Hostname: page-component-6bf8c574d5-pdxrj Total loading time: 0 Render date: 2025-03-07T11:23:58.015Z Has data issue: false hasContentIssue false
  • English
  • Français

The microbiome of the digestive system of ruminants – a review

Published online by Cambridge University Press:  10 January 2020

Paulina Cholewińska Open the ORCID record for Paulina Cholewińska [Opens in a new window] ,
Katarzyna Czyż ,
Piotr Nowakowski  and
Anna Wyrostek
Paulina Cholewińska*
Affiliation:
Institute of Animal Breeding, Wroclaw University of Environmental and Life Sciences, Chelmonskiego 38C, 51-630Wroclaw, Poland
Katarzyna Czyż
Affiliation:
Institute of Animal Breeding, Wroclaw University of Environmental and Life Sciences, Chelmonskiego 38C, 51-630Wroclaw, Poland
Piotr Nowakowski
Affiliation:
Institute of Animal Breeding, Wroclaw University of Environmental and Life Sciences, Chelmonskiego 38C, 51-630Wroclaw, Poland
Anna Wyrostek
Affiliation:
Institute of Animal Breeding, Wroclaw University of Environmental and Life Sciences, Chelmonskiego 38C, 51-630Wroclaw, Poland
*
Author for correspondence: Paulina Cholewińska, Institute of Animal Breeding, Wroclaw University of Environmental and Life Sciences, Chelmonskiego 38C, 51-630Wroclaw, Poland. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

This review aims to explain the influence and characterization of the microbiome in the ruminant digestive system by presenting the knowledge collected so far. The knowledge presented in this work is focused on the main factors affecting the microbiome and the main dependencies that have been found in it so far. The microbiome in the rumen is the first to come into contact with the biomass of the forage and its main purpose is to decompose into smaller particles or compounds. With the gradual increase in knowledge about the microbiome, there is a chance to manipulate it so that the animal continues to live in a symbiotic relationship with it, while reducing greenhouse gas emissions to the environment as well as increasing feed efficiency. Therefore, understanding the influence of the ruminant microbiome is the main step to achieve such results. However, learning the relationship between microorganisms is only at an early stage, because research focuses mainly on taxonomy. Future research should focus on interactions in the ecosystem which is the microbiome, on explaining individual functions and on influence of environmental factors.

Keywords

Digestive systemmicrobiomeruminants
Type
Review Article
Information
Animal Health Research Reviews , Volume 21 , Issue 1 , June 2020 , pp. 3 - 14
Check for updates
Copyright
Copyright © Cambridge University Press 2020

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

Abecia, L, Martín-García, AI, Martínez, G, Newbold, CJ and Yáñez-Ruiz, DR (2013) Nutritional intervention in early life to manipulate rumen microbial colonization and methane output by kid goats postweaning. Journal of Animal Science 91, 4832–4840.CrossRefGoogle ScholarPubMed
Adams, MR and Hall, CJ (1988) Growth inhibition of food-borne pathogens by lactic and acetic acid and their mixtures. International Journal of Food Science & Technology 23, 278–291.Google Scholar
Allison, MJ, Mayberry, WR, Mcsweeney, CS and Stahl, DA (1992) Synergistes jonesii, gen. nov., sp. nov.: a rumen bacterium that degrades toxic pyridinediols. Systematic and Applied Microbiology 15, 522–529.CrossRefGoogle Scholar
Avguštin, G, Wright, F and Flint, HJ (1994) Genetic diversity and phylogenetic relationships among strains of Prevotella (Bacteroides) ruminicola from the rumen. International Journal of Systematic and Evolutionary Microbiology 44, 246–255.Google ScholarPubMed
Barbosa, TM and Levy, SB (2000) The impact of antibiotic use on resistance development and persistence. Drug Resistance Updates 3, 303–311.CrossRefGoogle ScholarPubMed
Brown, D (2018) Optimising rumen health and the effect this will have on ketosis. Livestock 23, 174–178.CrossRefGoogle Scholar
Brzóska, F and Śliwiński, B (2011) Quality of ruminant feed in ruminant nutrition and its evaluation methods. II. Methods of analyzing and evaluating the nutritional value of volumetric fodder. Wiad Zootech 4, 57–68.Google Scholar
Chaucheyras-Durand, F and Durand, H (2009) Probiotics in animal nutrition and health. Beneficial Microbes 1, 3–9.CrossRefGoogle Scholar
Chilliard, Y, Ferlay, A and Doreau, M (2001) Effect of different types of forages, animal fat or marine oils in cow's diet on milk fat secretion and composition, especially conjugated linoleic acid (CLA) and polyunsaturated fatty acids. Livestock Production Science 70, 31–48.CrossRefGoogle Scholar
Collen, A (2016) Silent microbial authority. Bukowy Las, 69–100.Google Scholar
Dämmgen, U, Haenel, HD, Rösemann, C, Hutchings, NJ, Brade, W and Lebzien, P (2009) Improved national calculation procedures to assess energy requirements, nitrogen and VS excretions of dairy cows in the German emission model GAS-EM. Landbauforsch Voelkenrode 59, 233–252.Google Scholar
De Menezes, AB, Lewis, E, O'Donovan, M, O'Neill, BF, Clipson, N and Doyle, EM (2011) Microbiome analysis of dairy cows fed pasture or total mixed ration diets. FEMS Microbiology Ecology 78, 256–265.CrossRefGoogle ScholarPubMed
De Nadra, M (2007) Nitrogen metabolism in lactic acid bacteria from fruits: a review. Commun. Curr. Res. Educ. Topics. Trends Applied Microbiology 1, 500–510.Google Scholar
De Nardi, R, Marchesini, G, Li, S, Khafipour, E, Plaizier, JC, Gianesella, M, Ricci, R, Andrighetto, I and Segato, S (2016) Metagenomic analysis of rumen microbial population in dairy heifers fed a high grain diet supplemented with dicarboxylic acids or polyphenols. BMC Veterinaryu Research 12, 29.CrossRefGoogle ScholarPubMed
Deng, L, He, C, Zhou, Y, Xu, L and Xiong, H (2017) Ground transport stress affects bacteria in the rumen of beef cattle: a real-time PCR analysis. Animal Science Journal 88, 790–797.CrossRefGoogle ScholarPubMed
Dodd, D, Kiyonari, S, Mackie, RI and Cann, IK (2010) Functional diversity of four glycoside hydrolase family 3 enzymes from the rumen bacterium Prevotella bryantii B14. Journal of Bacteriology 192, 2335–2345.CrossRefGoogle ScholarPubMed
Efenberger, M, Brzezińska-Błaszczyk, E and Wódz, K (2014) Archeony – drobnoustroje ciągle nieznane. Postepy Higieny i Medycyny Doswiadczalnej 68, 1452–1463.CrossRefGoogle Scholar
FAO (2018) Global Livestock Environmental Assessment Model (GLEAM) – Assessment of greenhouse gas emissions and mitigation potential – version 2.0, July 2018.Google Scholar
Fernando, SC, Purvis, HT, Najar, FZ, Sukharnikov, LO, Krehbiel, CR, Nagaraja, TG and DeSilva, U (2010) Rumen microbial population dynamics during adaptation to a high-grain diet. Applied and Environmental Microbiology 76, 7482–7490.CrossRefGoogle ScholarPubMed
Fonty, G, Gouet, P, Jouany, JP and Senaud, J (1987) Establishment of the microflora and anaerobic fungi in the rumen of lambs. Journal of General Microbiology 133, 1835–1843.Google Scholar
Gabryszuk, M, Sakowski, T, Metera, E, Kuczyńska, B and Rembiałkowska, E (2013) Effect of nutrition on the content of bioactive components in cow milk from organic farms. Food Sci. Technol. Qual 3, 16–26.Google Scholar
Gajewska, J and Błaszczyk, MK (2012) Probiotyczne bakterie fermentacji mlekowej, LAB. Postepy Mikrobiol 51, 55–65.Google Scholar
Gao, F, Warren, A, Zhang, Q, Gong, J, Miao, M, Sun, P and Song, W (2016) The all-data-based evolutionary hypothesis of ciliated protists with a revised classification of the phylum Ciliophora (eukaryota, Alveolata). Scientific Reports 6, 24847.Google Scholar
Gliński, Z and Kostro, K (2015) Mikrobiom – charakterystyka i znaczenie. Życie Weterynaryjne 90, 7.Google Scholar
Górniak, W, Cholewińska, P and Konkol, D (2018) Feed additives produced on the basis of organic forms of micronutrients as a means of biofortification of food of animal origin. Journal of Chemistry 8, 1–9.CrossRefGoogle Scholar
Graham, S Mr (2010) Introduction, impact and retention of Synergistes jonesii in cattle herds grazing Leucaena leucocephala. The University of Queensland, School of Agriculture and Food Sciences.Google Scholar
Hanafy, RA, Johnson, B, Elshahed, MS and Youssef, NH (2018) Anaeromyces contortus sp. nov., a new anaerobic gut fungal species (Neocallimastigomycota) isolated from the feces of cow and goat. Mycologia 110, 502–512.CrossRefGoogle ScholarPubMed
Henderson, G, Cox, F, Ganesh, S, Jonker, A and Young, W (2015) Rumen microbial community composition varies with diet and host, but a core microbiome is found across a wide geographical range. Scientific Reports 5, 14567.CrossRefGoogle ScholarPubMed
Hernandez-Sanabria, E, Goonewardene, LA, Li, M, Mujibi, DF, Stothard, P, Moore, SS and Leon-Quintero, MC (2010) Correlation of particular bacterial PCR-denaturing gradient gel electrophoresis patterns with bovine ruminal fermentation parameters and feed efficiency traits. Applied and Environmental Microbiology 76, 6338–6350.CrossRefGoogle ScholarPubMed
Jami, E, Israel, A, Kotser, A and Mizrahi, I (2013) Exploring the bovine rumen bacterial community from birth to adulthood. The ISME Journal 7, 1069–1079.CrossRefGoogle ScholarPubMed
Jami, E, White, BA and Mizrahi, I (2014) Potential role of the bovine rumen microbiome in modulating milk composition and feed efficiency. PLoS One 9, e85423.CrossRefGoogle ScholarPubMed
Janssen, PH and Kirs, M (2008) Structure of the archaeal community of the rumen. Applied and Environmental Microbiology 74, 3619–3625.CrossRefGoogle ScholarPubMed
Jewell, KA, McCormick, C, Odt, CL, Weimer, PJ and Suen, G (2015) Ruminal bacterial community composition in dairy cows is dynamic over the course of two lactations and correlates with feed efficiency. Applied and Environmental Microbiology 1, AEM-00720, 4697–4710.CrossRefGoogle Scholar
Kassow, A, Rahmann, G, Blank, B, Paulsen, HM and Aulrich, K (2009). Studies on greenhouse gas emissions in organic and conventional dairy farms, in Ressortforschung für den Ökologischen Landbau. Johann Heinrich von Thünen-Institut-Bundesforschungsinstitut für Ländliche Räume, Wald und Fischerei vTI. pp. 65–76.Google Scholar
Khafipour, E, Li, S, Plaizier, JC and Krause, DO (2009) Rumen microbiome composition determined using two nutritional models of subacute ruminal acidosis. Applied and Environmental Microbiology 75, 7115–7124.CrossRefGoogle ScholarPubMed
Khafipour, E, Li, S, Tun, HM, Derakhshani, H, Moossavi, S and Plaizier, JC (2016) Effects of grain feeding on microbiota in the digestive tract of cattle. Animal Frontiers 6, 13–19.CrossRefGoogle Scholar
Kirchgessner, M (1995) Nutritional factors for the quantification of methane production. Ruminant Physiology: Digestion, Metabolism, Growth and Reproduction. pp. 317–331.Google Scholar
Knapp, E, Sartelet, A, Malniece, A and Guyot, H (2017) Ruminal Function Influenced by Diet Parameters in Dairy Herds with Milk fat Drop Syndrome in Belgium. Belgium: European Buiatrics Forum.Google Scholar
Kong, Y, Xia, Y, Seviour, R, Forster, R and McAllister, TA (2013) Biodiversity and composition of methanogenic populations in the rumen of cows fed alfalfa hay or triticale straw. FEMS Microbiology Ecology 84, 302–315.CrossRefGoogle ScholarPubMed
Kumar, N, Singh, RK, Mishra, SK, Singh, AK and Pachouri, UC (2012) Isolation and screening of soil Actinomycetes as source of antibiotics active against bacteria. International Journal of Microbiology Research 2, 12.CrossRefGoogle Scholar
Laven, RA, Ashmore, A and Stewart, CS (2003) Escherichia coli in the rumen and colon of slaughter cattle, with particular reference to E. coli o157. Veterinary Journal 165, 78–83.CrossRefGoogle ScholarPubMed
Li, S, Khafipour, E, Krause, DO, Rodriguez-Lecompte, JC and Plaizier, JC (2010) Free endotoxins in the feces of lactating dairy cows. Canadian Journal of Animal Science 90, 591–594.CrossRefGoogle Scholar
Li, M, Zhou, M, Adamowicz, E and Basarab, JA (2012) Characterization of bovine ruminal epithelial bacterial communities using 16S rRNAsequencing, PCR-DGGE, and qRT-PCR analysis. Veterinary Microbiology 155, 72–80.CrossRefGoogle ScholarPubMed
Li, Z, Wright, AD, Liu, H, Bao, K, Zhang, T, Wang, K, Cui, X, Yang, F, Zhang, Z and Li, G (2015) Bacterial community composition and fermentation patterns in the rumen of sika deer (Cervus nippon) fed three different diets. PLoS One 10, e0123481.CrossRefGoogle Scholar
Lipiński, K (1998) Mechanizm działania probiotyków paszowych. Trzoda Chlewna 1, 65–67.Google Scholar
Ljungdahl, LG (2008) The cellulase/hemicellulase system of the anaerobic fungus orpinomycespc-2 and aspects of its applied use. Annals of the New York Academy of Sciences 1125, 308–321.CrossRefGoogle ScholarPubMed
Mackie, RI, Rycyk, M, Ruemmler, RL and Aminov, RI (2004) Biochemical and microbiological evidence for fermentative digestion in free-living land iguanas (Conolophus pallidus) and marine iguanas (Amblyrhynchus cristatus) on the Galapagos archipelago. Physiological and Biochemical Zoology 77, 127–138.CrossRefGoogle ScholarPubMed
Madigan, M and Martinko, J (2005). Brock Biology of Microorganisms, 11th Edn. Upper Saddle River, NJ: Prentice Hall, p. 149–152.Google Scholar
Makarova, K, Slesarev, A, Wolf, Y and Sorokin, A (2006) Comparative genomics of the lactic acid bacteria. Proceedings of the National Academy of Sciences 103, 15611–15616.CrossRefGoogle ScholarPubMed
Malmuthuge, N (2017) Understanding host-microbial interactions in rumen: searching the best opportunity for microbiota manipulation. Journal of animal science and biotechnology 8, 8.CrossRefGoogle ScholarPubMed
Mao, SY, Huo, WJ and Zhu, WY (2016) Microbiome–metabolome analysis reveals unhealthy alterations in the composition and metabolism of ruminal microbiota with increasing dietary grain in a goat model. Environmental Microbiology 18, 525–541.CrossRefGoogle Scholar
McAllister, TA, Okine, EK, Mathison, GW and Cheng, KJ (1996) Dietary environmental and microbiological aspects of methane production in ruminants. Canadian Journal of Animal Science 76, 231–243.CrossRefGoogle Scholar
McCann, JC, Wickersham, TA and Loor, JJ (2014) High-throughput methods redefine the rumen microbiome and its relationship with nutrition and metabolism. Bioinformatics and Biology Insights 8, BBI-S15389. https://doi.org/10.4137/BBI.S15389.CrossRefGoogle ScholarPubMed
McDonald, P, Edwards, RA, Greenhalgh, JFD, Morgan, CA, Sinclair, LA and Wilkinson, RG (2010). Animal Nutrition, 7th Edn. UK: Pearson Education, pp. 171–187.Google Scholar
Meale, SJ, Li, S, Azevedo, P, Derakhshani, H, Plaizier, JC, Khafipour, E and Steele, MA (2016) Development of ruminal and fecal microbiomes are affected by weaning but not weaning strategy in dairy calves. Frontiers in Microbiology 7, 582.CrossRefGoogle Scholar
Minuti, A, Palladino, A, Khan, MJ, Alqarni, S, Agrawal, A, Piccioli-Capelli, F and Loor, JJ (2015) Abundance of ruminal bacteria, epithelial gene expression, and systemic biomarkers of metabolism and inflammation are altered during the peripartal period in dairy cows. Journal of Dairy Science 98, 8940–8951.CrossRefGoogle ScholarPubMed
Mordak, R (2008) Monitorowanie problemów zdrowotnych stad bydła. Poland: MedPharm Wrocław, pp. 87–109.Google Scholar
Moss, AR, Jouany, JP and Newbold, J (2000) Methane production by ruminants: its contribution to global warming. Ann Zoot 49, 231–253.CrossRefGoogle Scholar
Newbold, C, Wallace, R and Mcintosh, F (1996) Mode of action of the yeast Saccharomyces cerevisiae as a feed additive for ruminants. British Journal of Nutrition 76, 249–261.CrossRefGoogle ScholarPubMed
Orpin, CG (1997) The occurrence of chitin in the cell walls of the rumen organisms Neocallimastix frontalis, Piromonas communis and Sphaeromonas communis. Journal of General Microbiology 99, 215–218.CrossRefGoogle Scholar
Palmquist, DL (1995) Digestibility of cotton lint fiber and whole oilseeds by ruminal microorganisms. Animal Feed Science and Technology 56, 231–242.CrossRefGoogle Scholar
Paster, BJ, Russell, JB, Yang, CMJ, Chow, JM and Woese, CR (1993) Phylogeny of the ammonia-producing ruminal bacteria Peptostreptococcus anaerobius, Clostridium sticklandii, and Clostridium aminophilum sp. nov. International Journal of Systematic and Evolutionary Microbiology 43, 107–110.Google ScholarPubMed
Perdigon, G, Alvarez, S and Medici, M (1992) Systemic and local augmentation of the immune response in mice by feeding with milk fermented with Lactobacillus acidophilus and/or Lactobacillus casei. Nutrition Research 1, 66–76.Google Scholar
Randhawa, SS, Dhaliwal, PS, Gupta, PP, Ahuja, AK and Rathor, SS (1989) Studies of clinico-biochemical and pathological changes in the urea-induced acute rumen alkalosis in buffalo calves. Acta Veterinaria Brno 58, 225–243.CrossRefGoogle Scholar
Rey, M, Enjalbert, F, Combes, S, Cauquil, L, Bouchez, O and Monteils, V (2014) Establishment of ruminal bacterial community in dairy calves from birth to weaning is sequential. Journal of Applied Microbiology 116, 245–257.CrossRefGoogle ScholarPubMed
Rodríguez, MM, Pérez, D, Chaves, FJ, Esteve, E, Marin-Garcia, P, Xifra, G and Portero-Otin, M (2015) Obesity changes the human gut mycobiome. Scientific Reports 5, 14600.CrossRefGoogle Scholar
Rolfe, RD (2000) The role of probiotic cultures in the control of gastrointestinal health. The Journal of Nutrition 130, 396S–402S.CrossRefGoogle ScholarPubMed
Roszkowski, A (2011) Technologie produkcji zwierzęcej a emisje gazów cieplarnianych. Problemy In΀ynierii Rolniczej [PL] 19, 83–97.Google Scholar
Salisbury, JG, Nicholls, TJ, Lammerding, AM, Turnidge, J and Nunn, MJA (2002) Risk analysis framework for the long-term management of antibiotic resistance in food-producing animals. International Journal of Antimicrobial Agents 20, 153–164.CrossRefGoogle ScholarPubMed
Salminen, S, Ouwehand, A and Isolauri, E (1998) Clinical applications of probiotic bacteria. International Dairy Journal 8, 563–572.CrossRefGoogle Scholar
Skopińska-Różewska, E and Siwicki, KA (2003) Rola Immunomodulatorów Pochodzenia Naturalnego w Zaobieganiu i Leczeniu Chorób. Wydawnictwo Medyk, 121–128.Google Scholar
Średnicka-Tober, D, Barański, M, Seal, C, Sanderson, R, Benbrook, C, Steinshamn, H, Gromadzka-Ostrowska, J, Rembiałkowska, E, Skwarło-Sońta, K, Eyre, M and Cozzi, G (2016) Composition differences between organic and conventional meat: a systematic literature review and meta-analysis. British Journal of Nutrition 115, 994–1011.CrossRefGoogle ScholarPubMed
Šuľák, M, Sikorová, L, Jankuvová, J, Javorský, P and Pristaš, P (2012) Variability of Actinobacteria, a minor component of rumen microflora. Folia Microbiologica 57, 351–353.CrossRefGoogle ScholarPubMed
Szulc, T (2012) Tajemnice Mleka. Wrocław: Wydawnictwo UPWr.Google Scholar
Takahashi, Y and Omura, S (2003) Isolation of new actinomycete strains for the screening of new bioactive compounds. The Journal of General And Applied Microbiology 49, 141–154.CrossRefGoogle ScholarPubMed
Tamate, H, McGilliard, AD, Jacobson, NL and Getty, R (1962) Effect of various dietaries on the anatomical development of the stomach in the calf. Journal of Dairy Science 45, 408–420.CrossRefGoogle Scholar
Van Gylswyk, NO and Van Der Toorn, JJTK (1987) Clostridium aerotolerans sp. nov., a xylanolytic bacterium from corn stover and from the rumina of sheep fed corn stover. International Journal of Systematic and Evolutionary Microbiology 37, 102–105.Google Scholar
Vďačný, P, Orsi, W, Bourland, WA, Shimano, S, Epstein, SS and Foissner, W (2011) Morphological and molecular phylogeny of dileptid and tracheliid ciliates: resolution at the base of the class Litostomatea (ciliophora, rhynchostomatia). Protistologica 47, 295–313.Google Scholar
von Engelhardt, W (2011) Physiologie der Haustiere, vol. 24. Germany: ENKE, pp. 40–41, 80–82.Google Scholar
Weinberg, ZG, Muck, RE, Weimer, PJ, Chen, Y and Gamburg, M (2004) Lactic acid bacteria used in inoculants for silage as probiotics for ruminants. Applied Biochemistry and Biotechnology 118, 1–9.CrossRefGoogle ScholarPubMed
Weng, X, Zhao, W, Neethirajan, S and Duffield, T (2015) Microfluidic biosensor for β-hydroxybutyrate (βHBA) determination of subclinical ketosis diagnosis. Journal of Nanobiotechnology 13, 13.CrossRefGoogle ScholarPubMed
Włodarczyk, R and Budvytis, M (2011) Właściwe żywienie krów wysoko wydajnych–jak w pełni wykorzystać ich potencjał produkcyjny. Życie Weterynaryjne 86, 771–776.Google Scholar
Wolin, MJ (1979) The rumen fermentation: A model for microbial interactions in anaerobic ecosystems. In Alexander, M (eds), Advances in Microbial Ecology 3. Boston, MA: Springer, pp. 49–77.CrossRefGoogle Scholar
Yáñez-Ruiz, DR, Abecia, L and Newbold, CJ (2015) Manipulating rumen microbiome and fermentation through interventions during early life: a review. Frontiers in Microbiolology 6, 1133.Google ScholarPubMed
Young, E (2016) Microbiom. Wydawnictwo Uniwersytetu Jagiellońskiego, pp. 235, 237–239, 245–246.Google Scholar
Zabielski, R (2006) The shell of a young child soars … that is to what extent the function of the gastrointestinal tract and human can depend on its development in the early postnatal period. Folia Universitatis Agriculturae Stetinensis Zootechnica 250, 7–16.Google Scholar
Zabielski, R (2007) Sterowanie Rozwojem Układu Pokarmowego u Nowo Narodzonych Ssaków. Państwowe Wydawnictwo Rolnicze i Leśne, p. 136–143.Google Scholar
Zawadzki, W (2008) Fizjologiczne Podstawy Żywienia Zwierząt. Wydawnictwo Uniwersytetu Przyrodniczego Wrocław, pp. 37–44.Google Scholar
Zhou, M, Chung, YH, Beauchemin, KA, Holtshausen, L, Oba, M, McAllister, TA and Guan, LL (2011) Relationship between rumen methanogens and methane production in dairy cows fed diets supplemented with a feed enzyme additive. Journal of Applied Microbiology 111, 1148–1158.CrossRefGoogle ScholarPubMed