ORIGINAL PAPER
 
KEYWORDS
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ABSTRACT
The aim of the study was to assess the impact of potential probiotic strains of lactic acid bacteria (LAB), Apilactobacillus kunkeei EIR/BG-1 isolated from the gut of honeybees, and Enterococcus hirae EIR/CM-2 isolated from cow’s milk, on rumen fermentation parameters and microbial population in a high-concentrate diet using a rumen simulation technique (Rusitec). The experiment consisted of 7 days of adaptation and 7 days of data collection. The dietary treatments were as follows: no additives (control), addition of 1 ml/fermenter (108 CFU) of Al. kunkeei EIR/BG-1, and addition of 1 ml/fermenter (108 CFU) of E. hirae EIR/CM-2. Alongside rumen fermentation characteristics, rumen microbial composition was investigated using real-time PCR. Supplementation with LAB strains did not affect ruminal pH, production of methane, and total and individual short chain fatty acids, ammonia-N concentration, dry matter digestibility and total protozoa. However, the abundance of Ruminococcus flavefaciens increased in the Al. kunkeei EIR/BG-1 treatment (P < 0.05). Moreover, the size of R. flavefaciens population in E. hirae EIR/CM-2 was comparable to that in the Al. kunkeei EIR/BG-1 treatment. Selenomonas ruminantium was more abundant in the Al. kunkeei EIR/BG-1 treatment compared to the E. hirae EIR/CM-2 treatment (P < 0.05). The abundance of Streptococcus bovis and Megasphaera elsdenii decreased with both Al. kunkeei EIR/BG-1 and E. hirae EIR/CM-2 supplementations (P < 0.05). In conclusion, Al. kunkeei EIR/BG-1 and E. hirae EIR/CM-2 exhibited beneficial effects on some members of the rumen microbial population, although these effects did not manifest in significant alterations in ruminal fermentation. Further research is required to clarify the probiotic potentials of these LAB strains as feed additives for ruminant rations.
CONFLICT OF INTEREST
The Authors declare that there is no conflict of interest.
REFERENCES (64)
1.
Abdl-Rahman M.A., 2010. In vitro manipulation of rumen fermentation efficiency by fumaric acid – bentonite coupled addition as an alternative to antibiotics. J. Agric. Sci. 2, 174–180, https://doi.org/10.5539/jas.v2....
 
2.
Ahmad W., Khaliq S., Akhtar N., El Arab J., Akhtar K., Prakash S., Anwar M.A., Munawar N., 2022. Whole genome sequence analysis of a novel Apilactobacillus species from giant honeybee (Apis dorsata) gut reveals occurrence of genetic elements coding prebiotic and probiotic traits. Microorganisms 10, 904, https://doi.org/10.3390/microo....
 
3.
Amin A.B., Mao S., 2021. Influence of yeast on rumen fermentation, growth performance and quality of products in ruminants: A review. Anim. Nutr. 7, 31–41, https://doi.org/10.1016/j.anin....
 
4.
AOAC International, 2000. Official Methods of Analysis of AOAC International. 17th Edition. Gaithersburg, MD (USA).
 
5.
Arredondo D., Castelli L., Porrini M.P., Garrido P.M., Eguaras M.J., Zunino P., Antunez K., 2018. Lactobacillus kunkeei strains decreased the infection by honey bee pathogens Paenibacillus larvae and Nosema ceranae. Benef. Microbes 9, 279–290, https://doi.org/10.3920/BM2017....
 
6.
Attwood G.T., Klieve A.V., Ouwerkerk D., Patel B.K.C., 1998. Ammoniahyperproducing bacteria from New Zealand ruminants. Appl. Environ. Microbiol. 64, 1796–1804, https://doi.org/10.1128/AEM.64....
 
7.
Azzaz H.H., Kholif A.E., Murad H.A., Vargas-Bello-Pérez E., 2022. A newly developed strain of Enterococcus faecium isolated from fresh dairy products to be used as a probiotic in lactating Holstein cows. Front. Vet. Sci. 9, 989606, https://doi.org/10.3389/fvets.....
 
8.
Badel S., Bernardi T., Michaud, P., 2011. New perspectives for Lactobacilli exopolysaccharides. Biotechnol. Adv. 29, 54–66, https://doi.org/10.1016/j.biot....
 
9.
Becquet P., 2003. EU assessment of enterococci as feed additives. Int. J. Food Microbiol. 88, 247–254, https://doi.org/10.1016/S0168-....
 
10.
Beecher C., Daly M., Berry D.P., Klostermann K., Flynn J., Meaney W., Hill C., McCarthy T.V., Ross R.P., Giblin L., 2009. Administration of a live culture of Lactococcus lactis DPC3147 into the bovine mammary gland stimulates the local host immune response, particularly IL-1 and IL-8 gene expression. J. Dairy Res. 76, 340–348, https://doi.org/10.1017/S00220....
 
11.
Bintsis T., 2018. Lactic acid bacteria: their applications in foods. J. Bacteriol. Mycol. Open Acess 6, 89–94, https://doi.org/10.15406/jbmoa....
 
12.
Chaney A.L., Marbach E.P., 1962. Modified reagents for determination of urea and ammonia. Clin. Chem. 8, 130–132, https://doi.org/10.1093/clinch....
 
13.
Chen L., Ren A., Zhou C., Tan Z., 2017. Effects of Lactobacillus acidophilus supplementation for improving in vitro rumen fermentation characteristics of cereal straws. Ital. J. Anim. Sci. 16, 52–60, https://doi.org/10.1080/182805....
 
14.
Counotte G.H.M., Prins R.A., 1981. Regulation of lactate metabolism in the rumen. Vet. Res. Commun. 5, 101–115, https://doi.org/10.1007/bf0221....
 
15.
Czerkawski J.W., Breckenridge G., 1977. Design and development of a long term rumen simulation technique (Rusitec). Brit. J. Nutr. 38, 371–384, https://doi.org/10.1079/BJN197....
 
16.
Demirtas A., Musa S.A.A., Salgirli-Demirbas Y., Ozturk H., Pekcan M., Toprak N.N., Safak E., Unler M., Saral B., Emre M.B., 2021. The effects of Pinus brutia bark extract on pure and mixed continuous cultures of rumen bacteria and archaea, and fermentation characteristics in vitro. Vet. Arhiv 91, 523–535, https://doi.org/10.24099/vet.a....
 
17.
Demirtas A., Ozturk H., Sudagidan M., Keyvan E., Yavuz O., Gulay O.Y., Musa, S.A.A., 2019. Effects of commercial aldehydes from green leaf volatiles (green odour) on rumen microbial population and fermentation profile in an artificial rumen (Rusitec). Anaerobe 55, 83–92, https://doi.org/10.1016/j.anae....
 
18.
Denman S.E., McSweeney C.S., 2005. Quantitative (real-time) PCR. In: H.S. Makkar, C. McSweeney (Editors). Methods in Gut Microbial Ecology for Ruminants. Springer. Dordrecht (Netherlands), pp. 105–115, https://doi.org/10.1007/1-4020....
 
19.
Denman S.E., McSweeney C.S., 2006. Development of a realtime PCR assay for monitoring anaerobic fungal and cellulolytic bacterial populations within the rumen. FEMS Microbiol. Ecol. 58, 572–582, https://doi.org/10.1111/j.1574....
 
20.
Denman S.E., Tomkins N.W., McSweeney C.S., 2007. Quantitation and diversity analysis of ruminal methanogenic populations in response to the antimethanogenic compound bromochloromethane. FEMS Microbiol. Ecol. 62, 313–322, https://doi.org/10.1111/j.1574....
 
21.
Doyle N., Mbandlwa P., Kelly W.J., Attwood G., Li Y., Ross R.P., Stanton C., Leahy S., 2019. Use of lactic acid bacteria to reduce methane production in ruminants, a critical review. Front. Microbiol. 10, 2207, https://doi.org/10.3389/fmicb.....
 
22.
El-Nor S.A., AbuGhazaleh A.A., Potu R.B., Hastings D., Khattab M.S.A., 2010. Effects of differing levels of glycerol on rumen fermentation and bacteria. Anim. Feed Sci. Tech. 162, 99–105, https://doi.org/10.1016/j.anif....
 
23.
Espeche M.C., Pellegrino M., Frola I., Larriestra A., Bogni C., Nader-Macías M.F., 2012. Lactic acid bacteria from raw milk as potentially beneficial strains to prevent bovine mastitis. Anaerobe 18, 103–109, https://doi.org/10.1016/j.anae....
 
24.
Fuller R., 1989. Probiotics in man and animals. J. Appl. Bacteriol. 66, 365–378, https://doi.org/10.1111/j.1365....
 
25.
Gill H.S., Shu Q., Leng R.A., 2000. Immunization with Streptococcus bovis protects against lactic acidosis in sheep. Vaccine 18, 2541–2548, https://doi.org/10.1016/S0264-....
 
26.
Gómez J.A., Tejido M.L., Carro M.D., 2005. Influence of disodium malate on microbial growth and fermentation in rumen-simulation technique fermenters receiving medium-and high-concentrate diets. Brit. J. Nutr. 93, 479–484, https://doi.org/10.1079/BJN200....
 
27.
Guo G., Shen C., Liu Q., Zhang S., Shao T., Wang C., Wang Y., Xu Q., Huo W., 2020. The effect of lactic acid bacteria inoculums on in vitro rumen fermentation, methane production, ruminal cellulolytic bacteria populations and cellulase activities of corn stover silage. J. Integr. Agr. 19, 838–847, https://doi.org/10.1016/S2095-....
 
28.
Indira M., Venkateswarulu T.C., Abraham Peele K., Nazneen Bobby M., Krupanidhi S., 2019. Bioactive molecules of probiotic bacteria and their mechanism of action: a review. 3 Biotech 9, 306, https://doi.org/10.1007/s13205....
 
29.
ISO, 2000. Animal feeding stuffs – Determination of starch content – Polarimetric method. Standard ISO 6493 (E): 2000. International Organization for Standardization. Geneva (Switzerland).
 
30.
Jiao Y., Darzi Y., Tawaratsumida K. et al., 2013. Induction of bone loss by pathobiont-mediated Nod1 signaling in the oral cavity. Cell Host Microbe 13, 595–601, https://doi.org/10.1016/j.chom....
 
31.
Kim S.H., Mamuad L.L., Kim D.W., Kim S.K., Lee S.S., 2016. Fumarate reductase-producing enterococci reduce methane production in rumen fermentation in vitro. J. Microbiol. Biotechnol. 26, 558–566, http://dx.doi.org/10.4014/jmb.....
 
32.
Kiran F., Sevin S., Ceylan A., 2023. Biocontrol potential of Apilactobacillus kunkeei EIR/BG-1 against infectious diseases in honey bees (Apis mellifera L.). Vet. Res. Commun. 47, 753–765, https://doi.org/10.1007/s11259....
 
33.
Klieve A.V., Hennessy D., Ouwerkerk D., Forster R.J., Mackie R.I., Attwood G.T., 2003. Establishing populations of Megasphaera elsdenii YE 34 and Butyrivibrio fibrisolvens YE 44 in the rumen of cattle fed high grain diets. J. Appl. Microbiol. 95, 621–630, https://doi.org/10.1046/j.1365....
 
34.
Krehbiel C.R., Rust S.R., Zhang G., Gilliland S.E., 2003. Bacterial direct-fed microbials in ruminant diets: performance response and mode of action. J. Anim. Sci. 81, 120–132, https://doi.org/10.2527/2003.8....
 
35.
Kulkarni N.A., Chethan H.S., Srivastava R., Gabbur A.B., 2022. Role of probiotics in ruminant nutrition as natural modulators of health and productivity of animals in tropical countries: an overview. Trop. Anim. Health Pro. 54, 110, https://doi.org/10.1007/s11250....
 
36.
Li X., Durmic Z., Liu S., McSweeney C.S., Vercoe P.E., 2014. Eremophila glabra reduces methane production and methanogen populations when fermented in a Rusitec. Anaerobe 29, 100–107, https://doi.org/10.1016/j.anae....
 
37.
Mamuad L.L., Kim S.H., Biswas A.A., Yu Z., Cho K.K., Kim S.B., Lee K., Lee S.S., 2019. Rumen fermentation and microbial community composition influenced by live Enterococcus faecium supplementation. AMB Express 9, 1–12, https://doi.org/10.1186/s13568....
 
38.
Melo C. de C.S., da Silva Freire A., Galdeano M.A., da Costa C.F., de Oliveira Gonçalves A.P.D., Dias F.S., Menezes D.R., 2021. Probiotic potential of Enterococcus hirae in goat milk and its survival in canine gastrointestinal conditions simulated in vitro. Res. Vet. Sci. 138, 188–195, https://doi.org/10.1016/j.rvsc....
 
39.
Meng X., Gangoiti J., Wang X., Grijpstra P., van Leeuwen S.S., Pijning T., Dijkhuizen L., 2018. Biochemical characterization of a GH70 protein from Lactobacillus kunkeei DSM 12361 with two catalytic domains involving branching sucrase activity. Appl. Microbiol. Biot. 102, 7935–7950, https://doi.org/10.1007/s00253....
 
40.
Mombach M.A., da Silva Cabral L., Lima L.R., Ferreira D.C., e Pedreira B.C., Pereira D.H., 2021. Association of ionophores, yeast, and bacterial probiotics alters the abundance of ruminal microbial species of pasture intensively finished beef cattle. Trop. Anim. Health Pro. 53, 172, https://doi.org/10.1007/s11250....
 
41.
Morovský M., Pristaš P., Czikková S., Javorský P., 1998. A bacteriocinmediated antagonism by Enterococcus faecium BC25 against ruminal Streptococcus bovis. Microbiol. Res. 153, 277–281, https://doi.org/10.1016/S0944-....
 
42.
Mosoni P., Chaucheyras-Durand F., Béra-Maillet C., Forano E., 2007. Quantification by real-time PCR of cellulolytic bacteria in the rumen of sheep after supplementation of a forage diet with readily fermentable carbohydrates: effect of a yeast additive. J. Appl. Microbiol. 103, 2676–2685, https://doi.org/10.1111/j.1365....
 
43.
NRC (National Research Council), 1985. Nutrient Requirements of Sheep. 6th Edition. National Academies Press. Washington, DC (USA).
 
44.
Ouwerkerk D., Klieve A.V., Forster R.J., 2002. Enumeration of Megasphaera elsdenii in rumen contents by real-time Taq nuclease assay. J. Appl. Microbiol. 92, 753–758, https://doi.org/10.1046/j.1365....
 
45.
Peterson R.E., Klopfenstein T.J., Erickson G.E., Folmer J., Hinkley S., Moxley R.A., Smith D.R., 2007. Effect of Lactobacillus acidophilus strain NP51 on Escherichia coli O157: H7 fecal shedding and finishing performance in beef feedlot cattle. J. Food Protect. 70, 287–291, https://doi.org/10.4315/0362-0....
 
46.
Raeth-Knight M.L., Linn J.G., Jung H.G., 2007. Effect of direct-fed microbials on performance, diet digestibility, and rumen characteristics of Holstein dairy cows. J. Dairy Sci. 90, 1802–1809, https://doi.org/10.3168/jds.20....
 
47.
Sevin S., Karaca B., Haliscelik O., Kibar H., OmerOglou E., Kiran F., 2021. Postbiotics secreted by Lactobacillus sakei EIR/CM-1 isolated from cow milk microbiota, display antibacterial and antibiofilm activity against ruminant mastitis-causing pathogens. Ital. J. Anim. Sci. 20, 1302–1316, https://doi.org/10.1080/182805....
 
48.
Sheikh G.G., Ganai A.M., Ahmad Sheikh A., Mir D.M., 2022. Rumen microflora, fermentation pattern and microbial enzyme activity in sheep fed paddy straw based complete feed fortified with probiotics. Biol. Rhythm Res. 53, 547–558, https://doi.org/10.1080/092910....
 
49.
Simsek D., Kiymaci M.E., Tok K.C., Gumustas M., Altanlar N., 2022. Investigation of the probiotic and metabolic potential of Fructobacillus tropaeoli and Apilactobacillus kunkeei from apiaries. Arch. Microbiol. 204, 432, https://doi.org/10.1007/s00203....
 
50.
Soriano A.P., Mamuad L.L., Kim S.H., Choi Y.J., Jeong C.D., Bae G.S., Chang M.B., Lee S.S., 2014. Effect of Lactobacillus mucosae on in vitro rumen fermentation characteristics of dried brewers grain, methane production and bacterial diversity. Asian Australas. J. Anim. 27, 1562–1570, https://doi.org/10.5713/ajas.2....
 
51.
Stefańska B., Sroka J., Katzer F., Goliński P., Nowak W., 2021. 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. Tech. 272, 114738, https://doi.org/10.1016/j.anif....
 
52.
Tajima K., Aminov R.I., Nagamine T., Matsui H., Nakamura M., Benno Y., 2001. Diet dependent shifts in the bacterial population of the rumen revealed with Real-Time PCR. Appl. Environ. Microbiol. 67, 2766–2774, https://doi.org/10.1128/AEM.67....
 
53.
TSE (Turkish Standards Institute), 1991. Animal feed – determination of metabolisable energy (chemical method). Publication No. 9610. Ankara (Turkey), pp. 1–3.
 
54.
Van Soest P.J., Robertson J.B., Lewis B.A., 1991. Methods for dietary fiber, neutral detergent fiber, and non-starch polysaccharides in relation to animal nutrition. J. Dairy Sci. 74, 3583–3597, https://doi.org/10.3168/jds.S0....
 
55.
Vieco-Saiz N., Belguesmia Y., Raspoet R., Auclair E., Gancel F., Kempf I., Drider D., 2019. Benefits and inputs from lactic acid bacteria and their bacteriocins as alternatives to antibiotic growth promoters during food-animal production. Front. Microbiol. 10, 57, https://doi.org/10.3389/fmicb.....
 
56.
Wang Y., Alexander T.W., McAllister T.A., 2009. In vitro effects of phlorotannins from Ascophyllum nodosum (brown seaweed) on rumen bacterial populations and fermentation. J. Sci. Food Agric. 89, 2252–2260, https://doi.org/10.1002/jsfa.3....
 
57.
Watanabe Y., Suzuki R., Koike S., Nagashima K., Mochizuki M., Forster R.J., Kobayashi Y., 2010. In vitro evaluation of cashew nut shell liquid as a methane-inhibiting and propionate-enhancing agent for ruminants. J. Dairy Sci. 93, 5258–5267, https://doi.org/10.3168/jds.20....
 
58.
Weinberg Z.G., Shatz O., Chen Y., Yosef E., Nikbahat M., Ben-Ghedalia D., Miron J., 2007. Effect of lactic acid bacteria inoculants on in vitro digestibility of wheat and corn silages. J. Dairy Sci. 90, 4754–4762, https://doi.org/10.3168/jds.20....
 
59.
Wolin M.J., 1960. A theoretical rumen fermentation balance. J. Dairy Sci. 43, 1452–1459, https://doi.org/10.3168/jds.S0....
 
60.
Xu H., Huang W., Hou Q., Kwok L.Y., Sun Z., Ma H., Zhao F., Lee Y.K., Zhang H., 2017. The effects of probiotics administration on the milk production, milk components and fecal bacteria microbiota of dairy cows. Sci. Bull. 62, 767–774, https://doi.org/10.1016/j.scib....
 
61.
Yang H.E., Zotti C.A., McKinnon J.J., McAllister T.A., 2018. Lactobacilli are prominent members of the microbiota involved in the ruminal digestion of barley and corn. Front. Microbiol. 9, 718, https://doi.org/10.3389/fmicb.....
 
62.
Zhang R., Dong X., Zhou M., Tu Y., Zhang N., Deng K., Diao Q., 2017. Oral administration of Lactobacillus plantarum and Bacillus subtilis on rumen fermentation and the bacterial community in calves. Anim. Sci. J. 88, 755–762, https://doi.org/10.1111/asj.12....
 
63.
Zhang L., Jiang X., Liu X., Zhao X., Liu S., Li Y., Zhang Y., 2019. Growth, health, rumen fermentation, and bacterial community of Holstein calves fed Lactobacillus rhamnosus GG during the preweaning stage. J. Anim. Sci. 97, 2598–2608, https://doi.org/10.1093/jas/sk....
 
64.
Zhu W., Wei Z., Xu N., Yang F., Yoon I., Chung Y., Liu J., Wang J., 2017. Effects of Saccharomyces cerevisiae fermentation products on performance and rumen fermentation and microbiota in dairy cows fed a diet containing low quality forage. J. Anim. Sci. Biotechnol. 8, 36, https://doi.org/10.1186/s40104....
 
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