Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-30T19:01:39.223Z Has data issue: false hasContentIssue false
  • English
  • Français

Goats fed with non-protein nitrogen: ruminal bacterial community and ruminal fermentation, intake, digestibility and nitrogen balance

Published online by Cambridge University Press:  05 April 2021

A.S.M. Lopes ,
J.S. de Oliveira ,
E.M. Santos ,
A.N. Medeiros ,
P.E.N. Givisiez ,
M.L.P. Lemos ,
F.N.S. Santos Open the ORCID record for F.N.S. Santos [Opens in a new window] ,
N.M.V. Silva ,
P.S. Azevedo  and
L.S. Sousa
...Show all authors
A.S.M. Lopes
Affiliation:
Department of Animal Science, Federal University of Paraíba, Areia, PB, Brazil
J.S. de Oliveira*
Affiliation:
Department of Animal Science, Federal University of Paraíba, Areia, PB, Brazil
E.M. Santos
Affiliation:
Department of Animal Science, Federal University of Paraíba, Areia, PB, Brazil
A.N. Medeiros
Affiliation:
Department of Animal Science, Federal University of Paraíba, Areia, PB, Brazil
P.E.N. Givisiez
Affiliation:
Department of Animal Science, Federal University of Paraíba, Areia, PB, Brazil
M.L.P. Lemos
Affiliation:
Department of Animal Science, Federal University of Paraíba, Areia, PB, Brazil
F.N.S. Santos
Affiliation:
Department of Animal Science, Federal University of Paraíba, Areia, PB, Brazil
N.M.V. Silva
Affiliation:
Department of Animal Science, Federal University of Paraíba, Areia, PB, Brazil
P.S. Azevedo
Affiliation:
Department of Animal Science, Federal University of Paraíba, Areia, PB, Brazil
L.S. Sousa
Affiliation:
Department of Animal Science, Federal University of Paraíba, Areia, PB, Brazil
D.M. Pereira
Affiliation:
Department of Animal Science, Federal University of Paraíba, Areia, PB, Brazil
C.J.B. Oliveira
Affiliation:
Department of Animal Science, Federal University of Paraíba, Areia, PB, Brazil
*
Author for correspondence: J. S. de Oliveira, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The current study assessed ruminal fermentation parameters and bacterial community, nutrient intake, nutrient digestibility and nitrogen balance of goats fed diets containing buffel grass hay and ruminal ammonia nitrogen (N-NH3). Five rumen-cannulated mixed-breed castrated adult goats (45 ± 2.3 kg) were used in a 5 × 5 Latin square design represented by five N-NH3 levels (3.43, 9.95, 17.2, 23.0 and 33.7 mg/dl). Control animals were fed hay exclusively. Other treatments were represented by ruminal infusion composed of a mixture containing urea, ammonium sulphate and casein. The increasing N-NH3 concentrations did not affect rumen fluid pH, which averaged 6.43. Rumen ammoniacal nitrogen increased linearly in response to N-NH3. Volatile fatty acids were not affected by increasing N-NH3 concentrations. A higher abundance of Ruminococcaceae (Ruminococcus 1, Ruminococcaceae UCG-014 and Ruminococcaceae NK4A214 group) was observed in the rumen of goats infused with higher concentrations of N-NH3 (17.2 and 33.7 mg/dl N-NH3). There was a quadratic effect (P < 0.050) of N-NH3 levels on neutral detergent fibre intake with maximum values estimated at 13.7 mg/dl N-NH3. Nutrient intake, nitrogen excretion and nitrogen balance presented a positive linear effect (P < 0.050). In conclusion, 3.43 mg/dl of N-NH3 is the minimum level to maintain microbial activity, whereas the recommended level to optimize the microbial community is 14.5 mg/dl of N-NH3 in the rumen of goats fed buffel grass.

Keywords

Ammoniacrude proteinfibreruminal bacteria
Type
Animal Research Paper
Information
The Journal of Agricultural Science , Volume 158 , Issue 8-9 , November 2020 , pp. 781 - 790
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

AOAC (2012) Official Methods of Analysis, 19th Edn. Gaithersburg, MD, USA: Association of Official Analytical Chemists International.Google Scholar
Batista, ED, Detmann, E, Titgemeyer, EC, Valadares Filho, SC, Valadares, RFD, Prates, LL, Rennó, LN and Paulino, MF (2016) Effects of varying ruminally undegradable protein supplementation on forage digestion, nitrogen metabolism, and urea kinetics in Nellore cattle fed low-quality tropical forage. Journal of Animal Science 94, 201–216.CrossRefGoogle ScholarPubMed
Berchielli, TT, Pires, AV and Oliveirapires, SG (2006) Nutrição de Ruminantes. Jaboticabal, SP, Brazil: Funep.Google Scholar
Bolyen, E, Rideout, JR, Dillon, MR, Bokulich, NA, Abnet, CC, Al-Ghalith, GA, Knights, D, Koester, I, Kosciolek, T, Kreps, J, Langille, MGI, Lee, J, Ley, R, Liu, YX, Loftfield, E, Lozupone, C, Maher, M, Marotz, C, Martin, BD, McDonald, D, McIver, LJ, Melnik, AV, Metcalf, JL, Morgan, SC, Morton, JT, Naimey, AT, Navas-Molina, JA, Nothias, LF, Orchanian, SB, Pearson, T, Peoples, SL, Petras, D, Preuss, ML, Pruesse, E, Rasmussen, LB, Rivers, A, Robeson, MS 2nd, Rosenthal, P, Segata, N, Shaffer, M, Shiffer, A, Sinha, R, Song, SJ, Spear, JR, Swafford, AD, Thompson, LR, Torres, PJ, Trinh, P, Tripathi, A, Turnbaugh, PJ, Ul-Hasan, S, van der Hooft, JJJ, Vargas, F, Vázquez-Baeza, Y, Vogtmann, E, von Hippel, M, Walters, W, Wan, Y, Wang, M, Warren, J, Weber, KC, Williamson, CHD, Willis, AD, Xu, ZZ, Zaneveld, JR, Zhang, Y, Zhu, Q, Knight, R, Caporaso, JG and Bai, Y (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nature Biotechnology 37, 852–857. https://doi:10.1038/s41587-019-0209-9.CrossRefGoogle ScholarPubMed
Chaney, AL and Marbach, EP (1962) Modified reagents for determination of urea and ammonia. Clinical Chemistry 8, 130–132.CrossRefGoogle ScholarPubMed
Chen, XB and Gomes, MJ (1992) Estimation of microbial protein supply to sheep and cattle based on urinary excretion of purine derivatives – an overview of technical details. Rowett Research Institute 9SB, 1–21.Google Scholar
Cherdthong, A and Wanapat, M (2010). Development of urea products as rumen slow-release feed for ruminant production: a review. Australiana Journal of Basic and Applied Sciences 4, 2232–2241.Google Scholar
Dehority, BA (1973) Hemicellulose degradation by rumen bactéria. Federation Proceedings 32, 1819–1825.Google ScholarPubMed
Detmann, E, Paulino, MF, Valadares Filho, SC and Lana, RP (2007) Fatores controladores de consumo em suplementos múltiplos fornecidos ad libitum para bovinos manejados a pasto. Cadernos Técnicos de Veterinária e Zootecnia 55, 73–93.Google Scholar
Detmann, E, Paulino, MF, Mantovani, HC, Valadares Filho, SC, Sampaio, CB, Souza, MA, Lazzarini, I and Detmann, KSC (2009) Parameterization of ruminal fibre degradation in low-quality tropical forage using Michaelis–Menten kinetics. Livestock Science 126, 136–146.CrossRefGoogle Scholar
Dušková, D and Marounek, M (2001) Fermentation of pectin and glucose, and activity of pectin-degrading enzymes in the rumen bacterium Lachnospira multiparus. Letters in Applied Microbiology 33, 159–163.CrossRefGoogle ScholarPubMed
Edgar, RC, Haas, BJ, Clemente, JC, Quince, C and Knight, R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics (Oxford, England) 27, 2194–2200.CrossRefGoogle ScholarPubMed
Ferreira, LMM, Hervas, G, Belenguer, A, Celaya, R, Rodrigues, MAM, Garcia, U, Frutos, P and Osoro, K (2017) Comparison of feed intake, digestion and rumen function among domestic ruminant species grazing in upland vegetation communities. Journal of Animal Physiology and Animal Nutrition 5, 846–856.CrossRefGoogle Scholar
Figueiras, JF, Detmann, E, Paulino, MF, Valente, TNP, Valadares Filho, SC and Lazzarini, I (2010) Intake and digestibility in cattle under grazing supplemented with nitrogenous compounds during dry season. Revista Brasileira de Zootecnia 39, 1303–1312.CrossRefGoogle Scholar
Flythe, M and Kagan, I (2010) Antimicrobial effect of red clover (Trifolium pratense) phenolic extract on the ruminal hyper ammonia-producing bacterium, Clostridium sticklandii. Current Microbiology 61, 125–131.CrossRefGoogle ScholarPubMed
Gagen, EJ, Padmanabha, J, Denman, SE and McSweeney, CS (2015) Hydrogenotrophic culture enrichment reveals rumen Lachnospiraceae and Ruminococcaceae acetogens and hydrogen-responsive Bacteroidetes from pasture-fed cattle. FEMS Microbiology Letters 362, 1–8.CrossRefGoogle ScholarPubMed
Gradel, CM and Dehority, BA (1972) Fermentation of isolated pectin and pectin from intact forages by pure cultures of rumen bactéria. Journal of Applied Microbiology 23, 332–340.CrossRefGoogle ScholarPubMed
Hobson, PN and Stewart, CS (1997) The Rumen Microbial Ecosystem, 2nd Edn. London: Blackie Academic & Professional.CrossRefGoogle Scholar
Jin, D, Zhao, S, Zheng, N, Beckers, Y and Wang, J (2018) Urea metabolism and regulation by rumen bacterial urease in ruminants – a review. Annals of Animal Science 18, 303–318.CrossRefGoogle Scholar
Kamra, DN (2005) Rumen microbial ecosystem. Current Science 89, 124–134.Google Scholar
Katoh, K, Misawa, K, Kuma, K and Miyata, T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 3059–3066.CrossRefGoogle ScholarPubMed
Khattab, IM, Salem, AZM, Abdel-Wahed, AM and Kewan, KZ (2013) Effects of urea supplementation on nutrient digestibility, nitrogen utilisation and rumen fermentation in sheep fed diets containing dates. Livestock Science 155, 223–229.CrossRefGoogle Scholar
Ladeira, MM, Rodriguez, NM, Borges, I, Gonçalves, LC, Saliba, EOS and Miranda, LF (2002) Balanço de nitrogênio, degradabilidade de aminoácidos e concentração de ácidos graxos voláteis no rúmen de ovinos alimentados com feno de Stylosanthes guianensis. Revista Brasileira de Zootecnia 31(6), 2357–2363.CrossRefGoogle Scholar
Lage, FF (2009) Caracterização química e quantificação de compostos fenólicos em forrageiras (Dissertação de mestrado). Universidade Federal de Lavras, Brasil.Google Scholar
Leng, RA (1990) Factors affecting the utilization of poor-quality forages by ruminants particularly under tropical conditions. Nutrition Research Reviews 3, 277–303.CrossRefGoogle ScholarPubMed
Lozupone, C and Knight, R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Applied and Environmental Microbiology 71, 8228–8235.CrossRefGoogle ScholarPubMed
Lu, Z, Shen, H and Shen, Z (2019) Effects of dietary-SCFA on microbial protein synthesis and urinal urea-N excretion are related to microbiota diversity in rumen. Frontiers in Physiology 10, 1–13.CrossRefGoogle ScholarPubMed
McMurdie, PJ and Holmes, S (2013). Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8, 1–11.CrossRefGoogle Scholar
Mertens, DR (2002) Gravimetric determination of amylase-treated neutral detergent fiber in feed with refluxing in beakers or crucibles. Journal of AOAC Institute 85, 1217–1240.Google ScholarPubMed
Michalski, JP, Kowalczyk, J, Voigt, J, Hammon, HM and Czauderna, M and Metges, CC (2012) Efficiency of endogenous urea 15N nitrogen incorporation into bacterial and milk protein of goats fed diets with three different protein levels. Journal of Animal and Feed Sciences 21, 599–612.CrossRefGoogle Scholar
Moreira, JN, Lira, MA, Santos, MVF, Araujo, GGL and Silva, GC (2007) Potencial de produção de capim-buffel na época seca no semi-árido Pernambucano. Revista Caatinga 20, 22–29.Google Scholar
Noro, M and Wittwer, F (2012) Relationships between liver ureagenesis and gluconeogenesis in ruminants fed with a high nitrogen diet. Veterinaria México 43, 143–154.Google Scholar
NRC (2007) National Research Council. Nutrient Requeriments of Small Ruminants. 11th Edn. Washington, DC, USA: National Academy Press.Google Scholar
O'Donnell, MM, Harris, HMB, Ross, RP and O'Toole, PW (2017) Core fecal microbiota of domesticated herbivorous ruminant, hindgut fermenters, and monogastric animals. Microbiology Open 509, 1–11.Google Scholar
Oliveira, JS, Zanini, AM and Santos, EM (2007) Fisiologia, manejo e alimentação de bezerros de corte. Arquivos de Ciências Veterinária e Zootecnia 10, 39–48.Google Scholar
Pacheco, D and Waghorn, GC (2008) Dietary nitrogen – definitions, digestion, excretion and consequences of excess for grazing ruminants. Proceedings of the New Zealand Grassland 70, 107–116.CrossRefGoogle Scholar
Paciullo, DSC (2002) Anatomical traits related with nutritive value of forage grasses. Ciência Rural 32, 357–364.CrossRefGoogle Scholar
Paulino, PVR, Valadares Filho, SC, Detmann, E, Valadares, RFD, Fonseca, MA, Véras, RML and Oliveira, DM (2008) Desempenho produtivo de bovinos Nelore de diferentes classes sexuais alimentados com dietas contendo dois níveis de oferta de concentrado. Revista Brasileira de Zootecnia 37, 1079–1087.CrossRefGoogle Scholar
Perazzo, AF, Homem Neto, SP, Ribeiro, OL, Santos, EM, Carvalho, GG, Oliveira, JS, Bezerra, HF, Campos, FS and Freitas Junior, JE (2017) Intake and ingestive behavior of lambs fed diet as containing ammoniated buffel grass hay. Tropical Animal Health Production 49, 717–724.CrossRefGoogle ScholarPubMed
Pereira, GA, Oliveira, JSD, Santos, EM, Carvalho, GGP, Araújo, GGL, Sousa, WHD and Cartaxo, FQ (2018) Substitution of soybean meal for urea in diets based on deferred buffel grass hay for feedlot sheep. Revista Brasileira de Zootecnia 47, 1–11.CrossRefGoogle Scholar
Pinho, RMA, Santos, EM, Bezerra, HC, Oliveira, JS, Carvalho, GGP, Campos, FS, Pereira, GA and Correa, RM (2013) Avaliação de fenos de capim-buffel colhido em diferentes alturas de corte. Revista Brasileira de Saúde e Produção Animal 14, 437–447.CrossRefGoogle Scholar
Pires, PRS, Santana Neto, JA, Oliveira, JS, Oliveira, CJB, Santos, EM and Santos, VS (2016) Efeito de diferentes concentrações da amônia ruminal sobre a degradação in vitro da fibra em detergente neutro de forragem de baixa qualidade. In: X Simpósio Paraibano de Zootecnia. Areia, PB, Brazil: UFPB, pp. 1–3.Google Scholar
Price, MN, Dehal, PS and Arkin, AP (2010) FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS ONE 5, 94–90.CrossRefGoogle ScholarPubMed
Quast, C, Pruesse, E, Yilmaz, P, Gerken, J, Schweer, T, Yarza, P, Peplies, J and Glöckner, FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research 41, 590–596.CrossRefGoogle ScholarPubMed
Rognes, T, Flouri, T, Nichols, B, Quince, C and Mahé, F (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4, 1–22.CrossRefGoogle ScholarPubMed
Salah, N, Sauvant, D and Archimède, H (2014) Nutritional requirements of sheep, goats and cattle in warm climates: a meta-analysis. Animal: An International Journal of Animal Bioscience 8, 1439–1447.CrossRefGoogle ScholarPubMed
Sampaio, CB, Detmann, E, Lazzarini, I, Souza, MAS, Paulino, MF and Valadares Filho, SC (2009). Rumen dynamics of neutral detergent fiber in cattle fed low-quality tropical forage and supplemented with nitrogenous compounds. Revista Brasileira de Zootecnia 38, 560–569.CrossRefGoogle Scholar
Santana, MCA and Cavali, J (2006) Foundations and comparative evaluation of methods for analysis of lignin in forages. Revista Electrónica de Veterinaria 7, 1–13.Google Scholar
Santana Neto, JA, Oliveira, JS, Oliveira, CJB, Santos, EM, Costa, ECB, Saraiva, CAS and Pinho, RMA (2019) Ammonia levels on in vitro degradation of fibrous carbohydrates from buffel grass. South African Journal of Animal Science 49, 585–597.CrossRefGoogle Scholar
Santos, AB, Pereira, M, Silva, HG, Pedreira, MS, Carvalho, GG, Ribeiro, LS, Almeida, PJ, Pereira, TC and Moreira, JV (2014) Nitrogen metabolism in lactating goats fed with diets containing different protein sources. Asian-Australasian Journal of Animal Sciences 27, 658–666.CrossRefGoogle ScholarPubMed
SAS (2002) Statistical Analysis System. Institute Inc., User's guide: Version 8, 6th Edn. Cary: SAS Institute.Google Scholar
Satter, LD and Slyter, LL (1974) Effect of ammonia concentration on rumen microbial production in vitro. British Journal of Nutrition 32, 199–208.CrossRefGoogle ScholarPubMed
Segata, N, Izard, J, Waldron, G, Miropolsky, D, Garret, WS and Huttenhower, C (2011) Metagenomic biomarker discovery and explanation. Genome Biology 12, 1–18.CrossRefGoogle ScholarPubMed
Shi, PJ, Meng, K, Zhou, ZG, Wang, YR, Diao, QY and Yao, B (2008) The host species affects the microbial community in the goat rumen. Applied Microbiology 46, 132–135.Google ScholarPubMed
Sniffen, CJ, O'Connor, JD, Van Soest, PJ, Fox, DG and Russel, JB (1992) A net carbohydrate and protein system for evaluating cattle diets. 2. Carbohydrate and protein availability. Journal Animal Science 70, 3562–3577.CrossRefGoogle Scholar
Stefański, T, Ahvenjärvi, S, Vanhatalo, A and Huhtanen, P (2020) Ruminal metabolism of ammonia N and rapeseed meal soluble N fraction. Journal of Dairy Science 103, 7081–7093.CrossRefGoogle ScholarPubMed
Valadares, RFD, Broderick, GA, Valadares Filho, SC and Clayton, MK (1999) Effect of replacing alfalfa silage with high moisture corn on ruminal protein synthesis estimated from excretion of total purine. Journal of Dairy Science 82, 2686–2696.CrossRefGoogle ScholarPubMed
Van Soest, PJ (1994) Nutritional Ecology of the Ruminant, 2nd Edn. Ithaca, USA: Comstock Publishing Associates.CrossRefGoogle Scholar
Van Soest, PJ, Robertson, JB and Lewis, BA (1991). Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. Journal of Dairy Science 74, 3583–3597.CrossRefGoogle ScholarPubMed
Wang, L, Xu, Q, Kong, F, Yang, Y, Wu, D, Mishra, S and Li, Y (2016) Exploring the goat rumen microbiome from seven days to two years. PLoS ONE 11, 1–13.Google ScholarPubMed
Witzig, M, Boguhn, J, Kleinsteuber, S, Fetzer, I and Rodehutscord, M (2010) Influence of the maize silage to grass silage ratio and feed particle size of rations for ruminants on the community structure of ruminal Firmicutes in vitro. Journal of Applied Microbiology 109, 1998–2010.CrossRefGoogle ScholarPubMed
Zeoula, LM, Fereli, F, Prado, IN, Geron, LJV, Caldas Neto, SF, Prado, OPP and Maeda, EM (2006). Digestibilidade e balanço de nitrogênio de rações com diferentes teores de proteína degradável no rúmen e milho moído como fonte de amido em ovinos. Revista Brasileira de Zootecnia 35, 2179–2186.CrossRefGoogle Scholar