The Assays of Bacteria-Yeast Consortia as Probiotics Candidates and Their Influences on Nutrients Utilization of Quails Diet

A. Sofyan, R. S. H. Martin, E. B. Laconi, A. Jayanegara, H. Julendra, E. Damayanti, A. E. Suryani


This study aimed to assay L. plantarum (P1), S. cerevisiae (P2), and its combination (P3) as probiotics candidates and their effects on nutrient digestibility in Japanese quails (Cortunix cortunix japonica) diets. In vitro assays were employed to evaluate the antibacterial activities against pathogenic bacteria (Escherichia coli, Staphylococcus aureus, Pseudomonas aeruginosa, and Salmonella pullorum), sensitivity to antibiotics (i.e., streptomycin, penicillin, and erythromycin), stress on bile salt and acidity condition. Evaluation of probiotics on in vivo nutrient utilization was carried out by administration of probiotics to laying quails in drinking water with various treatments (R0, control; R1, L. plantarum; R2, S. cerevisiae; R3, combination of R1+R2; R4, commercial feed additive). Results showed that the highest inhibitory activity was performed by P2 on S. aureus (17.28 mm). Treatments P2 and P3 were resistant to all the tested antibiotics, while P1 was resistant to streptomycin and penicillin. P1 was tolerant to bile salts whereas P2 was tolerant to gastric acidity conditions. For the in vivo experiment, quails fed R1, R2, and R4 had higher nitrogen retention as compared to R0 (p<0.05). However, all treatments revealed similar metabolizable energy values. The cluster analysis showed that quails consuming the combination of L. plantarum and S. cerevisiae were within the same cluster with the control but different clusters from the individual probiotics across all parameters, indicating a possible antagonistic effect between the two species.  In conclusion, the inclusion of L. plantarum or S. cerevisiae inhibits pathogenic bacteria without influencing nutrient utilization of quail diet.


Ajuwon, J.M. 2016. Toward a better understanding of mechanisms of probiotics and prebiotics action in poultry species. J. Appl. Poult. Res. 25:277-283.

Arena, M.P., V. Capozzi, P. Russo, D. Drider, G. Spano, & D. Fiocco. 2018. Immunobiosis and probiosis: antimicrobial activity of lactic acid bacteria with a focus on their antiviral and antifungal properties. Appl. Microbiol. Biotechnol. 102:9949-9958.

AOAC. 2005. Official Methods of Analysis of AOAC International. 18th ed. Assoc. Off. Anal. Chem., Arlington.

Barbosa-Cánovas, G.V., E. Ortega-Rivas, P. Juliano, & H. En. 2005. Drying: In Food Powders-Physical Properties, Processing and Functionality, First Edition; Kluwer Academic/Plenum Publishers, New York, pp. 271-304.

Bonev, B.J., J. Hooper, & J. Parisot. 2008. Principles of assessing bacterial susceptibility to antibiotics using the agar diffusion method. J. Antimicrob. Chemother. 61:1295-1301.

Branco, P., D. Francisco, M. Monteiro, M.G. Almeida, J. Caldeira, N. Arneborg, N. Arneborg & H. Albergaria. 2017. Antimicrobial properties and death-inducing mechanisms of saccharomycin, a biocide secreted by Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 101: 159-171.

Cohort. 2008. Costat-Coplot Version 6.311. Cohort software798 light house Ave. PMB320, Monterey, CA93940, and USA.

Cox, C.M., & R.A. Dalloul. 2015. Immunomodulatory role of probiotics in poultry and potential in ovo application. Benef. Microbes. 6: 45-52.

de Melo Pereira, G.V., B. de Oliveira Coelho, A.I.M. Júnior, V. Thomaz-Soccol, & C.R. Soccol. 2018. How to select a probiotic? A review and update of methods and criteria. Biotechnol. Adv. 36: 2060-2076.

Damayanti, E., H. Julendra, A. Sofyan & S.N. Hayati. 2014. Bile salt and acid tolerant of lactic acid bacteria isolated from proventriculus of broiler chicken. Med. Pet. 37:80-86.

Gotcheva, V., E. Hristozova, T. Hristozova, M. Guo, Z. Roshkova, & A. Angelov. 2002. Assessment of potential probiotic properties of lactic acid bacteria and yeast strains. Food Biotechnol. 16: 211-225.

Goutard FL, M. Bordier, C. Calba, E. Erlacher-Vindel, D. Góchez, K. de Balogh, C. Benigno, W. Kalpravidh, F. Roger, & S. Vong. 2017. Antimicrobial policy interventions in food animal production in South East Asia. Br. Med. J. 358:36-41.

Farrell, D.J., S.I. Atmamihardja, & R.A.E. Pym. 1982. Calorimetric measurements of the energy and nitrogen metabolism of Japanese quail. Br. Poult. Sci. 23: 375-382.

Hammami, R., B. Fernandez, C. Lacroix, & I. Fliss. 2013. Anti-infective properties of bacteriocins: an update. Cell. Mol. Life Sci. 70: 2947-2967.

Hatoum, R., S. Labrie, & I. Fliss. 2012. Antimicrobial and probiotic properties of yeasts: from fundamental to novel applications. Front. Microbiol. 3: 421.

Harimurti S., & W. Hadisaputro. 2015. Probiotics in Poultry. In: Liong MT. (eds) Beneficial Microorganisms in Agriculture, Aquaculture and Other Areas. Microbiology Monographs, Vol. 29. Springer International Publishing, Switzerland.

Huyghebaert, G., R. Ducatelle, & F. Van Immerseel. 2011. An update on alternatives to antimicrobial growth promoters for broilers. Vet. J. 187:182-188.

Istiqomah, L., M. Anwar, A.S. Anggraeni, & E. Damayanti. 2018. Cholesterol assimilation of Saccharomyces cerevisiae B-18 isolated from gastrointestinal tract of Javanese duck. J. Indon. Trop. Anim. Agric. 43: 149-158.

Julendra, H., A.E. Suryani, L. Istiqomah, E. Damayanti, M. Anwar, & N. Fitriani. 2017. Isolation of lactic acid bacteria with cholesterol-lowering activity from digestive tracts of Indonesian native chicken. Med. Pet. 40: 35-41.

Kim, H., E.J. Oh, S.T. Lane, W.H. Lee, J.H. Cate, & Y.S. Jin. 2018. Enhanced cellobiose fermentation by engineered Saccharomyces cerevisiae expressing a mutant cellodextrin facilitator and cellobiose phosphorylase. J. Biotechnol. 275: 53-59.

Kumar, B. L., & D.S. Gopal. 2015. Effective role of indigenous microorganisms for sustainable environment. Biotech. 5: 867-876.

Martin, R.S.H., E.B. Laconi, A. Jayanegara, A. Sofyan, & L. Istiqomah. 2018. Activity and viability of probiotic candidates consisting of lactic acid bacteria and yeast isolated from native poultry gastrointestinal tract. AIP Conference Proc. 2021: 070012.

Ministry of Agriculture - Republic of Indonesia [MARI]. 2017. Peraturan Menteri Pertanian Republik Indonesia Nomor 14/Permentan/PK.350/5/2017 tentang Klasifikasi Obat Hewan (Animal Medicine Classification Act). Retrieved from: [12 May 2017].

Narendranath, N.V., K.C. Thomas, & W.M. Ingledew. 2001. Effects of acetic acid and lactic acid on the growth of Saccharomyces cerevisiae in a minimal medium. J. Indust. Microbiol. Biotechnol. 26: 171-177.

Ooi, L.G. & M.T. Liong. 2010. Cholesterol-lowering effects of probiotics and prebiotics: a review of in vivo and in vitro findings. Int. J. Mol. Sci. 11:2499-2522.

Rajoka, M.S.R., H.F. Hayat, S. Sarwar, H.M. Mehwish, F. Ahmad, N. Hussain, S.Z.H. Shah, M. Khurshid, M. Siddiqu, & J. Shi. 2018. Isolation and evaluation of probiotic potential of lactic acid bacteria isolated from poultry intestine. Microbiology 87: 116-126.

R Core Team. 2015. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Retrieved on 31 October 2015 from

Rizk, Z., Y. El Rayess, C. Ghanem, F. Mathieu, P. Taillandier, & N. Nehme. 2018. Identification of multiple-derived peptides produced by Saccharomyces cerevisiae involved in malolactic fermentation inhibition. FEMS Yeast Res. 18: foy080.

Ronquillo, M.G., & J.C.A. Hernandez. 2017. Antibiotic and synthetic growth promoters in animal diets: review of impact and analytical methods. Food Control 72: 255-267.

Sibbald, I. R., & M.S. Wolynetz. 1985. Relationships between estimates of bioavailable energy made with adult cockerels and chicks: effects of feed intake and nitrogen retention. Poult. Sci. 64: 127-138.

Sharifi, S.D., A.Dibamehr, H. Lotfollahian & B. Baurhoo. 2012. Effects of flavomycin and probiotic supplementation to diets containing different sources of fat on growth performance, intestinal morphology, apparent metabolizable energy, and fat digestibility in broiler chickens. Poult. Sci. 91: 918-927.

Sieuwerts, S., P.A. Bron, & E.J. Smid. 2018. Mutually stimulating interactions between lactic acid bacteria and Saccharomyces cerevisiae in sourdough fermentation. LWT - Food Sci. Technol. 90: 201-206.

Sofyan, A., A.N. Aswari, T. Purwoko, & E. Damayanti. 2013. Screening of lactic acid bacteria from rumen liquor and king grass silage as well as their antibacterial activities. Med. Pet. 36: 216.

Stadie, J., A. Gulitz, M.A. Ehrmann, & R.F. Vogel. 2013. Metabolic activity and symbiotic interactions of lactic acid bacteria and yeasts isolated from water kefir. Food Microbiol. 35: 92-98.

Stanley, D., R.J. Hughes & R.J. Moore. 2014. Microbiota of the chicken gastrointestinal tract: influence on health, productivity and disease. Appl. Microbiol. Biotechnol. 98: 4301-4310.

Syal, P. & A. Vohra. 2013. Probiotic potential of yeasts isolated from traditional Indian fermented foods. Int. J. Microbiol. Res. 5:390-398.

Torshizi, M.A.K., S.H. Rahimi, N. Mojgani, S. Esmaeilkhanian, & J.L. Grimes. 2008. Screening of indigenous strains of lactic acid bacteria for development of a probiotic for poultry. Asian-Australas. J. Anim. Sci. 21: 1495-1500.

Wang, Y., & Q. Gu. 2010. Effect of probiotic on growth performance and digestive enzyme activity of Arbor Acres broilers. Res. Vet. Sci. 89: 163-167.

Zhang, Z., F. Murtagh, S. Van Poucke, S. Lin, & P. Lan. 2017. Hierarchical cluster analysis in clinical research with heterogeneous study population: highlighting its visualization with R. Ann. Transl. Med. 5: 1-11.


A. Sofyan (Primary Contact)
R. S. H. Martin
E. B. Laconi
A. Jayanegara
H. Julendra
E. Damayanti
A. E. Suryani
Author Biography

A. Sofyan, Research Unit for Natural Product Technology (BPTBA), Indonesian Institute of Science (LIPI)

Research Group of Bio-Feed Additive Technology, Research Unit for Natural Product Technology (BPTBA), Indonesian Institute of Science (LIPI)
Jl. Jogja-Wonosari Km. 31.5 Gading, Playen, Gunungkidul, D.I. Yogyakarta 55861, Indonesia

SofyanA., MartinR. S. H., LaconiE. B., JayanegaraA., JulendraH., DamayantiE., & SuryaniA. E. (2019). The Assays of Bacteria-Yeast Consortia as Probiotics Candidates and Their Influences on Nutrients Utilization of Quails Diet. Tropical Animal Science Journal, 42(3), 196-202.

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