Maria S Miroshnikova, Azamat E Arinzhanov
DOI: 10.33284/2658-3135-104-3-57
UDC 636.085:577.17
Acknowledgements:
The research was carried out with the support of the Russian Science Foundation project (No. 20-16-00088)
Rumen microbiocenosis is a tool for the construction of artificial biosystems. Ruminal bioreactor (review)
Maria S Miroshnikova1, Azamat E Arinzhanov2
1Federal Research Centre of Biological Systems and Agrotechnologies of the Russian Academy of Sciences (Orenburg, Russia)
2Orenburg State University (Orenburg, Russia)
Abstract. Attempts to manipulate the rumen microbiome of cattle to address global agricultural problems have continued for decades with limited success, largely due to a lack of detailed understanding of it and the lack of technologies for culturing most microorganisms outside the rumen. To create such an artificial biosystem as a bioreactor that imitates the work of the rumen of ruminants, we need knowledge about the composition of the rumen microbiome, the interactions of these microorganisms with each other, depending on various factors. This review examines studies on the increase in degradation of the rumen microbiome of plant fiber, developments on the creation of a rumen continuous fermenter (RCF) using artificial microbiome profiling through next generation sequencing (NGS).
Keywords: ruminants, rumen microbiome, fermentation of rumen microbiome, bioreactor, artificial biosystems.
References
- Abecia L, Waddams KE, Martínez-Fernandez G, Martín-García AI, Ramos-Morales E, Newbold CJ, Yáñez-Ruiz DR. An antimethanogenic nutritional intervention in early life of ruminants modifies ruminal colonization by Archaea. Archaea. 2014;2014:841463. doi: 10.1155/2014/841463
- Allesina S, Levine JM. A competitive network theory of species diversity. Proc Natl Acad Sci USA. 2011 A;108(14):5638-5642. doi: 10.1073/pnas.1014428108
- Bainbridge ML, Cersosimo LM, Wright AD, Kraft J. Rumen bacterial communities shift across a lactation in Holstein, Jersey and Holstein × Jersey dairy cows and correlate to rumen function, bacterial fatty acid composition and production parameters. FEMS Microbiol Ecol. 2016;92(5):fiw059. doi: 10.1093/femsec/fiw059
- Barnes SP, Keller J. Cellulosic waste degradation by rumen-enhanced anaerobic digestion. Water Sci Technol. 2003;48(4):155-162.
- Belanche A, Jones E, Parveen I, Newbold CJ. A metagenomics approach to evaluate the impact of dietary supplementation with Ascophyllum nodosum or Laminaria digitata on rumen function in rusitec fermenters. Front Microbiol. 2016a; 7:299. doi: 10.3389/fmicb.2016.00299
- Belanche A, Kingston-Smith AH, Newbold CJ. An integrated multi-omics approach reveals the effects of supplementing grass or grass hay with vitamin E on the rumen microbiome and its function. Front Microbiol. 2016b; 7:905. doi: 10.3389/fmicb.2016.00905
- Belanche A, Pinloche E, Preskett D, Newbold CJ. Effects and mode of action of chitosan and ivy fruit saponins on the microbiome, fermentation and methanogenesis in the rumen simulation technique. FEMS Microbiol Ecol. 2016с; 92(1):fiv160. doi: 10.1093/femsec/fiv160
- Bernalier A, Fonty G, Bonnemoy F, Gouet P. Inhibition of the cellulolytic activity of Neocallimastix frontalis by Ruminococcus flavefaciens. J Gen Microbiol. 1993;139(4):873-880. doi: 10.1099/00221287-139-4-873
- Bickhart DM, Weimer PJ. Symposium review: Host-rumen microbe interactions may be leveraged to improve the productivity of dairy cows. J Dairy Sci. 2018;101(8):7680-7689. doi: 10.3168/jds.2017-13328
- Blasig JD, Holtzapple MT, Dale BE, Engler CR, Byers FM. Volatile fatty acid fermentation of AFEX-treated bagasse and newspaper by rumen microorganisms. Resour. Conserv. Recy. 1992;7(1-3):95-114. doi: https://doi.org/10.1016/0921-3449(92)90009-Q
- Cardozo PW, Calsamiglia S, Ferret A, Kamel C. Effects of natural plant extracts on ruminal protein degradation and fermentation profiles in continuous culture. J Anim Sci. 2004;82(11):3230-3236. doi: 10.2527/2004.82113230x
- Chalupa W. Manipulating rumen fermentation. J Anim Sci. 1977;45(3):585-599. doi: https://doi.org/10.2527/jas1977.453585x
- Chan WW, Dehority BA. Production of Ruminococcus flavefaciensgrowth inhibitor(s) by Ruminococcus albus. Anim Feed Sci Technol. 1999;77(1-2):61-71. doi: https://doi.org/10.1016/S0377-8401(98)00234-X
- Chen J, Weimer PJ. Competition among three predominant ruminal cellulolytic bacteria in the absence or presence of non-cellulolytic bacteria. Microbiology. 2001; 147(1):21-30. doi: 10.1099/00221287-147-1-21
- Chiquette J, Talbot G, Markwell F, Nili N, Forster RJ. Repeated ruminal dosing of Ruminococcus flavefaciens NJ along with a probiotic mixture in forage or concentrate-fed dairy cows: effect on ruminal fermentation, cellulolytic populations and in sacco digestibility. Can J Anim Sci. 2007;87(2):237-249. doi: https://doi.org/10.4141/A06-066
- Colombatto D, Morgavi DP, Furtado AF, Beauchemin KA. Screening of exogenous enzymes for ruminant diets: relationship between biochemical characteristics and in vitro ruminal degradation. J Anim Sci. 2003;81(10):2628-2638. doi: 10.2527/2003.81102628x
- Czerkawski JW, Breckenridge G. Design and development of a long-term rumen simulation technique (Rusitec). Br J Nutr. 1977;38(3):371-384. doi: 10.1079/bjn19770102
- Duarte AC, Holman DB, Alexander TW, Durmic Z, Vercoe PE, Chaves AV. The type of forage substrate preparation included as substrate in a RUSITEC system affects the ruminal microbiota and fermentation characteristics. Front Microbiol. 2017;8:704. doi: 10.3389/fmicb.2017.00704
- Ertl P, Knaus W, Metzler-Zebeli BU, Klevenhusen F, Khiaosa-Ard R, Zebeli Q. Substitution of common concentrates with by-products modulated ruminal fermentation, nutrient degradation, and microbial community composition in vitro. J Dairy Sci. 2015; 98(7):4762-4771. doi: 10.3168/jds.2014-9063
- Flachowsky G. Rumen Microbiology: Burk A Dehority (Ed.), Nottingham University Press, Nottingham, NG11 OAX, UK, 2003, Hardcover, ISBN 1-897676-99-9, £ 40, 372 pp. Animal Feed Science and Technology. 2004;113(1-4):253-254. doi: 10.1016/J.ANIFEEDSCI.2003.09.002
- Flint HJ, Bayer EA, Rincon MT, Lamed R, White BA. Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nature Reviews Microbiology. 2008;6(2):121-131. doi: 10.1038/nrmicro1817
- Flint HJ, Bisset J, Webb J. Use of antibiotic resistance mutations to track strains of obligately anaerobic bacteria introduced into the rumen of sheep. J Appl Bacteriol. 1989;67(2):177-183. doi: 10.1111/j.1365-2672.1989.tb03393.x
- Fonty G, Gouet P, Ratefiarivelo H, Jouany JP. Establishment of Bacteroides succinogenes and measurement of the main digestive parameters in the rumen of gnotoxenic lambs. Can J Microbiol. 1988;34(8):938-946. doi: 10.1139/m88-166
- Gijzen HJ, Lubberding HJ, Verhagen FJ, Zwart KB, Vogels GD. Application of rumen microorganisms for an enhanced anaerobic degradation of solid organic waste materials. Biol. Waste. 1987;22(2):81-95. doi: https://doi.org/10.1016/0269-7483(87)90041-3
- Giraldo LA, Ranilla MJ, Tejido ML, Carro MD. Influence of exogenous fibrolytic enzymes and fumarate on methane production, microbial growth and fermentation in Rusitec fermenters. Br J Nutr. 2007;98(4):753-761. doi: 10.1017/S0007114507744446
- Gregg K, Hamdorf B, Henderson K, Kopecny J, Wong C. Genetically modified ruminal bacteria protect sheep from fluoroacetate poisoning. Appl Environ Microbiol. 1998;64(9):3496-3498. doi: 10.1128/AEM.64.9.3496-3498.1998
- Guzman CE, Bereza-Malcolm LT, De Groef B, Franks AE. Presence of selected methanogens, fibrolytic bacteria, and proteobacteria in the gastrointestinal tract of neonatal dairy calves from birth to 72 hours. PLoS One. 2015;10(7):e0133048. doi: 10.1371/journal.pone.0133048
- Hammond AC. Leucaena toxicosis and its control in ruminants. J Anim Sci. 1995;73(5):1487-1492. doi: 10.2527/1995.7351487x
- Hobson PN, Stewart CS, eds. The Rumen Microbial Ecosystem. Netherlands: Springer Science & Business Media; 1997: 719 p. doi: 10.1007/978-94-009-1453-7
- Hoover WH, Crooker BA, Sniffen CJ. Effects of differential solid-liquid removal rates on fermentation parameters in continuous cultures of rumen contents. J Anim. Sci. 1976;43(2):528-534. doi: https://doi.org/10.2527/jas1976.432528x
- Hristov AN, Lee C, Hristova R, Huhtanen P, Firkins JL. A meta-analysis of variability in continuous-culture ruminal fermentation and digestibility data. J Dairy Sci. 2012 Sep;95(9):5299-5307. doi: 10.3168/jds.2012-5533. PMID: 22916935.
- Jami E, Israel A, Kotser A, Mizrahi I. Exploring the bovine rumen bacterial community from birth to adulthood. ISME J. 2013;7(6):1069-1079. doi: 10.1038/ismej.2013.2
- Jenkins TC, Bridges WC, Harrison JH, Young KM. Addition of potassium carbonate to continuous cultures of mixed ruminal bacteria shifts volatile fatty acids and daily production of biohydrogenation intermediates. J Dairy Sci. 2014; 97(2):975-984. doi: 10.3168/jds.2013-7164
- Jin D, Zhao S, Wang P, Zheng N, Bu D, Beckers Y, Wang J. Insights into abundant rumen ureolytic bacterial community using rumen simulation system. Front Microbiol. 2016;7:1006. doi: 10.3389/fmicb.2016.01006
- Jouany JP, Mathieu F, Senaud J, Bohatier J, Bertin G, Mercier M. The effect of Saccharomyces cerevisiae and Aspergillus oryzae on the digestion of the cell wall fraction of a mixed diet in defaunated and refaunated sheep rumen. Reprod Nutr Dev. 1998;38(4):401-416. doi: 10.1051/rnd:19980405
- Kalmokoff ML, Teather RM. Isolation and characterization of a bacteriocin (Butyrivibriocin AR10) from the ruminal anaerobe Butyrivibrio fibrisolvens AR10: evidence in support of the widespread occurrence of bacteriocin-like activity among ruminal isolates of B. fibrisolvens. Appl Environ Microbiol. 1997;63(2):394-402. doi: 10.1128/aem.63.2.394-402.1997
- Kong Y, Teather R, Forster R. Composition, spatial distribution, and diversity of the bacterial communities in the rumen of cows fed different forages. FEMS Microbiol Ecol. 2010;74(3):612-622. doi: 10.1111/j.1574-6941.2010.00977.x
- Krause DO, Bunch RJ, Conlan LL, Kennedy PM, Smith WJ, Mackie RI, McSweeney CS. Repeated ruminal dosing of Ruminococcus spp. does not result in persistence, but changes in other microbial populations occur that can be measured with quantitative 16S-rRNA-based probes. Microbiology. 2001;147(7):1719-1729. doi: 10.1099/00221287-147-7-1719
- Krause DO, Bunch RJ, Smith WJM, McSweeney CS. Diversity of Ruminococcus strains: a survey of genetic polymorphisms and plant digestibility. J Appl Microbiol. 1999a;86(3):487-495.
- Krause DO, Denman SE, Mackie RI, Morrison M, Rae AL, Attwood GT, McSweeney CS. Opportunities to improve fiber degradation in the rumen: microbiology, ecology, and genomics. FEMS Microbiology Reviews. 2003;27(5):663-693. doi: https://doi.org/10.1016/S0168-6445(03)00072-X
- Krause DO, Smith WJM, Ryan FME, Mackie RI, McSweeney CS. Use of 16S-rRNA based techniques to investigate the ecological succession of microbial populations in the immature lamb rumen: tracking of a specific strain of inoculated Ruminococcus and Interactions with other microbial populations in vivo. Microb Ecol. 1999b;38(4):365-376. doi: 10.1007/s002489901006
- Lengowski MB, Zuber KH, Witzig M, Mohring J, Boguhn J, Rodehutscord M. Changes in rumen microbial community composition during adaption to an in-vitro system and the impact of different forages. PLoS One. 2016;11(2):e0150115. doi: https://doi.org/10.1371/journal.pone.0150115
- Martínez ME, Ranilla MJ, Tejido ML, Ramos S, Carro MD. Comparison of fermentation of diets of variable composition and microbial populations in the rumen of sheep and Rusitec fermenters. I. Digestibility, fermentation parameters, and microbial growth. J Dairy Sci. 2010a; 93(8):3684-3698. doi: 10.3168/jds.2009-2933
- Martínez ME, Ranilla MJ, Tejido ML, Saro C, Carro MD. Comparison of fermentation of diets of variable composition and microbial populations in the rumen of sheep and Rusitec fermenters. II. Protozoa population and diversity of bacterial communities. J Dairy Sci. 2010b;93(8):3699-3712. doi: 10.3168/jds.2009-2934
- Matthews C, Crispie F, Lewis E, Reid M, O'Toole PW, Cotter PD. The rumen microbiome: a crucial consideration when optimising milk and meat production and nitrogen utilisation efficiency. Gut Microbes. 2019;10(2):115-132. doi: 10.1080/19490976.2018.1505176
- Menke K, Raab L, Salewski A, Steingass H, Fritz D, Schneider W. The estimation of the digestibility and metabolizable energy content of ruminant feedingstuffs from the gas production when they are incubated with rumen liquor in The Journal of Agricultural Science. 1979;93(1):217-222. doi: 10.1017/S0021859600086305
- Menke KH, Steingass H. Estimation of the energetic feed value obtained from chemical analysis and in vitro gas production using rumen fluid. Anim Res Dev. 1988;28:7-55.
- Mosoni P, Fonty G, Gouet P. Competition between ruminal cellulolytic bacteria for adhesion to cellulose. Curr Microbiol. 1997;35(1):44-47. doi: 10.1007/s002849900209
- Muetzel S, Lawrence P, Hoffmann EM, Becker K. Evaluation of a stratified continuous rumen incubation system. Anim Feed Sci Tech. 2009;151(1-2): 32-43. doi: 10.1016/j.anifeedsci.2008.11.001
- O'Sullivan CA, Burrell PC. The effect of media changes on the rate of cellulose solubilisation by rumen and digester derived microbial communities. Waste Manag. 2007;27(12):1808-1814. doi: 10.1016/j.wasman.2006.10.010
- Poulsen M, Schwab C, Jensen BB, Engberg RM, Spang A, Canibe N, Højberg O, Milinovich G, Fragner L, Schleper C, Weckwerth W, Lund P, Schramm A, Urich T. Methylotrophic methanogenic Thermoplasmata implicated in reduced methane emissions from bovine rumen. Nat Commun. 2013;4:1428. doi: 10.1038/ncomms2432
- Præsteng KE, Pope PB, Cann IK, Mackie RI, Mathiesen SD, Folkow LP, Eijsink VG, Sundset MA. Probiotic dosing of Ruminococcus flavefaciens affects rumen microbiome structure and function in reindeer. Microb Ecol. 2013;66(4):840-849. doi: 10.1007/s00248-013-0279-z
- Prevot S, Senaud J, Bohatier J, Prensier G. Variation in the composition of the ruminal bacterial microflora during the adaptation phase in an artificial fermenter (RUSITEC). Zool Sci. 1994;11(6):871-882.
- Puniya AK, Salem AZM, Kumar S, et al. Role of live microbial feed supplements with reference to anaerobic fungi in ruminant productivity: a review. J Integr Agric. 2015;14(3):550-560. doi: 10.1016/S2095-3119(14)60837-6
- Roehe R, Dewhurst RJ, Duthie C-A, Rooke JA, McKain N, Ross DW, et al. Bovine Host genetic variation influences rumen microbial methane production with best selection criterion for low methane emitting and efficiently feed converting hosts based on metagenomic gene abundance. PLoS Genet. 2016;12(2):e1005846. doi: https://doi.org/10.1371/journal.pgen.1005846
- Roger V, Fonty G, Komisarczuk-Bony S, Gouet P. Effects of physicochemical factors on the adhesion to cellulose avicel of the ruminal bacteria Ruminococcus flavefaciens and Fibrobacter succinogenes subsp. succinogenes. Appl Environ Microbiol. 1990;56(10):3081-3087. doi: 10.1128/aem.56.10.3081-3087.1990
- Santschi DE, Berthiaume R, Matte JJ, Mustafa AF, Girard CL. Fate of supplementary B-vitamins in the gastrointestinal tract of dairy cows. J Dairy Sci. 2005;88(6):2043-2054. doi: 10.3168/jds.S0022-0302(05)72881-2
- Schofield P, Pell AN. Measurement and kinetic analysis of the neutral detergent-soluble carbohydrate fraction of legumes and grasses. J Anim Sci. 1995;73(11):3455-3463. doi: 10.2527/1995.73113455x
- Shi Y, Odt CL, Weimer PJ. Competition for cellulose among three predominant ruminal cellulolytic bacteria under substrate-excess and substrate-limited conditions. Appl Environ Microbiol. 1997;63(2):734-742. doi:10.1128/aem.63.2.734-742.1997
- Shinkai T, Kobayashi Y. Localization of ruminal cellulolytic bacteria on plant fibrous materials as determined by fluorescence in situ hybridization and real-time PCR. Appl Environ Microbiol. 2007;73(5):1646-1652. doi: 10.1128/AEM.01896-06
- Shinkai T, Ueki T, Kobayashi Y. Detection and identification of rumen bacteria constituting a fibrolytic consortium dominated by Fibrobacter succinogenes. Anim Sci J. 2010;81(1):72-79. doi: 10.1111/j.1740-0929.2009.00698.x
- Soto EC, Molina-Alcaide E, Khelil H, Yáñez-Ruiz DR. Ruminal microbiota developing in different in vitro simulation systems inoculated with goats’ rumen liquor. Anim. Feed Sci. Technol. 2013;185(1-2):9-18. doi: https://doi.org/10.1016/j.anifeedsci.2013.06.003
- Soto EC, Yánez-Ruiz DR, Cantalapiedra-Hijar G, Vivas A, Molina-Alcaide E. Changes in ruminal microbiota due to rumen content processing and incubation in single-flow continuous culture fermenters. Anim. Prod. Sci. 2012;52(9):813-822. doi: 10.1071/AN11312
- Theodorou MK, Williams BA, Dhanoa MS, McAllan AB. A new laboratory procedure for estimating kinetic parameters associated with the digestibility of forages. In: Proceedings of the International Symposium on Forage Cell Wall Structure and Digestibility, USD-ARS; Madison, WI, USA. 7-10 October 1991.
- Walter J, Maldonado-Gómez MX, Martínez I. To engraft or not to engraft: an ecological framework for gut microbiome modulation with live microbes. Curr Opin Biotechnol. 2018;49:129-139. doi: 10.1016/j.copbio.2017.08.008
- Weimer PJ, Cox MS, Vieira de Paula T, Lin M, Hall MB, Suen G. Transient changes in milk production efficiency and bacterial community composition resulting from near-total exchange of ruminal contents between high- and low-efficiency Holstein cows. J Dairy Sci. 2017;100(9):7165-7182. doi: 10.3168/jds.2017-12746
- Weimer PJ. Redundancy, resilience, and host specificity of the ruminal microbiota: implications for engineering improved ruminal fermentations. Front Microbiol. 2015;6:296. doi: 10.3389/fmicb.2015.00296
- Yáñez-Ruiz DR, Abecia L, Newbold CJ. Manipulating rumen microbiome and fermentation through interventions during early life: a review. Front Microbiol. 2015;6:1133. doi: 10.3389/fmicb.2015.01133
- Yue ZB, Li WW, Yu HQ. Application of rumen microorganisms for anaerobic bioconversion of lignocellulosic biomass. Bioresour Technol. 2013;128:738-7 doi: 10.1016/j.biortech.2012.11.073
- Zhou M, Peng YJ, Chen Y, Klinger CM, Oba M, Liu JX, Guan LL. Assessment of microbiome changes after rumen transfaunation: implications on improving feed efficiency in beef cattle. Microbiome. 2018;6(1):62. doi: 10.1186/s40168-018-0447-y
- Ziemer CJ, Sharp R, Stern MD, Cotta MA, Whitehead TR, Stahl DA. Comparison of microbial populations in model and natural rumens using 16S ribosomal RNA-targeted probes. Environ Microbiol. 2000;2(6):632-6 doi: 10.1046/j.1462-2920.2000.00146.x
Miroshnikova Maria Sergeevna, Research Laboratory Assistant, Federal Research Centre of Biological Systems and Agrotechnologies of the Russian Academy of Sciences, 460000, Orenburg, Russia, 29, 9 Yanvarya St., сот.: 8-922-867-57-10, e-mail: marymiroshnikova@mail.ru
Arinzhanov Azamat Ersainovich, Cand. Sci. (Biol.), Associate Professor of the Department of Biotechnology of Animal Raw Materials and Aquaculture, Orenburg State University, 460018, Orenburg, Russia, 13 Pobedy Ave., e-mail: arin.azamat@mail.ru
Received: 16 August 2021; Accepted: 13 September 2021; Published: 30 September 2021
Download