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Evaluation of cellulolytic exogenous enzyme-containing microbial inoculants as feed additives for ruminant rations composed of low-quality roughage

Published online by Cambridge University Press:  11 August 2020

M. S. Zayed Open the ORCID record for M. S. Zayed [Opens in a new window] ,
M. Szumacher-Strabel ,
D. A. A. El-Fattah Open the ORCID record for D. A. A. El-Fattah [Opens in a new window] ,
M. A. Madkour ,
M. Gogulski ,
V. Strompfová ,
A. Cieślak Open the ORCID record for A. Cieślak [Opens in a new window]  and
N. E. El-Bordeny
M. S. Zayed
Affiliation:
Department of Agricultural Microbiology, Faculty of Agriculture, Ain Shams University, Cairo, Egypt
M. Szumacher-Strabel
Affiliation:
Department of Animal Nutrition, Poznań University of Life Sciences, Poznań, Poland
D. A. A. El-Fattah
Affiliation:
Central Laboratory for Agriculture Climate, Agricultural Research Center, Dokki, Giza, Egypt
M. A. Madkour
Affiliation:
Department of Animal Nutrition, Animal Production Research Institute, Dokki, Giza, Egypt
M. Gogulski
Affiliation:
University Center for Veterinary Medicine, Poznań University of Life Sciences, Poznań, Poland Department of Preclinical Sciences and Infectious Diseases, Poznań University of Life Sciences, Poznań, Poland Centre of Biosciences SAS, Institute of Animal Physiology, Kosice, Slovakia
V. Strompfová
Affiliation:
Centre of Biosciences SAS, Institute of Animal Physiology, Kosice, Slovakia
A. Cieślak*
Affiliation:
Department of Animal Nutrition, Poznań University of Life Sciences, Poznań, Poland
N. E. El-Bordeny
Affiliation:
Department of Animal Production, Faculty of Agriculture, Ain Shams University, Cairo, Egypt
*
Author for correspondence: A. Cieślak, E-mail: [email protected]
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Abstract

The supplementation of ruminant diets with exogenous cellulolytic enzymes can improve their digestibility and feeding value. The objective of this study was to determine the effect of supplementing roughage (rice straw) and concentrate with inoculants containing four fungal strains (Pleurotus ostreatus, Phanerochaete chrysosporium, Trichoderma reesei and Trichoderma viride) and four bacterial strains (Paenibacillus polymyxa, Bacillus megaterium, Bacillus circulans and Bacillus subtilis), given separately or as a mixture, as a source of exogenous cellulolytic enzymes, on basic rumen parameters in vitro, including digestibility and methane production. A batch culture trial was used to select the best supplements, and a long-term rumen simulation technique (RUSITEC) was used to evaluate the effects of P. chrysosporium, B. subtilis, and a 1 : 1 mixture of these two on dietary component digestibility and fermentation parameters. In the batch culture evaluation, there were significant increases in the organic matter (OM) digestibility, the total gas production expressed as ml/g of dry matter, the OM, the neutral detergent fibre (NDF) and the acid detergent fibre (ADF) of the supplemented rations, as compared to the control, excluding the rations supplemented with T. viride and B. circulans. In the RUSITEC, the ration supplemented with mixed inoculants showed significantly higher digestibility of crude protein, ether extract, NDF and ADF than did the ration supplemented with the P. chrysosporium and B. subtilis inoculants. It can be concluded that the simultaneous use of fungal and bacterial exogenous cellulases on rice straw roughage improves its digestibility, without negative effects on other rumen parameters.

Keywords

In vitrorumenenzymeinoculantdigestibility
Type
Animal Research Paper
Information
The Journal of Agricultural Science , Volume 158 , Issue 4 , May 2020 , pp. 326 - 338
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Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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Footnotes

*

Contributed equally to this study.

References

Adesogan, AT, Ma, ZX, Romero, JJ and Arriola, KG (2014) Ruminant nutrition symposium: improving cell wall digestion and animal performance with fibrolytic enzymes. Journal of Animal Science 92, 1317–1330.CrossRefGoogle ScholarPubMed
Allen, MS and Mertens, DR (1988) Evaluating constraints on fibre digestion by rumen microbes. Journal of Nutrition 118, 261–270.CrossRefGoogle ScholarPubMed
Anantasook, N and Wanapat, M (2012) Influence of rain tree pod meal supplementation on rice straw-based diets using in vitro gas fermentation technique. Asian–Australasian Journal of Animal Sciences 25, 325–334.CrossRefGoogle ScholarPubMed
AOAC (2007) Association of Official Analytical Chemists, 18th Edn edn, Gaithersburg, MA, USA: Official Methods of Analysis.Google Scholar
Arriola, KG, Oliveira, AS, Ma, ZX, Lean, IJ, Giurcanu, MC and Adesogan, AT (2017) A meta-analysis on the effect of dietary application of exogenous fibrolytic enzymes on the performance of dairy cows. Journal of Dairy Science 100, 4513–4527.CrossRefGoogle ScholarPubMed
Beauchemin, KA, Colombatto, D, Morgavi, D and Yang, W (2003) Use of exogenous fibrolytic enzymes to improve feed utilization by ruminants. Journal of Animal Science 81, E37–E47.Google Scholar
Bhatta, R, Enishi, O and Kurihara, M (2007) Measurement of methane production from ruminants. Asian–Australasian Journal of Animal Sciences 20, 1305–1318.CrossRefGoogle Scholar
Blümmel, and Ørskov, ER (1993) Comparison of in vitro gas production and nylon bag degradability of roughages in predicting feed intake in cattle. Animal Feed Science and Technology 40, 109–119.CrossRefGoogle Scholar
Bradford, M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.CrossRefGoogle ScholarPubMed
Cieslak, A, Zmora, P, Matkowski, A, Nawrot-Hadzik, I, Pers-Kamczyc, E, El-Sherbiny, M, Bryszak, M and Szumacher-Strabel, M (2016) Tannins from Sanguisorba officinalis affect in vitro rumen methane production and fermentation. Journal of Animal and Plant Sciences 26, 54–62.Google Scholar
De Los Angeles Olvera-Treviño, M, del Carmen Wacher-Rodarte, M and Canales, ALM (1989) An endoglucanase from an isolated strain of Bacillus circulans. Applied Microbiology and Biotechnology 31, 146–149.CrossRefGoogle Scholar
Demarchi, JJAA, Manella, MQ, Lourenço, AJ, Alleoni, GF, Frighetto, R and Primavesi, O (2003) Daily methane emission at different seasons of the year by Nelore cattle in Brasil grazing Brachiaria brizantha cv. Marandu. Preliminary results. World Conference on Animal Production, 9.Google Scholar
Ganai, AM, Sharma, T and Dhuria, RK (2015) Effect of yeast (Saccharomyces cerevisiae) supplementation on ruminal digestion of bajra (Pennisetum glaucum) straw and bajra straw-based complete feed in vitro. Animal Nutrition and Feed Technology 15, 145–153.CrossRefGoogle Scholar
Getachew, G, Makkar, HPS and Becker, K (2002) Tropical browses: contents of phenolic compounds, in vitro gas production and stoichiometric relationship between short chain fatty acid and in vitro gas production. Journal of Agricultural Science 139, 341–352.CrossRefGoogle Scholar
Gunun, P, Wanapat, M and Anantasook, N (2013) Effects of physical form and urea treatment of rice straw on rumen fermentation, microbial protein synthesis and nutrient digestibility in dairy steers. Asian–Australasian Journal of Animal Sciences 26, 1689–1697.CrossRefGoogle ScholarPubMed
Jacobs, MB and Gerstein, MJ (1960) Handbook of Microbiology (No. 576 J32).Google Scholar
Jalč, D, Lauková, A, Váradyová, Z, Homolka, P and Koukolová, V (2009) Effect of inoculated grass silages on rumen fermentation and lipid metabolism in an artificial rumen (RUSITEC). Animal Feed Science and Technology 151, 55–64.CrossRefGoogle Scholar
Jalilvand, G, Naserian, A, Kebreab, E, Odongo, NE, Valizadeh, R, Eftekhar Shahroodi, F, Lopez, S and France, J (2008) Rumen degradation kinetics of alfalfa hay, maize silage and wheat straw treated with fibrolytic enzymes. Archivos de Zootecnia 57, 155–164.Google Scholar
Keshk, SMAS and Sameshima, K (2005) Evaluation of different carbon sources for bacterial cellulose production. African Journal of Biotechnology 4, 478–482.Google Scholar
Klebaniuk, R, Kochman, G, Kowalczuk-Vasile, E, Grela, ER, Kowalczyk-Pecka, D and Bąkowski, M (2019) Dietary supplementation with glucogenic precursors and fatty acids improves performance and health of periparturient dairy cows. Animal Production Science 59, 109–121.CrossRefGoogle Scholar
Kumar, P, Barrett, DM, Delwiche, MJ and Stroeve, P (2009) Methods for pretreatment of lignocellulosic biomass for efficient hydrolysis and biofuel production. Industrial & Engineering Chemistry Research 48, 3713–3729.CrossRefGoogle Scholar
Kung, L Jr., Treacher, RJ, Nauman, GA, Smagala, AM, Endres, KM and Cohen, MA (2000) The effect of treating for ages with fibrolytic enzymes on its nutritive value and lactation performance of dairy cows. Journal of Dairy Science 83, 115–122.CrossRefGoogle Scholar
Kurihara, M (1995) Feeding method for dairy cattle to cope with global warming: technical assessment based on energy metabolism. Bulletin of Kyushu National Agricultural Experiment Station 29, 21–107.Google Scholar
Lamid, M, Ni Nyoman, TP and Sarwoko, M (2013) Addition of lignocellulolytic enzymes into rice straw improves in vitro rumen fermentation products. Journal of Applied Environmental and Biological Sciences 3, 166–171.Google Scholar
López, D, Elghandour, MMY, Salem, AZM, Vázquez-Armijo, JF, Salazar, MC and Gado, HM (2013) Influence of exogenous enzymes on in vitro gas production kinetics and dry matter degradability of a high concentrate diet. Animal Nutrition and Feed Technology 13, 527–536.Google Scholar
Lynd, LR, Weimer, PJ, Zyl, WH and Van Isak, S (2002) Microbial cellulose utilization: fundamentals and biotechnology microbial cellulose utilization: fundamentals and biotechnology. Microbiology and Molecular Biology Reviews 66, 506–577.CrossRefGoogle ScholarPubMed
Machmüller, A, Soliva, CR and Kreuzer, M (2002) In vitro ruminal methane suppression by lauric acid as influenced by dietary calcium. Canadian Journal of Animal Science 82, 233–239.CrossRefGoogle Scholar
Mai, C, Militz, H and Kües, U (2004) Biotechnology in the wood industry. Applied Microbiology and Biotechnology 63, 477–494.CrossRefGoogle ScholarPubMed
Malik, R and Bandla, S (2010) Effect of source and dose of probiotics and exogenous fibrolytic enzymes (EFE) on intake, feed efficiency, and growth of male buffalo (Bubalus bubalis) calves. Tropical Animal Health and Production 42, 1263–1269.CrossRefGoogle ScholarPubMed
Mandels, M (1969) The production of cellulases. Advances in Chemistry 95, 391–414.CrossRefGoogle Scholar
Menke, KH, Raab, L, Salewski, A, Steingass, H, Fritz, D and Schneider, W (1979) The estimation of the digestibility and metabolizable energy content of ruminant feeding stuffs from the gas production when they are incubated with rumen liquor in vitro. The Journal of Agricultural Science 93, 217–222.CrossRefGoogle Scholar
Miller, GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Analytical Chemistry 31, 426–428.CrossRefGoogle Scholar
Mocherla, VANS and Kavitha, P (2017) Role of exogenous fibrolytic enzymes in ruminant digestion: a review. International Journal of Current Microbiology and Applied Sciences 6, 1400–1408.Google Scholar
Peripolli, V, Barcellos, JOJ, Prates, ÊR, McManus, C, Stella, LA, Camargo, CM, Costa, JBG Jr and Bayer, C (2017) Additives on in vitro ruminal fermentation characteristics of rice straw. Revista Brasileira de Zootecnia 46, 240–250.CrossRefGoogle Scholar
Peters, A, Meyer, U and Dänicke, S (2015) Effect of exogenous fibrolytic enzymes on performance and blood profile in early and mid-lactation Holstein cows. Animal Nutrition 1, 229–238.CrossRefGoogle ScholarPubMed
Qiao, GH, Shan, AS, Ma, N, Ma, QQ and Sun, ZW (2009) Effect of supplemental Bacillus cultures on rumen fermentation and milk yield in Chinese Holstein cows. Journal of Animal Physiology and Animal Nutrition 94, 429–436.Google ScholarPubMed
Reddy, PRK, Raju, J, Reddy, AN, Ramadevi, A, Reddy, PRK and Raju, J (2016) Recent trends in supplementation of exogenous fibrolytic enzymes in ruminant nutrition: a review. Indian Journal of Natural Sciences 7, 11700–11708.Google Scholar
Romero, JJ, Zarate, MA, Queiroz, OCM, Han, JH, Shin, JH, Staples, CR, Brown, WF and Adesogan, AT (2013) Fibrolytic enzyme and ammonia application effects on the nutritive value, intake, and digestion kinetics of bermudagrass hay in beef cattle. Journal of Animal Science 91, 4345–4356.CrossRefGoogle ScholarPubMed
Salem, AZM, Gado, HM, Colombatto, D and Elghandour, MMY (2013) Effects of exogenous enzymes on nutrient digestibility, ruminal fermentation and growth performance in beef steers. Livestock Science 154, 69–73.CrossRefGoogle Scholar
Selçuk, Z, Çetinkaya, N, Salman, M and Genç, B (2016) The determination of in vitro gas production and metabolizable energy value of rice straw treated with exogenous fibrolytic enzymes. Turkish Journal of Veterinary and Animal Sciences 40, 707–713.CrossRefGoogle Scholar
Seo, JK, Kim, S, Kim, MH, Upadhaya, SD, Kam, DK and Ha, JK (2010) Direct-fed microbials for ruminant animals. Asian–Australasian Journal of Animal Sciences 23, 1657–1667.CrossRefGoogle Scholar
Sheikh, GG, Ganai, AM, Ishfaq, A, Afzal, Y and Ahmad, HA (2017) In vitro effect of probiotic mix and fibrolytic enzyme mixture on digestibility of paddy straw. Advances in Animal and Veterinary Sciences 5, 260–266.Google Scholar
Sloth, J, Bach, P, Jensen, AD and Kiil, S (2008) Evaluation method for the drying performance of enzyme containing formulations. Biochemical Engineering Journal 40, 121–129.CrossRefGoogle Scholar
Tang, SX, Tayo, GO, Tan, ZL, Sun, ZH, Shen, LX, Zhou, CS, Xiao, WJ, Ren, GP, Han, XF and Shen, SB (2008) Effects of yeast culture and fibrolytic enzyme supplementation on in vitro fermentation characteristics of low-quality cereal straws. Journal of Animal Science 86, 1164–1172.CrossRefGoogle ScholarPubMed
Tirado-González, DN, Miranda-Romero, LA, Ruíz-Flores, A, Medina-Cuéllar, SE, Ramírez-Valverde, R and Tirado-Estrada, G (2018) Meta-analysis: effects of exogenous fibrolytic enzymes in ruminant diets. Journal of Applied Animal Research 46, 771–783.CrossRefGoogle Scholar
Van Soest, PV, Robertson, JB and Lewis, BA (1991) Methods for dietary fiber, neutral detergent fiber, and non-starch polysaccharides in relation to animal nutrition. Journal of Dairy Science 74, 3583–3597.CrossRefGoogle Scholar
Varadyova, Z, Certik, M and Jalc, D (2018) The possible application of fungal enriched substrates in ruminant nutrition. A review. Journal of Animal and Feed Sciences 27, 3–10.Google Scholar
Wang, Y, Yan, J, Zhang, X and Han, B (2018) Tolerance properties and growth performance assessment of yarrowia lipolytic lipase in broilers. Journal of Applied Animal Research 46, 486–491.CrossRefGoogle Scholar
Wymelenberg, AV, Denman, S, Dietrich, D, Bassett, J, Yu, X, Atalla, R, Predki, P, Rudsander, U, Teeri, TT and Cullen, D (2002) Transcript analysis of genes encoding a family 61 endoglucanase and a putative membrane-anchored family 9 glycosyl hydrolase from Phanerochaete chrysosporium. Applied and Environmental Microbiology 68, 5765–5768.CrossRefGoogle Scholar
Yang, WZ, Beauchemin, KA and Rode, LM (1999) Effects of an enzyme feed additive on extent of digestion and milk production of lactating dairy cows. Journal of Dairy Science 82, 391–403.CrossRefGoogle ScholarPubMed
Yang, WZ, Beauchemin, KA and Rode, LM (2000) A comparison of methods of adding fibrolytic enzymes to lactating cow diets. Journal of Dairy Science 83, 2512–2520.CrossRefGoogle ScholarPubMed
Zayed, MS (2018) Enhancement the feeding value of rice straw as animal fodder through microbial inoculants and physical treatments. International Journal of Recycling of Organic Waste in Agriculture 7, 117–124.CrossRefGoogle Scholar
Zhang, YHP and Lynd, LR (2004) Kinetics and relative importance of phosphorolytic and hydrolytic cleavage of cellodextrins and cellobiose in cell extracts of Clostridium thermocellum. Applied and Environmental Microbiology 70, 1563–1569.CrossRefGoogle ScholarPubMed