Abstract
The overarching objective of this review is to compare methanogenesis in ruminant gut systems and industrial digesters that employ plants, crops and their processing residues or by-products as feedstocks. An important consideration is the presence of phytochemicals in these feedstocks, with the understanding that depending on the type and quantities, these phytochemicals affect the activity of biomass degrading microorganisms to varying extents. This review aims to evaluate currently available knowledge on the effects of phytochemicals in ruminants’ methanogenesis as well as industrial anaerobic digestion processes. Technology and scale up in industrial fermentation have always benefited from our understanding of natural biological processes as such, knowledge from the process of methanogenesis in the gastrointestinal tract of ruminants can be used to make inferences about the performance of industrial digester systems for biogas production. This is particularly important when the same feedstock is used in both systems. Thus, in this review, comparisons of the two methane generating systems are discussed with an emphasis on phytochemical inhibitory effects on microorganisms that are involved in anaerobic digestion.
Similar content being viewed by others
References
Abad P, Arroyo-Manzanares N, Gil L, García-Campaña AM (2016) Use of onion extract as dairy cattle feed supplement: monitoring of propyl propane thiosulphate as marker of its effect on milk attributes. J Agric Food Chem. https://doi.org/10.1021/acs.jafc.6b04395
Abendroth C, Simeonov C, Peretó J et al (2017) From grass to gas: microbiome dynamics of grass biomass acidification under mesophilic and thermophilic temperatures. Biotechnol Biofuels 10:1–12. https://doi.org/10.1186/s13068-017-0859-0
Abioye EO, Akinpelu DA, Aiyegoro OA et al (2013) Preliminary phytochemical screening and antibacterial properties of crude stem bark extracts and fractions of Parkia biglobosa (Jacq.). Molecules 8:8485–8499. https://doi.org/10.3390/molecules18078485
Adeleke BS, Babalola OO (2020) Oilseed crop sunflower (Helianthus annuus) as a source of food: nutritional and health benefits. Food Sci Nutr 8:4666–4684. https://doi.org/10.1002/fsn3.1783
Akanmu AM, Hassen A, Adejoro FA (2020) Gas production, digestibility and efficacy of stored or fresh plant extracts to reduce methane production on different substrates. Animals 10:4–6. https://doi.org/10.3390/ani10010146
Altemimi A, Lakhssassi N, Baharlouei A, Watson DG (2017) Phytochemicals: extraction, isolation and identification of bioactive compounds from plant extracts. Plants 6:1–23. https://doi.org/10.3390/plants6040042
Andreas OW, Reitschuler C, Illmer P (2014) Effect of different acetate:propionate ratios on the methanogenic community during thermophilic anaerobic digestion in batch experiments. Biochem Eng J. https://doi.org/10.1016/j.bej.2014.05.014
Appels L, Baeyens J, Degrève J, Dewil R (2008) Principles and potential of the anaerobic digestion of waste-activated sludge. Prog Energy Combust Sci 34:755–781. https://doi.org/10.1016/j.pecs.2008.06.002
Asam Z, Poulsen TG, Nizami A et al (2011) How can we improve biomethane production per unit of feedstock in biogas plants? Appl Energy 88:2013–2018. https://doi.org/10.1016/j.apenergy.2010.12.036
Ayo JO, Oladele SB, Ngam S et al (1998) Diurnal fluctuations in rectal temperature of the Red Sokoto goat during the harmattan season. Res Vet Sci 66:7–9. https://doi.org/10.1053/rvsc.1998.0231
Balcells J, Aris A, Serrano A et al (2012) Effects of an extract of plant flavonoids (Bioflavex) on rumen fermentation and performance in heifers fed high-concentrate diets. J Anim Sci 90:4975–4984. https://doi.org/10.2527/jas2011-4955
Baruah L, Malik PK, Kolte AP et al (2019) Rumen methane amelioration in sheep using two selected tanniferous phyto-leaves. Carbon Manag. https://doi.org/10.1080/17583004.2019.1605480
Bayané A, Guiot SR (2011) Animal digestive strategies versus anaerobic digestion bioprocesses for biogas production from lignocellulosic biomass. Rev Environ Sci Biotechnol 10:43–62. https://doi.org/10.1007/s11157-010-9209-4
Benchaar C, Greathead H (2011) Essential oils and opportunities to mitigate enteric methane emissions from ruminants. Anim Feed Sci Technol 167:338–355. https://doi.org/10.1016/j.anifeedsci.2011.04.024
Benchaar C, Hassanat F, Gervais R et al (2014) Methane production, digestion, ruminal fermentation, nitrogen balance, and milk production of cows fed corn silage- or barley silage-based diets. J Dairy Sci 97:961–974. https://doi.org/10.3168/jds.2013-7122
Bergmann GT (2017) Microbial community composition along the digestive tract in forage- and grain-fed bison. BMC Vet Res 13:1–9. https://doi.org/10.1186/s12917-017-1161-x
Bernard L, Shingfield KJ, Rouel J et al (2009) Effect of plant oils in the diet on performance and milk fatty acid composition in goats fed diets based on grass hay or maize silage. Br J Nutr 101:213–224. https://doi.org/10.1017/S0007114508006533
Bhatt RS, Sahoo A, Soni LK, Sharma P (2019) Methane emission, nutrient utilization, microbial protein synthesis and growth performance in finisher lambs fed complete feed blocks containing phytochemical-rich forages of semi-arid region. Carbon Manag 3004:1–11. https://doi.org/10.1080/17583004.2019.1706143
Bhatta R, Uyeno Y, Tajima K et al (2009) Difference in the nature of tannins on in vitro ruminal methane and volatile fatty acid production and on methanogenic archaea and protozoal populations. J Dairy Sci. https://doi.org/10.3168/jds.2008-1441
Bird SH, Hegarty RS, Woodgate R (2008) Persistence of defaunation effects on digestion and methane production in ewes. Aust J Exp Agric 48:152–155. https://doi.org/10.1071/EA07298
Bobeica V, Covaliov V, Nenno V, Covaliova O (2015) Phytochemical compounds and plant products that stimulate methanogenic processes of anaerobic fermentation by microorganisms. In: INCD ECOIND-international symposium—SIMI 2015. The Environment and the Industry, pp 57–65
Bodas R, Prieto N, Garcia-Gonzalez R et al (2012) Manipulation of rumen fermentation and methane production with plant secondary metabolites. Anim Feed Sci Technol 176:78–93. https://doi.org/10.1016/j.anifeedsci.2012.07.010
Bovina S, Frascari D, Ragini A, Avolio F (2020) Development of a continuous-flow anaerobic co-digestion process of olive mill wastewater and municipal sewage sludge. J Chem Technol Biotechnol. https://doi.org/10.1002/jctb.6570
Brielmann HL, Setzer WN, Kaufman PB et al (2006) Phytochemicals: the chemical components of plants. In: Cseke JL, Kirakosyan A, Kaufman BP et al (eds) Natural products from plants, 2nd edn. Taylor & Francis, London, pp 1–50
Buhse HE, Suzanne MM, John CC, Ping S (2011) Vorticella. In: eLS. Wiley, Chichester
Burt S (2004) Essential oils: heir antibacterial properties and potential applications in foods—a review. Int J Food Microbiol 94:223–253. https://doi.org/10.1016/j.ijfoodmicro.2004.03.022
Calabrò PS, Pontoni L, Porqueddu I et al (2016) Effect of the concentration of essential oil on orange peel waste biomethanization: preliminary batch results. Waste Manag 48:440–447. https://doi.org/10.1016/j.wasman.2015.10.032
Calsamiglia S, Busquet M, Cardozo PW et al (2007) Invited review: essential oils as modifiers of rumen microbial fermentation. J Dairy Sci 90:2580–2595. https://doi.org/10.3168/jds.2006-644
Cansunar E, Richardson AJ, Wallace G, Stewart CS (1990) Effect of coumarin on glucose uptake by anaerobic rumen fungi in the presence and absence of Methanobrevibacter smithii. FEMS Microbiol Lett 70(2):157–160. https://doi.org/10.1016/S0378-1097(05)80031-X
Castillo-González AR, Burrola-Barraza ME, Domínguez-Viveros J, Chávez-Martínez A (2014) Rumen microorganisms and fermentation. Arch Med Vet 46:349–361
Cerrato-Sanchez M, Calsamiglia S, Ferret A (2004) Effect of the magnitude of the decrease of rumen pH on rumen fermentation in a dual-flow continuous culture system. J Anim Sci 86:378–383. https://doi.org/10.2527/jas.2007-0180
Cerrilla MEO, Martínez GM (2003) Starch digestion and glucose metabolism in the ruminant: a review. Interciencia 28:380-386+426
Chanakya HN, Malayil S (2012) Anaerobic digestion for bioenergy from agro-residues and other solid wastes—an overview of science, technology and sustainability. J Indian Inst Sci 92:111–143
Chandramoni C, Jadhao S, Tiwad C et al (2001) Energy metabolism and methane production in faunated and defaunated sheep fed two diets with same concentrate to roughage ratio (70:30) but varying in composition. Asian Australas J Anim Sci 14:1238–1244
Chaudhary P, Sharma A, Singh B, Nagpal AK (2018) Bioactivities of phytochemicals present in tomato. J Food Sci Technol 55:2833–2849. https://doi.org/10.1007/s13197-018-3221-z
Chen Y, Cheng JJ, Creamer KS (2008) Inhibition of anaerobic digestion process: a review. Bioresour Technol 99:4044–4064. https://doi.org/10.1016/j.biortech.2007.01.057
Cheok CY, Mohd Adzahan N, Abdul Rahman R et al (2018) Current trends of tropical fruit waste utilization. Crit Rev Food Sci Nutr 58:335–361. https://doi.org/10.1080/10408398.2016.1176009
Cieslak A, Stochmal A, Oleszek W (2013a) Plant components with specific activities against rumen methanogens. Animal. https://doi.org/10.1017/S1751731113000852
Cieslak A, Szumacher-Strabel M, Stochmal A, Oleszek W (2013b) Plant components with specific activities against rumen methanogens. Animal 7(Suppl 2):253–265. https://doi.org/10.1017/S1751731113000852
Correddu F, Lunesu MF, Buffa G et al (2020) Can agro-industrial by-products rich in polyphenols be advantageously used in the feeding and nutrition of dairy small ruminants? Animals 10:1–25. https://doi.org/10.3390/ani10010131
Croce S, Wei Q, Dong R et al (2016) Anaerobic digestion of straw and corn stover: the effect of biological process optimization and pre-treatment on total bio-methane yield and energy performance. Biotechnol Adv. https://doi.org/10.1016/j.biotechadv.2016.09.004
Cubero-Cardoso J, Trujillo-Reyes Á, Serrano A et al (2020) High-value-added compound recoverey with high-temperature hydrothermal treatment and steam explosion, and subsequent biomethanization of residual strawberry extrudate. Foods 9:1–16. https://doi.org/10.3390/foods9081082
De Barros IB, Feijó J, Daniel DS, Pinto JP (2011) Phytochemical and antifungal activity of anthraquinones and root and leaf extracts of Coccoloba mollis on phytopathogens. Brazilian Arch Biol Technol 54:535–541. https://doi.org/10.1590/S1516-89132011000300015
Dehority BA (2002) Gastrointestinal tracts of herbivores, particularly the ruminant: anatomy, physiology and microbial digestion of plants. J Appl Anim Res 21:145–160. https://doi.org/10.1080/09712119.2002.9706367
Demirel B, Scherer P (2008) The roles of acetotrophic and hydrogenotrophic methanogens during anaerobic conversion of biomass to methane: a review. Rev Environ Sci Bio/Technology 7:173–190. https://doi.org/10.1007/s11157-008-9131-1
Dentinho MTP, Bessa RJB (2016) Effect of tannin source and pH on stability of tannin-protein and fibre complexes. Rev Agrar 39:114–121. https://doi.org/10.19084/RCA15062
Dhanasekaran DK, Dias-Silva TP, Filho ALA et al (2020) Plants extract and bioactive compounds on rumen methanogenesis. Agrofor Syst 94:1541–1553. https://doi.org/10.1007/s10457-019-00411-6
Fantozzi F, Buratti C (2009) Biogas production from different substrates in an experimental continuously stirred tank reactor anaerobic digester. Bioresour Technol 100:5783–5789. https://doi.org/10.1016/j.biortech.2009.06.013
Farnsworth RN (1966) Biological and phytochemical screening of plants. J Pharm Sci 55:255–276. https://doi.org/10.1126/science.151.3712.874
Ferguson RMW, Coulon F, Villa R (2016) Organic loading rate: a promising microbial management tool in anaerobic digestion. Water Res 100:348–356. https://doi.org/10.1016/j.watres.2016.05.009
Fink-Gremmels J (2010) Defense mechanisms against toxic phytochemicals in the diet of domestic animals. Mol Nutr Food Res 54:249–258. https://doi.org/10.1002/mnfr.200900361
Firkins JL, Yu Z (2006) Characterisation and quantification of the microbial populations of the rumen. In: Sejrsen K, Hvelplund T, Nielsen MO (eds) Ruminant physiology: digestion, metabolism and impact of nutrition on gene expression, immunology and stress. Wageningen Academic Publishers, Wageningen, pp 19–54
Fredotovic Z, Soldo B, Šprung M et al (2020) Comparison of organosulfur and amino acid composition between triploid onion Allium cornutum Clementi ex Visiani, 1842, and common onion Allium cepa L., and evidences for antiproliferative activity of their extracts. Plants 9:1–16. https://doi.org/10.3390/plants9010098
Gebashe F, Aremu AO, Van Staden J et al (2020) Phytochemical profiles and antioxidant activity of grasses used in South African traditional medicine. Plants 9:1–23. https://doi.org/10.3390/plants9030371
Gebhardt R, Beck H (1996) Differential inhibitory effects of garlic-derived organosulfur compounds on cholesterol biosynthesis in primary rat hepatocyte cultures. Lipids 31:1269–1276
Greiner R, Konietzny U (2006) Phytase for food application. Food Technol Biotechnol 44(2):125–140
Guimaraes CA, Meireles LM, Lemos MF et al (2019) Antibacterial activity of terpenes and terpenoids present in essential oils. Molecules 24:1–12. https://doi.org/10.3390/molecules24132471
Günal M, Pinski B, AbuGhazaleh AA (2017) Evaluating the effects of essential oils on methane production and fermentation under in vitro conditions. Ital J Anim Sci 16:500–506. https://doi.org/10.1080/1828051X.2017.1291283
Gunjan G, Puniya AK, Aguilar CN, Singh K (2005) Interaction of gut microflora with tannins in feeds. Naturwissenschaften 92:497–503. https://doi.org/10.1007/s00114-005-0040-7
Hamadani A, Ganai NA, Shanaz S et al (2018) Usage of phytochemicals in veterinary practice. J Entomol Zool Stud 6:1997–2000
Han X, Yang Y, Yan H et al (2015) Rumen bacterial diversity of 80 to 110-day-old goats using 16s rRNA sequencing. PLoS ONE. https://doi.org/10.1371/journal.pone.0117811
Hee-Soon H, Dong-Uk H, Su-Kyoung L et al (2013) Effects of terpenoids-rich plant extracts on ruminal-fermentation and methane production. Korean J Org Agric 21:629–646. https://doi.org/10.11625/KJOA.2013.21.4.629
Henderson G, Cox F, Ganesh S et al (2015) Rumen microbial community composition varies with diet and host, but a core microbiome is found across a wide geographical range. Sci Rep. https://doi.org/10.1038/srep14567
Herrero N, Mattioli A, Gil A et al (2019) Evaluation of the methane potential of different agricultural and food processing substrates for improved biogas production in rural areas. Renew Sustain Energy Rev 112:1–10. https://doi.org/10.1016/j.rser.2019.05.040
Hęś M, Dziedzic K, Górecka D et al (2019) Aloe vera (L.) Webb.: natural sources of antioxidants—a review. Plant Foods Hum Nutr 74:255–265. https://doi.org/10.1007/s11130-019-00747-5
Hook SE, Wright ADG, McBride BW (2010) Methanogens: methane producers of the rumen and mitigation strategies. Archaea 2010:50–60. https://doi.org/10.1155/2010/945785
Hu Y, Shen Y, Wu X et al (2018) Synthesis and biological evaluation of coumarin derivatives containing imidazole skeleton as potential antibacterial agents. Eur J Med Chem 143:958–969. https://doi.org/10.1016/j.ejmech.2017.11.100
Huang X, Yun S, Zhu J et al (2016) Mesophilic anaerobic co-digestion of aloe peel waste with dairy manure in the batch digester: focusing on mixing ratios and digestate stability. Bioresour Technol 218:62–68. https://doi.org/10.1016/j.biortech.2016.06.070
Humer E, Zebeli Q (2015) Phytate in feed ingredients and potentials for improving the utilization of phosphorus in ruminant nutrition. Anim Feed Sci Technol 209:1–15. https://doi.org/10.1016/j.anifeedsci.2015.07.028
Irem G, Sarıkaya B, Ali M et al (2011) Antiprotozoal alkaloids from Galanthus trojanus. Phytochem Lett 4:301–305. https://doi.org/10.1016/j.phytol.2011.05.008
Janssen PH, Kirs M (2008) Structure of the archaeal community of the rumen. Appl Environ Microbiol 74:3619–3625. https://doi.org/10.1128/AEM.02812-07
Jarvis NG, Strompl C, Burgess MD et al (2000) Isolation and identification of ruminal methanogens from grazing cattle. Curr Microbiol 40:327–332. https://doi.org/10.1007/s002849910065
Jayanegara A, Leiber F, Kreuzer M (2012) Meta-analysis of the relationship between dietary tannin level and methane formation in ruminants from in vivo and in vitro experiments. J Anim Physiol Anim Nutr 96:365–375. https://doi.org/10.1111/j.1439-0396.2011.01172.x
Jayanegara A, Wina E, Takahashi J (2014) Meta-analysis on methane mitigating properties of saponin-rich sources in the rumen: influence of addition levels and plant sources. Asian-Australas J Anim Sci 27:1426–1435. https://doi.org/10.5713/ajas.2014.14086
Jayanegara A, Gunjan G, Harinder PSM, Klaus B (2015) Divergence between purified hydrolysable and condensed tannin effects on methane emission, rumen fermentation and microbial population in vitro. Anim Feed Sci Technol 209:60–68. https://doi.org/10.1016/j.anifeedsci.2015.08.002
John PH, Forsberg LS (1978) Determination of the sugar sequences and the glycosidic-bond arrangements of immunogenic heteroglycans. Carbohydr Res 60:167–178
Jones RR, Harkrader RJ, Southard GL (1986) The effect of pH on sanguinarine iminium ion form. J Nat Prod 49:1109–1111
Jouany J, Morgavi DP (2007) Use of ‘natural’ products as alternatives to antibiotic feed additives in ruminant production. Animal 1:1443–1466. https://doi.org/10.1017/S1751731107000742
Jouany J, Jose M, Morgavi DP, De LU (2012) Rumen protozoa and methanogenesis: not a simple cause—effect relationship. Br J Nutr 107:388–397. https://doi.org/10.1017/S0007114511002935
Juottonen H, Galand PE, Yrjälä K (2006) Detection of methanogenic Archaea in peat: comparison of PCR primers targeting the mcrA gene. Res Microbiol 157:914–921. https://doi.org/10.1016/j.resmic.2006.08.006
Kamra DN, Singh B (2019) Rumen microbiome and plant secondary metabolites (PSM): inhibition of methanogenesis and improving nutrient utilization. In: Satyanarayana T, Deshmukh S, Deshpande M (eds) Advancing frontiers in mycology and mycotechnology. Springer, Berlin
Khiaosa-ard R, Mahmood M, Lerch F et al (2020) Physicochemical stressors and mixed alkaloid supplementation modulate ruminal microbiota and fermentation. Anaerobe 65:102263. https://doi.org/10.1016/j.anaerobe.2020.102263
Kim ET, Guan LL, Lee SJ et al (2015) Effects of flavonoid-rich plant extracts on in vitro ruminal methanogenesis, microbial populations and fermentation characteristics. Asian Australas J Anim Sci 28:530–537. https://doi.org/10.5713/ajas.14.0692
Klop G, Dijkstra J, Dieho K et al (2017) Enteric methane production in lactating dairy cows with continuous feeding of essential oils or rotational feeding of essential oils and lauric acid. J Dairy Sci 100:3563–3575. https://doi.org/10.3168/jds.2016-12033
Knudsen D, Jutfelt F, Sundh H et al (2008) Dietary soya saponins increase gut permeability and play a key role in the onset of soyabean-induced enteritis in Atlantic salmon (Salmo salar L.). Br J Nutr 100:120–129. https://doi.org/10.1017/S0007114507886338
Kougias PG, Angelidaki I (2018) Biogas and its opportunities—a review. Front Environ Sci 12:1–22. https://doi.org/10.1007/s11783-018-1037-8
Krehbiel CR, Step DL, Fulton RW et al (2014) Rumen temperature change monitored with remote rumen temperature boluses after challenges with bovine viral diarrhea virus and Mannheimia haemolytica Rumen temperature change monitored with remote rumen temperature boluses after challenges with bovine vir. J Anim Sci 89:1193–1200. https://doi.org/10.2527/jas.2010-3051
Kumar A, Kameshwar S, Qin W (2018) Genome wide analysis reveals the extrinsic cellulolytic and biohydrogen generating abilities of Neocallimastigomycota fungi. J Genomics 6:74–87. https://doi.org/10.7150/jgen.25648
Kumar DD, Pannunzio Dias-Silva T, Sakita GZ et al (2020) Plants extract and bioactive compounds on rumen methanogenesis. Agrofor Syst 6:1541–1553. https://doi.org/10.1007/s10457-019-00411-6
Ku-Vera JC, Jiménez-Ocampo R, Valencia-Salazar SS et al (2020) Role of secondary plant metabolites on enteric methane mitigation in ruminants. Front Vet Sci 7:1–14. https://doi.org/10.3389/fvets.2020.00584
Lakes JE, Richards CI, Flythe MD (2020) Anaerobe inhibition of bacteroidetes and firmicutes by select phytochemicals. Anaerobe 61:102145. https://doi.org/10.1016/j.anaerobe.2019.102145
Lebiocka M, Montusiewicz A, Cydzik-Kwiatkowska A (2018) Effect of bioaugmentation on biogas yields and kinetics in anaerobic digestion of sewage sludge. Int J Environ Res Public Health. https://doi.org/10.3390/ijerph15081717
Lee JH, Kumar S, Lee GH et al (2013) Methanobrevibacter boviskoreani sp. nov., isolated from the rumen of Korean native cattle. Int J Syst Evol Microbiol 63:4196–4201. https://doi.org/10.1099/ijs.0.054056-0
Lee S, Baek Y, Lee J, Kim M (2020) Methanogenic archaeal census of ruminal microbiomes. J Korea Acad Coop Soc 21:312–320
Leng L, Yang P, Singh S et al (2018) A review on the bioenergetics of anaerobic microbial metabolism close to the thermodynamic limits and its implications for digestion applications. Bioresour Technol 247:1095–1106. https://doi.org/10.1016/j.biortech.2017.09.103
Li J, Rui J, Yao M et al (2015) Substrate type and free ammonia determine bacterial community structure in full-scale mesophilic anaerobic digesters treating cattle or swine manure. Front Microbiol 6:1–10. https://doi.org/10.3389/fmicb.2015.01337
Li W, Hou Q, Wang Y et al (2018a) Analysis of the gut microbial diversity of dairy cows during peak lactation by PacBio single-molecule real-time (SMRT) sequencing. Curr Biotechnol 75:1316–1323. https://doi.org/10.1007/s00284-018-1526-9
Li Z, Deng Q, Liu Y et al (2018b) Dynamics of methanogenesis, ruminal fermentation and fiber digestibility in ruminants following elimination of protozoa: a meta-analysis. J Anim Sci Biotechnol 9:1–9. https://doi.org/10.1186/s40104-018-0305-6
Liang Y, Li Y, Zhang L, Liu X (2019) Phytochemicals and antioxidant activity in four varieties of head cabbages commonly consumed in China. Food Prod Process Nutr 1:1–9. https://doi.org/10.1186/s43014-019-0003-6
Lila ZA, Mohammed N, Kanda S et al (2003) Effect of sarsaponin on ruminal fermentation with particular reference to methane production in vitro. J Dairy Sci 86:3330–3336. https://doi.org/10.3168/jds.S0022-0302(03)73935-6
Lugo-Coyote R, Kholif AE, Elghandour MMY et al (2016) The effect of garlic oil, xylanase enzyme and yeast on biomethane and carbon dioxide production from 60-days old holstein dairy calves fed a high concentrate diet. J Clean Prod. https://doi.org/10.1016/j.jclepro.2016.11.036
Malecky M, Albarello H, Broudiscou LP (2012) Degradation of terpenes and terpenoids from Mediterranean rangelands by mixed rumen bacteria in vitro. Animal 6:612–616. https://doi.org/10.1017/S1751731111001947
Manatbay B, Cheng Y, Mao S, Zhu W (2014) Effect of gynosaponin on rumen in vitro methanogenesis under different forage-concentrate ratios. Asian-Australas J Anim Sci 27:1088–1097. https://doi.org/10.5713/ajas.2013.13714
Mangwe MC, Mlambo V, Chiang HI (2017) Enteric methane emissions and protozoa populations in Holstein steers fed spent mushroom (Flammulina velutipes) substrate silage-based diets. Anim Feed Sci Technol 234:78–87. https://doi.org/10.1016/j.anifeedsci.2017.06.005
Maria JM, Lourdes S, Eugenio U et al (2015) Coumarins—an important class of phytochemicals. In: Rao AV, Rao LG (eds) Phytochemicals isolation, characterisation and role in human health. IntechOpen, Rijeka, Croatia, pp 113–140
Mart G, Abecia L, Mart AI et al (2015) Response of the rumen archaeal and bacterial populations to anti-methanogenic organosulphur compounds in continuous-culture fermenters. FEMS Microbiol Ecol 91:1–11. https://doi.org/10.1093/femsec/fiv079
Masebinu SO, Akinlabi ET, Muzenda E et al (2018) Experimental and feasibility assessment of biogas production by anaerobic digestion of fruit and vegetable waste from Joburg Market. Waste Manag 75:236–250. https://doi.org/10.1016/j.wasman.2018.02.02.011
Matsubayashi M, Shimada Y, Li Y et al (2017) Phylogenetic diversity and in situ detection of eukaryotes in anaerobic sludge digesters. PLoS ONE 12:1–13. https://doi.org/10.1371/journal.pone.0172888
McAllister TA, Bae HD, Jones GA, Cheng KJ (1994) Microbial attachment and feed digestion in the rumen. J Anim Sci 72:3004–3018. https://doi.org/10.2527/1994.72113004x
Mendel VE, Raghavan GV (1964) A study of diurnal temperature patterns in sheep. J Physiol 174:206–216. https://doi.org/10.1113/jphysiol.1964.sp007482
Merrettig-Bruns U, Jelen E (2009) Anaerobic biodegradation of detergent surfactants. Materials (Basel) 2:181–206. https://doi.org/10.3390/ma2010181
Mickdam E, Khiaosa-ard R, Metzler-Zebeli BU et al (2016) Rumen microbial abundance and fermentation profile during severe subacute ruminal acidosis and its modulation by plant derived alkaloids in vitro. Anaerobe 39:4–13. https://doi.org/10.1016/j.anaerobe.2016.02.002
Miller TL (2015) Methanobrevibacter. Bergey’s Man Syst Archaea Bact. https://doi.org/10.1002/9781118960608.gbm00496
Moniello G, Richardson AJ, Duncan SH (1996) Effects of coumarin and sparteine on attachment to cellulose and cellulolysis by Neocallimastix frontalis RE1. Appl Environ Microbiol 62:4666–4668
Morgavi DP, Forano E, Martin C, Newbold CJ (2010) Microbial ecosystem and methanogenesis in ruminants. Animal 4:1024–1036. https://doi.org/10.1017/S1751731110000546
Naas A, Pope P (2019) A mechanistic overview of ruminal fibre digestion. Peer J Repr 7:e27831v1:1-35. https://doi.org/10.7287/peerj.preprints.27831v1
Neves L, Ferreira R, Oliveira R, Madalena Alves M (2010) Influence of innoculum acclimation in the biodegradation rate and estimated biodegradbility of cow manure, food waste and oil. Environ Eng Manag J 9:327–334
Ng F, Kittelmann S, Patchett ML et al (2016) An adhesin from hydrogen-utilizing rumen methanogen Methanobrevibacter ruminantium M1 binds a broad range of hydrogen-producing microorganisms. Environ Microbiol 18:3010–3021. https://doi.org/10.1111/1462-2920.13155
Nguyen SH, Nguyen HDT, Hegarty RS (2020) Defaunation and its impacts on ruminal fermentation, enteric methane production and animal productivity. Livest Res Rural Dev 32:4
Niwiska B (2012) Digestion in ruminants. Carbohydr Compr Stud Glycobiol Glycotechnol. https://doi.org/10.5772/51574
Nzila A (2017) Mini review: update on bioaugmentation in anaerobic processes for biogas production. Anaerobe 46:3–12. https://doi.org/10.1016/j.anaerobe.2016.11.007
Oatway L, Vasanthan T, Helm JH (2001) Phytic acid. Food Rev Int 17:419–431. https://doi.org/10.1081/FRI-100108531
Oleszek M, Kozachok S (2018) Antioxidant activity of plant extracts and their effect on methane fermentation in bioreactors. Int Agrophys 32:395–401. https://doi.org/10.1515/intag-2017-0031
Oleszek M, Krzeminska I (2017) Enhancement of biogas production by co-digestion of maize silage with common goldenrod rich in biologically active compounds. Bioresources 12:704–714. https://doi.org/10.15376/biores.12.1.704-714
Oleszek M, Król A, Tys J et al (2014) Comparison of biogas production from wild and cultivated varieties of reed canary grass. Bioresour Technol 156:303–306. https://doi.org/10.1016/j.biortech.2014.01.055
Olufemi FE, Veronica D, Godwin H (2019) Effect of anaerobic co-digestion on microbial community and biogas production. Biosci Biotechnol Res Asia 16:391–401. https://doi.org/10.13005/bbra/2754
Oppermann RA, Nelson WO, Brown RE (1957) In vitro studies on methanogenic rumen bacteria. J Dairy Sci 40:779–788. https://doi.org/10.3168/jds.S0022-0302(57)94554-X
Ozbayram EG, Ince O, Kleinsteuber S, Ince B (2016) Anaerobic co-digestion of cow manure and barley: effect of cow manure to barley ratio on methane production and digestion stability. Environ Prog Sustain Energy 35:589–595. https://doi.org/10.1002/ep.12250
Ozbayram EG, Ince O, Ince B, Harms H (2018) Comparison of rumen and manure microbiomes and implications for the inoculation of anaerobic digesters. Microorganisms 6:1–10. https://doi.org/10.3390/microorganisms6010015
Pan X, Liang C, Wang C et al (2017) One freshwater species of the genus Cyclidium, Cyclidium sinicum spec. nov. (Protozoa; Ciliophora), with an improved diagnosis of the genus Cyclidium. Int J Syst Evol Microbiol 67:557–564. https://doi.org/10.1099/ijsem.0.001642
Pang J, Liu ZY, Hao M et al (2017) An isolated cellulolytic Escherichia coli from bovine rumen produces ethanol and hydrogen from corn straw. Biotechnol Biofuels 10:1–10. https://doi.org/10.1186/s13068-017-0852-7
Parmar NR, Nirmal Kumar JI, Joshi CG (2015) Deep insights into carbohydrate metabolism in the rumen of Mehsani buffalo at different diet treatments. Genomics Data 6:59–62. https://doi.org/10.1016/j.gdata.2015.08.007
Pastor-Belda M, Arroyo-Manzanares N, Yavir K et al (2020) A rapid dispersive liquid–liquid microextraction of antimicrobial onion organosulfur compounds in animal feed coupled to gas chromatography–mass. Anal Methods. https://doi.org/10.1039/d0ay00632g
Patra AK, Saxena J (2009) The effect and mode of action of saponins on the microbial populations and fermentation in the rumen and ruminant production. Nutr Res Rev 22:204–219. https://doi.org/10.1017/S0954422409990163
Patra KA, Saxena J (2010) A new perspective on the use of plant secondary metabolites to inhibit methanogenesis in the rumen. Phytochemistry 71:1198–1222. https://doi.org/10.1016/j.phytochem.2010.05.010
Patra AK, Stiverson J, Yu Z (2012) Effects of quillaja and yucca saponins on communities and select populations of rumen bacteria and archaea, and fermentation in vitro. J Appl Microbiol 113:1329–1340. https://doi.org/10.1111/j.1365-2672.2012.05440.x
Patra A, Park T, Kim M, Yu Z (2017) Rumen methanogens and mitigation of methane emission by anti-methanogenic compounds and substances. J Anim Sci Biotechnol 8:1–18. https://doi.org/10.1186/s40104-017-0145-9
Pavi S, Kramer LE, Gomes LP et al (2017) Biogas production from co-digestion of organic fraction of municipal solid waste and fruit and vegetable waste. Bioresour Technol 228:362–367. https://doi.org/10.1016/j.biortech.2017.01.003
Pellikaan WF, Stringano E, Leenaars J et al (2011) Evaluating effects of tannins on extent and rate of in vitro gas and CH4 production using an automated pressure evaluation system (APES). Anim Feed Sci Technol 166–167:377–390. https://doi.org/10.1016/j.anifeedsci.2011.04.072
Perna FJ, Cassiano EC, Martins M et al (2017) Effect of tannins-rich extract from Acacia mearnsii or monensin as feed additives on ruminal fermentation efficiency in cattle. Livest Sci 203:21–29. https://doi.org/10.1016/j.livsci.2017.06.009
Piluzza G, Sulas L, Bullitta S (2014) Tannins in forage plants and their role in animal husbandry and environmental sustainability: a review. Grass Forage Sci 69:32–48. https://doi.org/10.1111/gfs.12053
Pinotti L, Manoni M, Fumagalli F et al (2020) Reduce, reuse, recycle for food waste: a second life for fresh-cut leafy salad crops in animal diets. Animals 10:1–14. https://doi.org/10.3390/ani10061082
Popp D, Schrader S, Kleinsteuber S et al (2015) Biogas production from coumarin-rich plants–inhibition by coumarin and recovery by adaptation of the bacterial community. FEMS Microbiol Ecol Adv Access 91:fiv103. https://doi.org/10.1093/femsec/fiv103
Popp D, Harms H, Sträuber H (2016) The alkaloid gramine in the anaerobic digestion process—inhibition and adaptation of the methanogenic community. Environ Biotechnol 100:7311–7322. https://doi.org/10.1007/s00253-016-7571-z
Popp D, Plugge CM, Kleinsteuber S et al (2017) Inhibitory effect of coumarin on syntrophic fatty acid oxidising and methanogenic cultures and biogas reactor microbiomes. Environ Microbiol 83:e00438-e517. https://doi.org/10.1128/AEM.00438-17
Prabhudessai V, Ganguly A, Mutnuri S (2009) Effect of caffeine and saponin on anaerobic digestion of food waste. Ann Microbiol 59:643–648. https://doi.org/10.1007/BF03179203
Priya M, Haridas A, Manilal VB (2008) Anaerobic protozoa and their growth in biomethanation systems. Biodegradation 19:179–185. https://doi.org/10.1007/s10532-007-9124-8
Purba RAP, Paengkoum S, Yuangklang C, Paengkoum P (2020) Flavonoids and their aromatic derivatives in piper betle powder promote in vitro methane mitigation in a variety of diets. Cienc Agrotecnol 44:1–11. https://doi.org/10.1590/1413-7054202044012420
Qian B, Yin L, Yao X et al (2018) Effects of fermentation on the hemolytic activity and degradation of Camellia oleifera saponins by Lactobacillus crustorum and Bacillus subtilis. FEMS Microbiol Lett. https://doi.org/10.1093/femsle/fny014
Rabii A, Aldin S, Dahman Y, Elbeshbishy E (2019) A review on anaerobic co-digestion with a focus on the microbial populations and the effect of multi-stage digester configuration. Energies. https://doi.org/10.3390/en12061106
Rafińska K, Pomastowski P, Wrona O et al (2017) Medicago sativa as a source of secondary metabolites for agriculture and pharmaceutical industry. Phytochem Lett 20:520–539. https://doi.org/10.1016/j.phytol.2016.12.006
Ramírez-Restrepo CA, Barry TN (2005) Alternative temperate forages containing secondary compounds for improving sustainable productivity in grazing ruminants. Anim Feed Sci Technol 120:179–201. https://doi.org/10.1016/j.anifeedsci.2005.01.015
Rashama C, Ijoma G, Matambo T (2019) Biogas generation from by-products of edible oil processing: a review of opportunities, challenges and strategies. Biomass Convers Biorefinery 9:803–826. https://doi.org/10.1007/s13399-019-00385-6
Rathod VP, Bhale PV, Mehta RS et al (2018) Biogas production from water hyacinth in the batch type anaerobic digester. Mater Today Proc 5:23346–23350. https://doi.org/10.1016/j.matpr.2018.11.072
Ribeiro GO, Gruninger RJ, Badhan A, McAllister TA (2016) Mining the rumen for fibrolytic feed enzymes. Anim Front 6:20–26. https://doi.org/10.2527/af.2016-0019
Rincón B, Fernando GF, Borja R (2012) Olive oil mill waste treatment: improving the sustainability of the olive oil industry with anaerobic digestion technology. In: Dimitrios B (ed) Olive oil—constituents, quality, health properties and bioconversions. Intechopen, London, pp 274–292. https://doi.org/10.5772/28583m
Rira M, Morgavi DP, Genestoux L et al (2019) Methanogenic potential of tropical feeds rich in hydrolyzable tannins. J Anim Sci 97:2700–2710. https://doi.org/10.1093/jas/skz199
Rojas C, Fang S, Uhlenhut F et al (2010) Stirring and biomass starter influences the anaerobic digestion of different substrates for biogas production. Eng Life Sci 10:339–347. https://doi.org/10.1002/elsc.200900107
Ruiz B, Flotats X (2014) Citrus essential oils and their influence on the anaerobic digestion process: an overview. Waste Manag 34:2063–2079. https://doi.org/10.1016/j.wasman.2014.06.026
Russell JB, Hespell RB (1981) Microbial rumen fermentation. J Dairy Sci 64:1153–1169. https://doi.org/10.3168/jds.S0022-0302(81)82694-X
Ryckebosch E, Drouillon M, Vervaeren H (2011) Techniques for transformation of biogas to biomethane. Biomass Bioenergy 35:1633–1645. https://doi.org/10.1016/j.biombioe.2011.02.033
Sahu N, Sharma A, Mishra P et al (2017) Evaluation of biogas production potential of kitchen waste in the presence of spices. Waste Manag 70:236–246. https://doi.org/10.1016/j.wasman.2017.08.045
Santos ET, Pereira MLA, Flávia C, Silva PG (2013) Antibacterial activity of the alkaloid-enriched extract from Prosopis juliflora pods and its influence on in vitro ruminal digestion. Mol Sci 14:8496–8516. https://doi.org/10.3390/ijms14048496
Satyajit DS, Lutfun N (2018) Phytochemicals and phyto-extracts in cosmetics. Trends Phytochem Res 2:185–186
Saxena M, Jyoti S, Rajeev N et al (2013) Phytochemistry of medicinal plants. J Pharmacogn Phytochem 1:13–14. https://doi.org/10.1007/978-1-4614-3912-7_4
Seradj AR, Abecia L, Crespo J et al (2014) The effect of Bioflavex® and its pure flavonoid components on in vitro fermentation parameters and methane production in rumen fluid from steers given high concentrate diets. Anim Feed Sci Technol 197:85–91. https://doi.org/10.1016/j.anifeedsci.2014.08.013
Shreck AL, Nuttelman BL, Harding JL, Griffin WA (2015) Digestibility and performance of steers fed low-quality crop residues treated with calcium oxide to partially replace corn in distillers grains finishing diets 1. J Anim Sci 93:661–671. https://doi.org/10.2527/jas2013-7194
Sinz S, Kunz C, Liesegang A et al (2018) In vitro bioactivity of various pure flavonoids in ruminal fermentation, with special reference to methane formation. Czech J Anim Sci 63:293–304. https://doi.org/10.17221/118/2017-CJAS
Sioud M, Possot O, Elie C et al (1988) Coumarin and quinolone action in archaebacteria: evidence for the presence of a DNA gyrase-like enzyme. J Bacteriol 170:946–953
Sirohi SK, Pandey N, Singh B, Puniya AK (2010) Rumen methanogens: a review. Indian J Microbiol 50:253–262. https://doi.org/10.1007/s12088-010-0061-6
Skillman LC, Evans PN, Naylor GE et al (2004) 16S ribosomal DNA-directed PCR primers for ruminal methanogens and identification of methanogens colonising young lambs. Anaerobe 10:277–285. https://doi.org/10.1016/j.anaerobe.2004.05.003
Smith HP, Hungate RE (1958) Isolation and characterization of Methanobacterium formicicum MF. Int J Syst Bacteriol 75:713. https://doi.org/10.1099/00207713-37-2-171
Spence A, Madrigal EB, Patil R, Fernandez YB (2019) Evaluation of anaerobic digestibility of energy crops and agricultural byproducts. Bioresour Technol 5:243–250. https://doi.org/10.1016/j.biteb.2018.11.004
St-Pierre B, Wright AG (2014) Comparative metagenomic analysis of bacterial populations in three full-scale mesophilic anaerobic manure digesters. Appl Microbiol Biotechnol 98:2709–2717. https://doi.org/10.1007/s00253-013-5220-3
Tsapekos P, Kougias PG, Treu L et al (2017) Process performance and comparative metagenomic analysis during co-digestion of manure and lignocellulosic biomass for biogas production. Appl Energy 185:126–135. https://doi.org/10.1016/j.apenergy.2016.10.081
Urbano G, Aranda P, Tenorio E, Porres J (2000) The role of phytic acid in legumes: antinutrient or beneficial function? J Physiol Biochem 56:283–294
Ushida K (1997) Ciliate protozoa and ruminal methanogenesis. In: Karger AS (ed) Rumen microbes and digestive physiology in ruminants. Japan Scientific Societies Press, Tokyo, pp 209–220
Van Lingen HJ, Plugge CM, Fadel JG et al (2016) Thermodynamic driving force of hydrogen on rumen microbial metabolism: a theoretical investigation. PLoS ONE 11:1–18. https://doi.org/10.1371/journal.pone.0161362
Vavouraki AI, Zakoura MV, Dareioti MA, Kornaros M (2020) Biodegradation of polyphenolic compounds from olive mill wastewaters (OMW) during two-stage anaerobic co-digestion of agro-industrial mixtures. Waste Biomass Valoris 11:5783–5791. https://doi.org/10.1007/s12649-019-00887-4
Verstraete W, Wittebolle L, Heylen K et al (2007) Microbial resource management: the road to go for environmental biotechnology. Eng Life Sci 7:117–126. https://doi.org/10.1002/elsc.200620176
Wanapat M, Chanthakhoun V, Phesatcha K, Kang S (2014) Influence of mangosteen peel powder as a source of plant secondary compounds on rumen microorganisms, volatile fatty acids, methane and microbial protein synthesis in swamp buffaloes. Livest Sci 162:126–133. https://doi.org/10.1016/j.livsci.2014.01.025
Wang M, Zhao Z, Niu J, Zhang Y (2019) Potential of crystalline and amorphous ferric oxides for biostimulation of anaerobic digestion. ACS Sustain Chem Eng 7:697–708. https://doi.org/10.1021/acssuschemeng.8b04267
Wilkins D, Rao S, Lu X, Lee PKH (2015) Effects of sludge inoculum and organic feedstock on active microbial communities and methane yield during anaerobic digestion. Front Microbiol 6:1–11. https://doi.org/10.3389/fmicb.2015.01114
Winardi DN, Syafrudin S, Lathifah LP (2020) Biogas production from water hyacinth. In: Abomohra AE-F, Mahdy E, Qin Z et al (eds) Biogas. Intotech, London, p 13
Wink M (2015) Modes of action of herbal medicines and plant secondary metabolites. Medicines 2:251–286. https://doi.org/10.3390/medicines2030251
Wright AG, St-Pierre B (2013) Diversity of gut methanogens in herbivorous animals. Animal 7:49–56. https://doi.org/10.1017/S1751731112000912
Yang Y, Yu K, Xia Y et al (2014) Metagenomic analysis of sludge from full-scale anaerobic digesters operated in municipal wastewater treatment plants. Environ Biotechnol 98:5709–5718. https://doi.org/10.1007/s00253-014-5648-0
Zehavi T, Probst M, Mizrahi I (2018) Insights into culturomics of the rumen microbiome. Front Microbiol 9:1–10. https://doi.org/10.3389/fmicb.2018.01999
Zema DA, Fòlino A, Zappia G et al (2018) Anaerobic digestion of orange peel in a semi-continuous pilot plant: an environmentally sound way of citrus waste management in agro-ecosystems. Sci Total Environ 630:401–408. https://doi.org/10.1016/j.scitotenv.2018.02.168
Zhan J, Liu M, Su X et al (2017) Effects of alfalfa flavonoids on the production performance, immune system, and ruminal fermentation of dairy cows. Asian-Australas J Anim Sci 30:1416–1424
Ziyang L, Youcai Z (2017) Leachate pollution control technology at sanitary landfill. In: McCombs K (ed) Pollution control and resource recovery: municipal solid wastes at landfill. Butterworth-Heinemann, Oxford, pp 147–226
Acknowledgements
Funding was provided by Department of Science and Technology (RSA) (Grant No. DST/CON 0197/2017) and Technology and Innovation Agency (RSA) (Grant No. 2018/FUN/0166). Authors would also like to thank colleagues Judith Kgodiso and Sylvie Heri for proofreading and constructive criticism about ruminant methanogenesis and biochemical pathways.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Rashama, C., Ijoma, G.N. & Matambo, T.S. The effects of phytochemicals on methanogenesis: insights from ruminant digestion and implications for industrial biogas digesters management. Phytochem Rev 20, 1245–1271 (2021). https://doi.org/10.1007/s11101-021-09744-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11101-021-09744-6