood metabolites, rumen fermentation and bacterial communities of preweaning calves. Livest Sci 239:104–120. https://doi.org/10.1016/j.livsci.2020.104120
Kailasapathy K, Chin J (2000) Survival and therapeutic potential of probiotic organisms with reference to Lactobacillus acidophilus and Bifidobacterium spp. Immunol Cell Biol 78:80–88. https://doi.org/10.1046/j.1440-1711.2000.00886.x
Kim MK, Lee HG, Park JA, Kang SK, Choi YJ (2011) Effect of feeding direct-fed microbial as an alternative to antibiotics for the prophylaxis of calf diarrhea in Holstein calves. Asian-Australas J Anim Sci 24:643–649. https://doi.org/10.5713/ajas.2011.10322
Kore KB, Pattanaik AK, Das A, Sharma K (2009) Evaluation of alternative cereal sources in dog diets: effect on nutrient utilisation and hindgut fermentation characteristics. J Sci Food Agric 89:2174–2180. https://doi.org/10.1002/jsfa.3698
Kralik P, Ricchi M (2017) A basic guide to real time PCR in microbial diagnostics: definitions, parameters, and everything. Front Microbiol 8:108. https://doi.org/10.3389/fmicb.2017.00108
Kumar S, Pattanaik AK, Sharma S, Jadhav SE, Dutta N, Kumar A (2017) Probiotic potential of a Lactobacillus bacterium of canine faecal-origin and its impact on select gut health indices and immune response of dogs. Probiotics Antimicrob Proteins 9:262–277. https://doi.org/10.1007/s12602-017-9256-z
Kumar M, Kala A, Chaudhary LC, Agarwal N, Kochewad SA (2021a) Microencapsulated and lyophilized Lactobacillus acidophilus improved gut health and immune status of preruminant calves. Probiotics Antimicro Prot 1-12. https://doi.org/10.1007/s12602-021-09821-4
Kumar S, Pattanaik AK, Jadhav SE (2021b) Potent health-promoting effects of a synbiotic formulation prepared from Lactobacillus acidophilus NCDC15 fermented milk and Cichorium intybus root powder in Labrador dogs. Curr Res Biotechnol 3:109–119. https://doi.org/10.1016/j.crbiot.2021.06.001
Larson LL, Owen FG, Albright JL, Appleman RD, Lamb RC, Muller LD (1977) Guidelines toward more uniformity in measuring and reporting calf experimental data. J Dairy Sci 60:989–991. https://doi.org/10.3168/jds.S0022-0302(77)83975-1
Lesmeister KE, Heinrichs AJ, Gabler MT (2004) Effects of supplemental yeast (Saccharomyces cerevisiae) culture on rumen development, growth characteristics, and blood parameters in neonatal dairy calves. J Dairy Sci 87:1832–1839. https://doi.org/10.3168/jds.S0022-0302(04)73340-8
Maldonado NC, Nader MEF (2016) Production of fermented milk with autochthonous lactobacilli for newborn calves and resistance to the dairy farm conditions. J Bioprocess Biotech 6:278 https://doi.org/10.4172/2155-9821.1000278
Malmuthuge N, Griebel PJ, Guan LL (2015) The gut microbiome and its potential role in the development and function of new-born calf gastrointestinal tract. Front Vet Sci 2:36. https://doi.org/10.3389/fvets.2015.00036
Martin CC, de Oliveira SMFN, dos Reis Costa JF, Baccili CC, Silva BT, Hurley DJ, Gomes V (2021) Influence of feeding fresh colostrum from the dam or frozen colostrum from a pool on indicator gut microbes and the inflammatory response in neonatal calves. Res Vet Sci 135:355–365. https://doi.org/10.1016/j.rvsc.2020.10.017
Markowiak-Kopeć P, Śliżewska K (2020) The effect of probiotics on the production of short-chain fatty acids by human intestinal microbiome. Nutrients 12(4):1107. https://doi.org/10.3390/nu12041107
Masucci F, De Rosa G, Grasso F, Napolitano F, Esposito G, Di Francia A (2011) Performance and immune response of buffalo calves supplemented with probiotic. Livest Sci 137:24–30. https://doi.org/10.1016/j.livsci.2010.09.019
Meale SJ, Chaucheyras-Durand F, Berends H, Steele MA (2017) From pre-to postweaning: Transformation of the young calf's gastrointestinal tract. J Dairy Sci 100(7):5984–5995. https://doi.org/10.3168/jds.2016-12474
Meydani SN, Ha WK (2000) Immunologic effects of yogurt. Am J Clin Nutr 71:861–872. https://doi.org/10.1093/ajcn/71.4.861
Mohammed SAEM, Marouf SAEM, Erfana AM, El JKAEH, Hessain AM, Dawoud TM, Kabli SA, Moussa IM (2019) Risk factors associated with E. coli causing neonatal calf diarrhea. Saudi J Biol Sci 26(5):1084–1088. https://doi.org/10.1016/j.sjbs.2018.07.008
Ohya T, Akiba M, Ito H (2001) Use of a trial probiotic product in calves experimentally infected with Escherichia coli O157. Japan Agric Res 35:189–194. https://doi.org/10.6090/jarq.35.189
Ouwehand AC, Salminen S, Isolauri E (2002) Probiotics: an overview of beneficial effects, in Lactic Acid Bacteria: Genetics. Metabolism and Applications. Antonie Van Leeuwenhoek:279–289. https://doi.org/10.1007/978-94-017-2029-8_18
Qadis AQ, Goya S, Ikuta K, Yatsu M, Kimura A, Nakanishi S, Sato S (2014) Effects of a bacteria-based probiotic on ruminal pH, volatile fatty acids, and bacterial flora of Holstein calves. J Vet Med Sci 14:01–28. https://doi.org/10.1292/jvms.14-0028
Renaud DL, Kelton DF, Weese JS, Noble C, Duffield TF (2019) Evaluation of a multispecies probiotic as a supportive treatment for diarrhea in dairy calves: a randomized clinical trial. J Dairy Sci 102:4498–4505. https://doi.org/10.3168/jds.2018-15793
Reuben RC, Roy PC, Sarkar SL, Alam RU, Jahid IK (2019) Isolation, characterization, and assessment of lactic acid bacteria toward their selection as poultry probiotics. BMC Microbiol 19:253. https://doi.org/10.1186/s12866-019-1626-0
Riddle JB, Gallegos AJ, Harmon DL, McLeod KR (2010) Addition of a Bacillus based probiotic to the diet of preruminant calves: Influence on growth, health, and blood parameters. Int J Appl Res Vet Med 8:78–85
Ripamonti B, Agazzi A, Bersani C, De Dea P, Pecorini C, Pirani S, Rebucci R, Savoini G, Stella S, Stenico A (2011) Screening of species-specific lactic acid bacteria for veal calves multi-strain probiotic adjuncts. Anaerobe 17:97–105. https://doi.org/10.1016/j.anaerobe.2011.05.001
Sakata T, Kojima T, Fujieda M, Takahashi M, Michibata T (2003) Influences of probiotic bacteria on organic acid production by pig caecal bacteria in vitro. Proc Nutr Soc 62:73–80. https://doi.org/10.1079/PNS2002211
Sanders ME, Benson A, Lebeer S, Merenstein DJ, Klaenhammer TR (2018) Shared mechanisms among probiotic taxa: implications for general probiotic claims. Curr Opin Biotech 49:207–216. https://doi.org/10.1016/j.copbio.2017.09.007
Sharma AN, Kumar S, Tyagi AK (2018) Effects of mannan-oligosaccharides and Lactobacillus acidophilus supplementation on growth performance, nutrient utilization and faecal characteristics in Murrah buffalo calves. J Anim Physiol Anim Nutr 102:679–689. https://doi.org/10.1111/jpn.12878
Singh M, Kumar S, Banakar PS, Vinay VV, Das A, Tyagi N, Tyagi AK (2021a) Synbiotic formulation of Cichorium intybus root powder with Lactobacillus acidophilus NCDC15 and Lactobacillus reuteri BFE7 improves growth performance in Murrah buffalo calves via altering selective gut health indices. Trop Anim Health Pro 53(2):1–9. https://doi.org/10.1007/s11250-021-02733-z
Singh A, Kumar S, Vinay VV, Tyagi B, Choudhury PK, Rashmi HM, Banakar PS, Tyagi N, Tyagi AK (2021b) Autochthonous Lactobacillus spp. isolated from Murrah buffalo calves show potential application as probiotic. Curr Res Biotechnol 3:109–119. https://doi.org/10.1016/j.crbiot.2021.04.002
Soto LP, Zbrun MV, Frizzo LS, Signorini ML, Sequeira GJ, Rosmini MR (2014) Effects of bacterial inoculants in milk on the performance of intensively reared calves. Anim Feed Sci Technol 189:117–122. https://doi.org/10.1016/j.anifeedsci.2013.12.004
Sreedhar S, Ranganadham M, Mohan EM (2010) Calf mortality in indigenous buffaloes. Indian Vet J 87:197–198
Stefańska B, Sroka J, Katzer F, Goliński P, Nowak W (2020) The effect of probiotics, phytobiotics and their combination as feed additives in the diet of dairy calves on performance, rumen fermentation and blood metabolites during the preweaning period. Anim Feed Sci Technol 114738. https://doi.org/10.1016/j.anifeedsci.2020.114738
Timmerman HM, Koning CJM, Mulder L, Rombouts FM, Beynen AC (2004) Monostrain, multistrain and multispecies probiotics—a comparison of functionality and efficacy. Int J Food Microbiol 96:219–233. https://doi.org/10.1016/j.ijfoodmicro.2004.05.012
Vlasova AN, Kandasamy S, Chattha KS, Rajashekara G, Saif LJ (2016) Comparison of probiotic lactobacilli and bifidobacteria effects, immune responses and rotavirus vaccines and infection in different host species. Vet Immunol Immunopathol 172:72–84. https://doi.org/10.1016/j.vetimm.2016.01.003
Wegmann TG, Smithies O (1966) A simple hemagglutination system requiring small amounts of red cells and antibodies. Transfusion 6:67–73. https://doi.org/10.1111/j.1537-2995.1966.tb04696.x
Xanthopoulos V, Litopoulou-Tzanetaki E, Tzanetakis N (2000) Characterization of Lactobacillus isolates from infant faeces as dietary adjuncts. Food Microbiol 17:205–215. https://doi.org/10.1006/fmic.1999.0300
Zhang R, Zhou M, Tu Y, Zhang NF, Deng KD, Ma T, Diao QY (2016) Effect of oral administration of probiotics on growth performance, apparent nutrient digestibility and stress-related indicators in Holstein calves. J Anim Physiol Anim Nutr 100:33–38. https://doi.org/10.1111/jpn.12338
Acknowledgments
The authors are thankful to the Director, National Dairy Research Institute, Karnal, India, for the facilities provided. This study was supported by ICAR-NCVTCC, Hisar, India (F.No: NCVTC/Budget/2019-20/860).
Author information
Authors and Affiliations
Contributions
VV: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Visualization, Original draft writing SK: Conceptualization, Funding acquisition, Project administration, Writing – review and editing, Formal analysis. PS: Writing – review and editing, Software. AD: Writing – review and editing, Software. NT: Funding acquisition, Resources, Supervision. HM: Conceptualization, Software. AK: Funding acquisition, Resources, Supervision. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics Approval
All procedures performed in studies involving animals were in accordance with the ethical standards of the Institutional Animal Ethics Committee (IAEC), NDRI, Karnal, Haryana, India under Approval No.42-IAEC-18-34 dated 30/06/18. The authors confirm that animal care and use were according to the relevant standard operating protocol laid down by the above mentioned ethics committee to protect animals for scientific purposes.
Competing interests
The authors declare that they have no competing interest.
Consent for publication
All authors give their consent for publication of this manuscript.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Varada, V.V., Tyagi, A.K., Banakar, P.S. et al. Autochthonous Limosilactobacillus reuteri BFE7 and Ligilactobacillus salivarius BF17 probiotics consortium supplementation improves performance, immunity, and selected gut health indices in Murrah buffalo calves. Vet Res Commun 46, 757–767 (2022). https://doi.org/10.1007/s11259-022-09896-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11259-022-09896-6