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Use of Asian selected agricultural byproducts to modulate rumen microbes and fermentation

Use of Asian selected agricultural byproducts to modulate rumen microbes and fermentation In the last five decades, attempts have been made to improve rumen fermentation and host animal nutrition through modulation of rumen microbiota. The goals have been decreasing methane production, partially inhibiting protein degradation to avoid excess release of ammonia, and activation of fiber digestion. The main approach has been the use of dietary supplements. Since growth-promoting antibiotics were banned in European countries in 2006, safer alternatives including plant-derived materials have been explored. Plant oils, their component fatty acids, plant secondary metabolites and other compounds have been studied, and many originate or are abundantly available in Asia as agricultural byproducts. In this review, the potency of selected byproducts in inhibition of methane production and protein degradation, and in stimulation of fiber degradation was described in relation to their modes of action. In particular, cashew and ginkgo byproducts containing alkylphenols to mitigate methane emission and bean husks as a source of functional fiber to boost the number of fiber-degrading bacteria were highlighted. Other byproducts influencing rumen microbiota and fermentation profile were also described. Future application of these feed and additive candidates is very dependent on a sufficient, cost-effective supply and optimal usage in feeding practice. Keywords: Agricultural byproduct, Fermentation, Fiber degradation, Methane mitigation, Microbiota, Plant secondary metabolites, Rumen Backgrounds respectively. These effects were observed after supple- The rumen is a dense and diverse microbial ecosystem, mentation with antibiotics [4] and halogenic chemicals capable of transforming fibrous plant material and non- [7], the majority of which have now fallen out of favor due protein nitrogen into valuable products, such as short to global concerns regarding food safety and environmen- chain fatty acids and microbial protein [1]. However, this tal burden. Therefore, alternative agents are required, fermentation process is accompanied by the synthesis of preferably naturally occurring materials such as plant non-beneficial products such as methane and is not resources [3, 8]. The main components, most of which are always efficient, due to the limited supply of essential plant secondary materials, have been screened out. They nutrients and/or inadequate feed formulation. Therefore, have ecological functions as chemical messengers between particular attention should be paid to dietary regimens plants and the environment, often exhibiting antimicrobial that optimize fermentation. Several dietary supplements activity [9]. Such alternatives have been actively ex- have been proposed for such a purpose [2–6], targeting plored, especially since growth-promoting antibiotics inhibition of methane and rapid ammonia release, and were banned in Europe in 2006. improvement of fiber degradation. Fiber digestion is preceded by fiber-digesting rumen Inhibition of methane production and excess ammonia microbes, mainly bacteria [10]. Therefore, preferential formation conserves dietary energy and proteins, activation of fibrolytic rumen bacteria is important. Bac- terial growth can be stimulated by vitamins, amino acids, branched chain fatty acids and other nutrients. Add- * Correspondence: kyas@anim.agr.hokudai.ac.jp Lab of Animal Function and Nutrition, Research Faculty of Agriculture, itionally, the use of easily degradable fiber as a strategy Hokkaido University, Sapporo 060-8589, Japan © The Author(s). 2016 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Kobayashi et al. Journal of Animal Science and Biotechnology (2016) 7:70 Page 2 of 10 has been known since the 1980s [11–13]. Evaluation of Indeed, Watanabe et al. [21] first indicated that unheated supplements as boosters for fiber degradation should in- CNSL dramatically reduced methane production while clude the determination of fiber digestibility as well as increasing propionate production in batch cultures. They the analysis of rumen bacterial abundance and activity. also reported that CNSL reduced methane levels in a A mechanistic understanding of expected events would rumen simulation technique (RUSITEC) fermenter, ac- confirm theoretical knowledge, making supplement use companied by drastic alterations in rumen microbiota. more acceptable to farmers. Materials that have been Quantitative polymerase chain reaction (PCR) demon- proposed in the last decade include agricultural by- strated that formate and/or hydrogen producing bacteria products deemed safe, cost-effective and easily accept- decreased in abundance, while succinate and/or propionate able among farmers and product consumers. producing bacteria increased with CNSL supplementation. This review describes selected agricultural byproducts In feeding experiments using cattle, we observed a similar that are available in the Asian region as potent feed or response to CNSL [22]; specifically, a reduction in methane additive candidates for the above purposes. Character- emission (19-38%) accompanied by alteration in the rumi- istics, actions and benefits of such agricultural bypro- nal abundance of bacterial species responsible for methane ducts are discussed from the viewpoint of modulation of and propionate production, causing a shift in hydrogen rumen microbiota and fermentation. flow [23]. However, as expected, alterations of microbiota and fermentation profile in these feeding studies were less Selected byproducts containing plant secondary pronounced than those in in vitro studies. In feeding ex- compounds as inhibitors of formation of non-beneficial periments using sheep, microbial and metabolic alterations fermentation products were also observed, although alterations in the abundance Cashew byproduct of bacterial and archaeal members in sheep rumen (Suzuki Cashew nut shell liquid (CNSL), a byproduct of cashew et al. unpublished results) were not the same as those ob- nut production that accounts for about 32% of the shell, served in cattle rumen (Su et al. unpublished results). In has many industrial applications and is used as a raw fact, in response to CNSL feeding, groups belonging to material for products such as paints, brake linings, lac- Proteobacteria, relatives of Succinivibrio and Succinimonas, quers and coatings [14]. The global production of CNSL showed increased levels in the rumen of cattle and sheep, is estimated at 450,000 metric tonnes per year [15], pro- while increases in Methanomicrobium mobile and Metha- viding a readily available supply of CNSL. Vietnam and nobrevibacter wolinii were respectively observed in the India are major CNSL-producing countries. This liquid rumen of cattle and sheep. also exhibits a wide range of biological activities, as it As CNSL administration did not adversely affect contains compounds with antimicrobial [16], antioxida- digestibility in either cattle or sheep, this agricultural tive [17] and antitumor [18] properties, represented by byproduct can be recommended for use as a potent anacardic acid, cardanol and cardol, which are all methane-inhibiting and propionate-enhancing agent, salicylic acid derivatives with a carbon-15 alkyl group. due to its effects on rumen microbiota. However, the These phenolic compounds, especially anacardic acid, long-term effects of CNSL should be evaluated for prac- are reported to inhibit a variety of bacteria [19]. Propor- tical application, as was emphasized for the ionophore tions of these alkyl phenols in CNSL vary with produ- monensin [24], which showed a reduction in efficacy cing area (cultivar) and deshelling process (heating). with increased feeding period duration. Therefore, the function of CNSL as a rumen modifier Later in vitro and in vivo studies on CNSL do not can also vary with these factors, as indicated in Tables 1 wholly support the above favorable results, due to the and 2. low level of CNSL supplementation and heat treatment An early study by Van Nevel et al. [20] first indicated for CNSL preparation (Table 1). Although CNSL supple- that anacardic acid could be used as a propionate mentation decreased methane production, inhibition enhancer in the rumen. Anacardic acid is found in was only 18% [25], while it was 57% in the similar cashew and ginkgo trees, particularly in their seeds. As batch culture system used in our study [21]. CNSL feed- cashew is the more abundant plant material, it is con- ing to dairy cows decreased methane emission by only sidered a more useful source of anacardic acid. The 8% [26]. The differences between these later results and main action of anacardic acid and related phenolics is our initial ones might be the quantity and quality of a surfactant action that inhibits mainly Gram-positive CNSL. Danielson et al. [25] tested 3 times lower supple- bacteria [16] lacking an outer membrane. Such cells mentation level of CNSL than the level examined by are physically disrupted by anacardic acid. This select- Watanabe et al. [21], and Branco et al. [26] used heat- ive inhibition of Gram-positive rumen bacteria might processed CNSL that contains cardanol as a main phen- result in the alteration of rumen microbiota and fer- olic compound instead of the most potent phenolic, mentation products. anacardic acid [27–29]. Microbial response was clearly Kobayashi et al. Journal of Animal Science and Biotechnology (2016) 7:70 Page 3 of 10 Table 1 Effect of selected agricultural byproducts containing anacardic acid and other phenolics on dry matter (DM) digestibility and rumen fermentation parameters Byproduct, origin Description Phenolics, % in weight Reference Test by Dosed at DM digestibility, % Total VFA, Inhibition, % Reference mmol/dL Anacardic acid Caldanol Caldol Methane Ammonia Cashew shell, India Heated - 71.4 14.4 [21] Batch culture 0.5 mg/mL - ns 9.2 - [21] Raw 57.7 8.2 19.9 ibid. ibid - ns 56.9 - ibid. Raw ibid. ibid. ibid. ibid. RUSITEC 0.2 mg/mL ↑ ns 70.1 16.5 ibid. Raw ibid. ibid. ibid. ibid. Feeding (dry cow) 0.32% of DMI ns ns 19.3–38.3 ns [22] Raw ibid. ibid. ibid. ibid. Feeding (milking cow) ibid. ns ns 12.7 ns Shinkai et al. unpublished Raw ibid. ibid. ibid. ibid. Feeding (sheep) ibid. ns ns 61.4 43.0 Suzuki et al. unpublished Cashew shell, Tanzania Raw - - - [25] Batch culture 0.17 mg/mL - ns 17.8 - [25] Cashew shell, Brazil Heated - 62.9 13.4 [26] Feeding (milking cow) 0.11% of DMI ns - 8.0 - [26] Raw 64.9 1.2 13.3 [29] Cashew shell, Brazil Heated - 73.3 19.4 [28] Feeding (milking cow) 0.036% of DMI ns - - - [28] Raw 49.3 30.5 20.2 [27] Ginkgo fruit, Japan Cultivar A 85.0 2.3 12.7 Oh et al. Batch culture 3.2 mg/mL - ns 85.7 42.0 Oh et al. unpublished Cultivar B 86.8 2.3 10.9 unpublished ibid. 4.5 mg/mL - ns 65.9 46.0 ibid. RUSITEC 3.2 mg/mL ns ns 47.3 53.7 ibid. Ginkgo leaf, Korea Unspecified - - - Batch 1.0 mg/mL ns ns 46.7 - [30] -, No data available ns, Not significantly changed ↑, Significantly increased Calculated on basis of CH4 ml for in vitro test and of CH4 g/kg DMI for in vivo test, respectively Heat was used in deshelling process g of extract/mL (not calculable as original leaf) Kobayashi et al. Journal of Animal Science and Biotechnology (2016) 7:70 Page 4 of 10 Table 2 Effect of selected agricultural byproducts containing anacardic acid and other phenolics on rumen microbial abundance determined by quantitative PCR Byproduct Main compound Tested by Dosed at Abundance of rumen microbe, relative % to total bacteria Reference involved Pro Meth Fu Fs Rf Ra Me Sr Sd Tb Sb Pr Pb Rm Al Cashew shell Anacardic acid RUSITEC 0.2 mg/mL ↓ ns - ↓↓ ns ↑↑ ↑ ↓ ns ↓↓ ns ↑ [21] Feeding (dry cow) 0.32% of DMI ns ns - ns ↓↓ - ↑↑ ↓ - ↑ -- ↑ [22] Feeding (milking cow) 0.33% of DMI - ns ns ↓ ns ns ns ns ns ns ns ns ns ns ns Shinkai et al. unpublished Feeding (sheep) 0.32% of DMI ↓ - - ns ns ns ns ns ns ns ns ns ns ns ns Suzuki et al. unpublished Ginkgo fruit Anacardic acid Batch culture, culivar A 3.2 mg/mL - ↑ -ns ns ns ↑↑ ↑ ↓ ↑ ns ↑ ns ns Oh et al. unpublished Batch culture, cultivar B 4.5 mg/mL - ↑ -ns ns ns ns ns ↓ ns ↑ ns ↑ ns ↓ ibid. RUSITEC, cultivar A 3.2 mg/mL ↓↓ ↓ ↓ ↓ ↓ ↑ ↑ ↑ ↓ ns ↑↓ ↑ ↑ ibid. Ginkgo leaf Unspecified Batch culture 1.0 mg/mL ↓↑ - ↑↓ ↓ - - - --- - - - [30] Pro protozoa, Meth methanogen, Fu fungi, Fs Fibrobacter succinogenes,Rf Ruminococcus flavefaciens,Ra Ruminococcus albus,Me Megasphaera elsdenii,Sr Selenomonas ruminantium,Sd Succinovibrio dextrinosolvens,Tb Treponema bryantii,Sb Streptococcus bovis,Pr Prevotella ruminicola,Pb Prevotella bryantii,Rm Ruminobacter amylophilus,Al Anaerovibrio lipolytica -, No data available ns, Not significantly changed ↑, Significantly increased ↓, Significantly decreased Value were obtained by direct counting g of extract/mL (not calculable as original leaf) Kobayashi et al. Journal of Animal Science and Biotechnology (2016) 7:70 Page 5 of 10 different between these studies. Our MiSeq data in our Both CNSL [21] and ginkgo fruit extract (Oh et al. RUSITEC study demonstrated drastic alteration of mi- unpublished results) decrease ammonia concentration in crobial community structures: for eubacteria, a higher RUSITEC. Since both inhibit the growth of proteolytic, detection frequency of Veillonellaceae and Succinivibrio- peptidolytic and deaminating rumen bacteria in pure cul- naceae and lower frequency of the Ruminococcaceae, ture, feeding of these extracts may spare dietary protein, and for archaea, a higher frequency of Methanomicro- peptide and amino acid. In fact, the growth of hyper biaceae and lower frequency of Methanobacteriaceae ammonia-producing rumen bacteria was markedly inhib- (Kobayashi et al. unpublished results). Therefore, this ited by either the form of anacardic acid contained in cashew byproduct should be used in unheated form at an CNSL or ginkgo fruit extract (Oh et al. unpublished re- optimized supplementation level. Of alkylphenols present sults). Manipulation of protein and amino acid degradation in CNSL, anacardic acid is most functional but decarboxy- is important, because excreted ammonia could be the lated and converted to caldanol by heating and long ex- source of nitrous oxide, which has much higher potential posure to oxygen. Therefore, preparation and storage of for global warming than methane. Also, decreased ammo- CNSL are important to maintain its functionality. nia level in the rumen, but not lower than 5 mgN/dL to Recently, we found that CNSL feeding improved anti- ensure microbial protein synthesis [32], may improve feed oxidative status in cattle, causing higher free radical nitrogen economy. Since ginkgo fruit has not been tested scavenging activity and lower lipid peroxidation products in a feeding study, in vivo evaluation is to be made on in the rumen and blood serum (Konda et al. unpublished rumen and animal responses including palatability of the results). Although the mechanisms involved in these diet to which ginkgo fruit is supplemented. changes are not yet clear, anacardic acid possessing anti- oxidative activity [17], can affect theses parameters dir- Tea byproduct ectly and/or indirectly through alteration of rumen China is one of the biggest tea producers globally. Tea microbiota and their fermentation products. seed meal after oil extraction has previously been con- sidered worthless. However, saponins contained in the Ginkgo byproduct tea seed meal have been found to exert beneficial anti- Another source of anacardic acid is the ginkgo plant, protozoal and antimethanogenic effects through surfac- grown widely among Far-East countries such as China, tant action [33]. Significance of tea saponins and other Korea and Japan. Industrial uses of ginkgo are its leaves source plants such as yucca and quillaja for the use of for medicinal use (China) and its nuts for food (Japan). ruminant feed has been demonstrated [33, 34]. Table 3 Leaf extracts for medicinal use are even exported to shows functionality of saponins of tea seed, tea seed European countries and also evaluated as a rumen modi- meal and other source plants (Thai blueberry, fenugreek, fier [30]. Ginkgo fruit is a byproduct in the process of and mangosteen). A series of studies on tea seed sapo- ginkgo nut separation (unsuitable for human food use nins revealed that the addition of tea seed saponins to in due to its peculiar smell), yielding ca. 2,600 metric vitro cultures killed up to 79 % of protozoa. Moreover, t/yr in Japan, accounted for 230% of nut production in vivo experiments (feeding of tea seed saponin to [31]. Therefore, biomass of ginkgo fruit is much lambs at 3 g/d) showed that the relative number of smaller in comparison with CNSL. In this regard, use for rumen protozoa to rumen bacteria was reduced by 41% feed additive might be limited locally. after 72 d of tea saponin administration [35]. Using de- The main phenolic of ginkgo is anacardic acid, but it naturing gradient gel electrophoresis (DGGE) analysis, a has different alkyl groups in comparison with those of significantly lower diversity in protozoa was reported cashew (C13:0, C15:1 and C17:1 for ginkgo vs. C15:1, [36], indicating that the antiprotozoal activity of tea sapo- C15:2 and C15:3 for cashew). An in vitro evaluation of nins might not be transient. Although an exception was ginkgo fruit extract as a rumen modifier using batch and observed by Ramirez-Restrepo [37], negative effect of tea RUSITEC systems showed that the extract decreased saponins on rumen protozoa is consistent regardless of in methane production in a dose-dependent manner and vitro and in vivo conditions, and considered as one of microbial responses were similar to those observed for main factors to modulate rumen fermentation in relation CNSL (Tables 1 and 2), though such potency depends to bacterial and archaeal changes as discussed below. on the cultivar (Oh et al. unpublished results). The most The effect of tea saponins on the ruminal abundance potent phenolic for bacterial selection was anacardic of methanogenic archaea was not significant, while they acid, in particular monoenoic (15:1) anacardic acid. Our drastically decreased the expression of the methyl coen- MiSeq data suggest that ginkgo fruit extract greatly zyme M reductase gene (mcrA) in the rumen [38]. This modulates the microbiota of RUSITEC (Oh et al. unpub- suggests that selective inhibition of methanogens might lished results) similarly to what was found for CNSL be involved in the antiprotozoal action. Using defau- supplementation. nated and refaunated sheep, Zhou et al. [36] showed that Kobayashi et al. Journal of Animal Science and Biotechnology (2016) 7:70 Page 6 of 10 Table 3 Effect of selected agricultural byproducts containing saponins and other phenolics on dry matter (DM) digestibility, rumen fermentation parameters and microbial abundance Byproduct Main compounds Tested by Dosed at DM digestibility, % Total VFA, Inhibition, % Abundance, relative % Reference involved mmol/dL Methane Ammonia Protozoa Meth Fungi Fs Rf Ra Tea seed/seed meal Saponins Batch culture 0.4 mg/mL - ns 8.0 - 51.3 ns ↓↑ ns - [38] Feeding (sheep) 3 g/d - ns 10.6 13.2 43.2 ns ns ↓ ns ns [36] Feeding (steer) 0.24–0.38% of DMI - ns 15.6 - ns ns - ↑↓ ↑ [37] Feeding (growing lamb) 0.41% of DMI - ↑ 27.5 ns 41.1 ns ns - ns ns [35] Thai bllueberry seed Saponins Feeding (goat) 0.8–24% of DMI ns ns 2.2–8.0 ns ns - - - - - [46] Fenugreek seed Saponins Batch culture 0.14–0.29 mg/mL - ns 1.8–2.0 - 15.0–39.0 ↓↓ ↑ ↑ -[41] Mangosteen peel Saponins, tannins Feeding (dairy cow) 100–300 g/d - - 5.5–13.8 - 20.5–47.1 ↓ ns ns ns ns [47] Eucarypus leaf meal Cineol, cryptone etc. Feeding (swamp buffalo) 0.7–2.0% of DMI ns ↑ 8.4–13.9 12.7–33.9 5.5–22.0 - - - - - {51} Meth methanogen, Fs Fibrobacter succinogenes,Rf Ruminococcus flavefaciens,Ra Ruminococcus albus -, No data available ns, Not significantly changed ↑, Significantly increased ↓, Significantly decreased Dosage could not be expressed as % of dry matter intake (DMI) due to lack of data on feed intake Kobayashi et al. Journal of Animal Science and Biotechnology (2016) 7:70 Page 7 of 10 tea saponins reduce methane production by inhibiting fatty acid production toward more propionate and less protozoa, most likely in coordination with their suppres- acetate and butyrate. Methane production linearly de- sive effects on protozoa-associated methanogens. Indeed, creased (up to 8%) and nitrogen retention linearly in- the presence and functional significance of protozoa- creased (up to 45%) with seed meal supplementation associated methanogens has been demonstrated [39, 40]. level. Therefore, this byproduct might be an effective Saponins alter rumen microbial community with a de- modulator of rumen fermentation and ruminant nutri- crease in protozoa and fungi and increase in Fibrobacter tion, though the mechanisms involved are not clear. succinogenes [38, 41]. The latter can compensate for Feeding of mangosteen peel powder to lactating cows fiber digestion possibly depressed by the decreased num- (300 g/d) can decrease methane production by 14% with ber of fungi, leading to a fermentation change toward a drastic decrease of rumen protozoa, while other repre- less methane and more propionate, since protozoa and sentative rumen microbes are not affected [47]. Since fungi produce hydrogen, while F. succinogenes produces mangosteen contains not only saponins but also con- succinate as a propionate precursor. Recently, Belanche densed tannins, microbial and fermentation changes et al. [42] reported decreased diversity in the archaeal might be due to these two secondary metabolites. community by supplementation with ivy fruit saponins Polyphenols in chickpea husk (abundantly available in in RUSITEC fermenter: Methanomassilicocaaceae is southern and western Asia) exert antibacterial activity substituted by Methanobrevibacter, a theoretically less against mainly Gram-positive bacteria [48]. Rats fed chick- active community member even though it is predomin- pea husk at 5% level showed an altered hindgut bacterial ant in the rumen [43]. From these reports, it is apparent community based on different DGGE banding patterns that the mechanism involved in the modulation of [49]. The authors also found that chickpea husk extract rumen fermentation by saponins remains to be fully exhibited anti-oxidative activity measured as free radical characterized. Ruminal responses could differ depending scavenging activity and lipid peroxidation. In fact, rats fed on saponins that occur in a number of plants and com- chickpea husk had lower thiobarbituric acid reactive sub- prise a variety of molecules. Tea saponins are, as indi- stance (TBARS) values in their blood plasma, suggesting cated by a review article [34], one of the promising the potency of this byproduct as a health-promoting agent rumen modifier without negative influence on feed in- in animals [49]. These favorable effects of chickpea husk take and digestibility if supplemented properly (3–5 g/d are considered to be due to the presence of tannins that for goats and lambs). could have different impact depending on molecular spe- Tea byproducts also contain catechin that can increase cies (i.e. source plants, cultivars and growing region) [50]. the proportion of unsaturated fatty acids in goat meat Asia is the origin of many plants that are sources of [44], presumably through alterations in the rumen essential oils. As a byproduct of essential oil, leaf meal of microbiota. Another beneficial action of tea catechin is Eucalyptus camaldulensis is paid attention due to the to improve antioxidant status of beef, once the catechins ability to decrease rumen ammonia level (by 34%) when are ingested and absorbed by the animal. This was spec- fed to swamp buffaloes (120 g/d) possibly through the ulated by direct addition of tea catechins to beef [45]. action of 1,8-cineol [51]. Therefore, it is proposed as an- other possible manipulator of protein and amino acid Other byproducts degradation in the rumen, which might save feed nitro- Other materials potentially modulating rumen fermenta- gen. Since essential oils are generally expensive, their tion are also shown in Table 3. Fenugreek is cultivated byproducts (residue of oil extraction) such as the above in western and southern Asian regions, where it is used leaf meal is one option recommended for practical use. as a spice, seasoning, fragrance in the form of sprouts, New additive candidates from Asian agricultural and is also known as a source of saponins. Fenugreek byproducts have been explored for the use to decrease seed extract rich in saponin (0.29 mg/mL of diluted rumen methane and ammonia, in which in vitro evalu- rumen fluid) inhibits growth of protozoa and fungi and ation is often used for initial screening. This evaluation increases growth of fibrolytic bacteria, leading to 2% de- is quick, quantitative, and very useful to define mecha- crease of methane production in vitro [41], awaiting a nisms involved in the efficacy of candidate material. feeding assessment. However, as in vitro effect is always higher than in vivo The seeds of Thai blueberry, Antidesma thwaitesia- effect, final recommendation is to be made after detailed num Muell. Arg., containing condensed tannin, were evaluation by a series of feeding studies. evaluated as a ruminant feed [46]; goats fed the diet with this meal from the wine and juice industry (inclusion of Easily digestible fibers as boosters of fiber degraders 0.8–2.4% in DM) did not show any differences in feed Chickpea and lablab bean husks intake, digestibility, ruminal pH or ammonia-nitrogen, Fibers are not always efficiently degraded in the rumen while they showed a dose-dependent shift in short chain due to complexity of fiber structure and components Kobayashi et al. Journal of Animal Science and Biotechnology (2016) 7:70 Page 8 of 10 and less well optimized rumen microbiota. Recently, heavily colonized by F. succinogenes. Pure cultures of some easily degradable fibers have been proposed to several different strains of F. succinogenes revealed modulate rumen microbiota toward quick optimization growth stimulation after addition of the bean husks as of developing fiber-degrading consortia [52]. We have the sole carbon substrate. found that husks from a few species of local beans Finally, a digestion trial, in which each type of husk was (chickpea and lablab bean) show high potency in im- supplemented at 10%, was employed to evaluate them as proving rumen fermentation [52, 53]. The functionality digestion boosters for a rice straw-based diet [53]. The of these husks is summarized in Table 4. These fiber digestibility of acid detergent fiber was 3.1–5.5% greater in sources are considered a replaceable fibrous feed, as well diets supplemented with chickpea husk or lablab bean as a booster of the degradation of the main forage. In- husk than in the control. Total short chain fatty acid levels deed, these fiber sources can be characterized as easily were higher in sheep fed lablab bean husk-supplemented digestible [11, 12]. diet than in sheep fed other diets, while acetate levels were Easily digestible fiber sources might promote the rapid higher in lablab bean husk-supplemented diet than in the growth of fibrolytic microbial biomass, which in turn fa- control diet. Ruminal abundance of F. succinogenes was cilitates the digestion of the other fiber in the rumen. 1.3–1.5 times greater in diets supplemented with chickpea Ammonia-treated barley straw and hay [11] have been husk or lablab bean husk than the control diet. These used as sources of easily digestible cellulose and/or results suggest that bean husk supplementation might im- hemicellulose. Unmolassed sugar beet pulp [12, 54], cit- prove the nutritive value of a rice straw diet by stimulating rus pulp and dried grass [12], ammonia-treated rice the growth of fibrolytic bacteria, represented by F. succino- straw [55] and soybean hull [56] are also sources of eas- genes. Regarding the use of chickpea husk, selection of ily digestible fiber. However, their properties have not cultivar may be important, because some show a higher been fully characterized, especially in relation to the acti- content of tannin (e.g. chickpea husk from western Asia) vation of fibrolytic rumen microbes. that can inhibit fibrolytic bacteria and their enzymes. It is imperative to determine whether the rumen bac- teria that are activated by supplemental fiber correspond Soybean hull to the bacteria that are responsible for main forage Soybean hull (soybean husk) is one of a number of digestion [53]; otherwise, this fiber cannot be considered popular feed ingredients that are partly interchangeable a booster of main forage degradation. In this regard, with main forages (up to 25–30% of dry matter intake) local bean husks seem ideal for the enhancement of rice for lactating dairy cows without negatively affecting fer- straw digestion, as they increased the ruminal abundance mentation, digestion or production performance [67]. of the representative fibrolytic bacterium Fibrobacter Soybean hull activated representative rumen cellulolytic succinogenes [53], whose importance in the degradation and hemicellulolytic bacteria in a pure culture study, of grass forage such as rice straw is extensively studied and growth stimulation of Prevotella ruminocola was [57–64] and widely accepted [65, 66]. Sugar beet pulp, notable after incubation with the water soluble fraction another easily digestible fiber that finds popular use in of soybean hull (Yasuda et al. unpublished results). There- several countries, was eliminated by initial screening due fore, this familiar feed should be reevaluated for its po- to its failure to activate F. succinogenes [53]. tency in activating specific but important rumen bacteria Specific activation of F. succinogenes by selected mate- and further examined to optimize its usage. Soybean hull rials (chickpea husk and lablab bean husk) was con- also has unidentified functions that can modulate hindgut firmed in a series of in situ and in vitro studies [52, 53]. microbiota and fermentation in monogastric animals. Rats Quantitative PCR indicated that these fiber sources were fed a diet containing 5% soybean hull showed higher Table 4 Stimulation of growth of representative fibrolytic rumen bacteria by bean husks a b Rumen bacterial colonization Rumen bacterial abundance c 7 7 Fiber or husk, origin H/C ratio By qPCR, × 10 /mL By clone library, % By qPCR, × 10 /mL Fs Rf Ra Fs Rf Ra Fs Rf Ra Beet pulp, Japan 1.53 0.2 5.0 0.1 - - - - - - Rice straw, Japan 0.68 747.4 36.7 19.0 3.2 0.0 0.0 30.9 1.2 0.8 Chickpea, Myanmar 0.06 476.3 72.4 7.2 6.5 0.0 3.2 229.1 1.9 0.3 Lablab bean, Myanmar 0.38 1044.0 27.5 91.6 1.4 0.0 2.8 371.5 3.2 6.0 Data are based on Fuma et al. [52] and Ngwe et al. 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Use of Asian selected agricultural byproducts to modulate rumen microbes and fermentation

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Life Sciences; Agriculture; Biotechnology; Food Science; Animal Genetics and Genomics; Animal Physiology
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Abstract

In the last five decades, attempts have been made to improve rumen fermentation and host animal nutrition through modulation of rumen microbiota. The goals have been decreasing methane production, partially inhibiting protein degradation to avoid excess release of ammonia, and activation of fiber digestion. The main approach has been the use of dietary supplements. Since growth-promoting antibiotics were banned in European countries in 2006, safer alternatives including plant-derived materials have been explored. Plant oils, their component fatty acids, plant secondary metabolites and other compounds have been studied, and many originate or are abundantly available in Asia as agricultural byproducts. In this review, the potency of selected byproducts in inhibition of methane production and protein degradation, and in stimulation of fiber degradation was described in relation to their modes of action. In particular, cashew and ginkgo byproducts containing alkylphenols to mitigate methane emission and bean husks as a source of functional fiber to boost the number of fiber-degrading bacteria were highlighted. Other byproducts influencing rumen microbiota and fermentation profile were also described. Future application of these feed and additive candidates is very dependent on a sufficient, cost-effective supply and optimal usage in feeding practice. Keywords: Agricultural byproduct, Fermentation, Fiber degradation, Methane mitigation, Microbiota, Plant secondary metabolites, Rumen Backgrounds respectively. These effects were observed after supple- The rumen is a dense and diverse microbial ecosystem, mentation with antibiotics [4] and halogenic chemicals capable of transforming fibrous plant material and non- [7], the majority of which have now fallen out of favor due protein nitrogen into valuable products, such as short to global concerns regarding food safety and environmen- chain fatty acids and microbial protein [1]. However, this tal burden. Therefore, alternative agents are required, fermentation process is accompanied by the synthesis of preferably naturally occurring materials such as plant non-beneficial products such as methane and is not resources [3, 8]. The main components, most of which are always efficient, due to the limited supply of essential plant secondary materials, have been screened out. They nutrients and/or inadequate feed formulation. Therefore, have ecological functions as chemical messengers between particular attention should be paid to dietary regimens plants and the environment, often exhibiting antimicrobial that optimize fermentation. Several dietary supplements activity [9]. Such alternatives have been actively ex- have been proposed for such a purpose [2–6], targeting plored, especially since growth-promoting antibiotics inhibition of methane and rapid ammonia release, and were banned in Europe in 2006. improvement of fiber degradation. Fiber digestion is preceded by fiber-digesting rumen Inhibition of methane production and excess ammonia microbes, mainly bacteria [10]. Therefore, preferential formation conserves dietary energy and proteins, activation of fibrolytic rumen bacteria is important. Bac- terial growth can be stimulated by vitamins, amino acids, branched chain fatty acids and other nutrients. Add- * Correspondence: kyas@anim.agr.hokudai.ac.jp Lab of Animal Function and Nutrition, Research Faculty of Agriculture, itionally, the use of easily degradable fiber as a strategy Hokkaido University, Sapporo 060-8589, Japan © The Author(s). 2016 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Kobayashi et al. Journal of Animal Science and Biotechnology (2016) 7:70 Page 2 of 10 has been known since the 1980s [11–13]. Evaluation of Indeed, Watanabe et al. [21] first indicated that unheated supplements as boosters for fiber degradation should in- CNSL dramatically reduced methane production while clude the determination of fiber digestibility as well as increasing propionate production in batch cultures. They the analysis of rumen bacterial abundance and activity. also reported that CNSL reduced methane levels in a A mechanistic understanding of expected events would rumen simulation technique (RUSITEC) fermenter, ac- confirm theoretical knowledge, making supplement use companied by drastic alterations in rumen microbiota. more acceptable to farmers. Materials that have been Quantitative polymerase chain reaction (PCR) demon- proposed in the last decade include agricultural by- strated that formate and/or hydrogen producing bacteria products deemed safe, cost-effective and easily accept- decreased in abundance, while succinate and/or propionate able among farmers and product consumers. producing bacteria increased with CNSL supplementation. This review describes selected agricultural byproducts In feeding experiments using cattle, we observed a similar that are available in the Asian region as potent feed or response to CNSL [22]; specifically, a reduction in methane additive candidates for the above purposes. Character- emission (19-38%) accompanied by alteration in the rumi- istics, actions and benefits of such agricultural bypro- nal abundance of bacterial species responsible for methane ducts are discussed from the viewpoint of modulation of and propionate production, causing a shift in hydrogen rumen microbiota and fermentation. flow [23]. However, as expected, alterations of microbiota and fermentation profile in these feeding studies were less Selected byproducts containing plant secondary pronounced than those in in vitro studies. In feeding ex- compounds as inhibitors of formation of non-beneficial periments using sheep, microbial and metabolic alterations fermentation products were also observed, although alterations in the abundance Cashew byproduct of bacterial and archaeal members in sheep rumen (Suzuki Cashew nut shell liquid (CNSL), a byproduct of cashew et al. unpublished results) were not the same as those ob- nut production that accounts for about 32% of the shell, served in cattle rumen (Su et al. unpublished results). In has many industrial applications and is used as a raw fact, in response to CNSL feeding, groups belonging to material for products such as paints, brake linings, lac- Proteobacteria, relatives of Succinivibrio and Succinimonas, quers and coatings [14]. The global production of CNSL showed increased levels in the rumen of cattle and sheep, is estimated at 450,000 metric tonnes per year [15], pro- while increases in Methanomicrobium mobile and Metha- viding a readily available supply of CNSL. Vietnam and nobrevibacter wolinii were respectively observed in the India are major CNSL-producing countries. This liquid rumen of cattle and sheep. also exhibits a wide range of biological activities, as it As CNSL administration did not adversely affect contains compounds with antimicrobial [16], antioxida- digestibility in either cattle or sheep, this agricultural tive [17] and antitumor [18] properties, represented by byproduct can be recommended for use as a potent anacardic acid, cardanol and cardol, which are all methane-inhibiting and propionate-enhancing agent, salicylic acid derivatives with a carbon-15 alkyl group. due to its effects on rumen microbiota. However, the These phenolic compounds, especially anacardic acid, long-term effects of CNSL should be evaluated for prac- are reported to inhibit a variety of bacteria [19]. Propor- tical application, as was emphasized for the ionophore tions of these alkyl phenols in CNSL vary with produ- monensin [24], which showed a reduction in efficacy cing area (cultivar) and deshelling process (heating). with increased feeding period duration. Therefore, the function of CNSL as a rumen modifier Later in vitro and in vivo studies on CNSL do not can also vary with these factors, as indicated in Tables 1 wholly support the above favorable results, due to the and 2. low level of CNSL supplementation and heat treatment An early study by Van Nevel et al. [20] first indicated for CNSL preparation (Table 1). Although CNSL supple- that anacardic acid could be used as a propionate mentation decreased methane production, inhibition enhancer in the rumen. Anacardic acid is found in was only 18% [25], while it was 57% in the similar cashew and ginkgo trees, particularly in their seeds. As batch culture system used in our study [21]. CNSL feed- cashew is the more abundant plant material, it is con- ing to dairy cows decreased methane emission by only sidered a more useful source of anacardic acid. The 8% [26]. The differences between these later results and main action of anacardic acid and related phenolics is our initial ones might be the quantity and quality of a surfactant action that inhibits mainly Gram-positive CNSL. Danielson et al. [25] tested 3 times lower supple- bacteria [16] lacking an outer membrane. Such cells mentation level of CNSL than the level examined by are physically disrupted by anacardic acid. This select- Watanabe et al. [21], and Branco et al. [26] used heat- ive inhibition of Gram-positive rumen bacteria might processed CNSL that contains cardanol as a main phen- result in the alteration of rumen microbiota and fer- olic compound instead of the most potent phenolic, mentation products. anacardic acid [27–29]. Microbial response was clearly Kobayashi et al. Journal of Animal Science and Biotechnology (2016) 7:70 Page 3 of 10 Table 1 Effect of selected agricultural byproducts containing anacardic acid and other phenolics on dry matter (DM) digestibility and rumen fermentation parameters Byproduct, origin Description Phenolics, % in weight Reference Test by Dosed at DM digestibility, % Total VFA, Inhibition, % Reference mmol/dL Anacardic acid Caldanol Caldol Methane Ammonia Cashew shell, India Heated - 71.4 14.4 [21] Batch culture 0.5 mg/mL - ns 9.2 - [21] Raw 57.7 8.2 19.9 ibid. ibid - ns 56.9 - ibid. Raw ibid. ibid. ibid. ibid. RUSITEC 0.2 mg/mL ↑ ns 70.1 16.5 ibid. Raw ibid. ibid. ibid. ibid. Feeding (dry cow) 0.32% of DMI ns ns 19.3–38.3 ns [22] Raw ibid. ibid. ibid. ibid. Feeding (milking cow) ibid. ns ns 12.7 ns Shinkai et al. unpublished Raw ibid. ibid. ibid. ibid. Feeding (sheep) ibid. ns ns 61.4 43.0 Suzuki et al. unpublished Cashew shell, Tanzania Raw - - - [25] Batch culture 0.17 mg/mL - ns 17.8 - [25] Cashew shell, Brazil Heated - 62.9 13.4 [26] Feeding (milking cow) 0.11% of DMI ns - 8.0 - [26] Raw 64.9 1.2 13.3 [29] Cashew shell, Brazil Heated - 73.3 19.4 [28] Feeding (milking cow) 0.036% of DMI ns - - - [28] Raw 49.3 30.5 20.2 [27] Ginkgo fruit, Japan Cultivar A 85.0 2.3 12.7 Oh et al. Batch culture 3.2 mg/mL - ns 85.7 42.0 Oh et al. unpublished Cultivar B 86.8 2.3 10.9 unpublished ibid. 4.5 mg/mL - ns 65.9 46.0 ibid. RUSITEC 3.2 mg/mL ns ns 47.3 53.7 ibid. Ginkgo leaf, Korea Unspecified - - - Batch 1.0 mg/mL ns ns 46.7 - [30] -, No data available ns, Not significantly changed ↑, Significantly increased Calculated on basis of CH4 ml for in vitro test and of CH4 g/kg DMI for in vivo test, respectively Heat was used in deshelling process g of extract/mL (not calculable as original leaf) Kobayashi et al. Journal of Animal Science and Biotechnology (2016) 7:70 Page 4 of 10 Table 2 Effect of selected agricultural byproducts containing anacardic acid and other phenolics on rumen microbial abundance determined by quantitative PCR Byproduct Main compound Tested by Dosed at Abundance of rumen microbe, relative % to total bacteria Reference involved Pro Meth Fu Fs Rf Ra Me Sr Sd Tb Sb Pr Pb Rm Al Cashew shell Anacardic acid RUSITEC 0.2 mg/mL ↓ ns - ↓↓ ns ↑↑ ↑ ↓ ns ↓↓ ns ↑ [21] Feeding (dry cow) 0.32% of DMI ns ns - ns ↓↓ - ↑↑ ↓ - ↑ -- ↑ [22] Feeding (milking cow) 0.33% of DMI - ns ns ↓ ns ns ns ns ns ns ns ns ns ns ns Shinkai et al. unpublished Feeding (sheep) 0.32% of DMI ↓ - - ns ns ns ns ns ns ns ns ns ns ns ns Suzuki et al. unpublished Ginkgo fruit Anacardic acid Batch culture, culivar A 3.2 mg/mL - ↑ -ns ns ns ↑↑ ↑ ↓ ↑ ns ↑ ns ns Oh et al. unpublished Batch culture, cultivar B 4.5 mg/mL - ↑ -ns ns ns ns ns ↓ ns ↑ ns ↑ ns ↓ ibid. RUSITEC, cultivar A 3.2 mg/mL ↓↓ ↓ ↓ ↓ ↓ ↑ ↑ ↑ ↓ ns ↑↓ ↑ ↑ ibid. Ginkgo leaf Unspecified Batch culture 1.0 mg/mL ↓↑ - ↑↓ ↓ - - - --- - - - [30] Pro protozoa, Meth methanogen, Fu fungi, Fs Fibrobacter succinogenes,Rf Ruminococcus flavefaciens,Ra Ruminococcus albus,Me Megasphaera elsdenii,Sr Selenomonas ruminantium,Sd Succinovibrio dextrinosolvens,Tb Treponema bryantii,Sb Streptococcus bovis,Pr Prevotella ruminicola,Pb Prevotella bryantii,Rm Ruminobacter amylophilus,Al Anaerovibrio lipolytica -, No data available ns, Not significantly changed ↑, Significantly increased ↓, Significantly decreased Value were obtained by direct counting g of extract/mL (not calculable as original leaf) Kobayashi et al. Journal of Animal Science and Biotechnology (2016) 7:70 Page 5 of 10 different between these studies. Our MiSeq data in our Both CNSL [21] and ginkgo fruit extract (Oh et al. RUSITEC study demonstrated drastic alteration of mi- unpublished results) decrease ammonia concentration in crobial community structures: for eubacteria, a higher RUSITEC. Since both inhibit the growth of proteolytic, detection frequency of Veillonellaceae and Succinivibrio- peptidolytic and deaminating rumen bacteria in pure cul- naceae and lower frequency of the Ruminococcaceae, ture, feeding of these extracts may spare dietary protein, and for archaea, a higher frequency of Methanomicro- peptide and amino acid. In fact, the growth of hyper biaceae and lower frequency of Methanobacteriaceae ammonia-producing rumen bacteria was markedly inhib- (Kobayashi et al. unpublished results). Therefore, this ited by either the form of anacardic acid contained in cashew byproduct should be used in unheated form at an CNSL or ginkgo fruit extract (Oh et al. unpublished re- optimized supplementation level. Of alkylphenols present sults). Manipulation of protein and amino acid degradation in CNSL, anacardic acid is most functional but decarboxy- is important, because excreted ammonia could be the lated and converted to caldanol by heating and long ex- source of nitrous oxide, which has much higher potential posure to oxygen. Therefore, preparation and storage of for global warming than methane. Also, decreased ammo- CNSL are important to maintain its functionality. nia level in the rumen, but not lower than 5 mgN/dL to Recently, we found that CNSL feeding improved anti- ensure microbial protein synthesis [32], may improve feed oxidative status in cattle, causing higher free radical nitrogen economy. Since ginkgo fruit has not been tested scavenging activity and lower lipid peroxidation products in a feeding study, in vivo evaluation is to be made on in the rumen and blood serum (Konda et al. unpublished rumen and animal responses including palatability of the results). Although the mechanisms involved in these diet to which ginkgo fruit is supplemented. changes are not yet clear, anacardic acid possessing anti- oxidative activity [17], can affect theses parameters dir- Tea byproduct ectly and/or indirectly through alteration of rumen China is one of the biggest tea producers globally. Tea microbiota and their fermentation products. seed meal after oil extraction has previously been con- sidered worthless. However, saponins contained in the Ginkgo byproduct tea seed meal have been found to exert beneficial anti- Another source of anacardic acid is the ginkgo plant, protozoal and antimethanogenic effects through surfac- grown widely among Far-East countries such as China, tant action [33]. Significance of tea saponins and other Korea and Japan. Industrial uses of ginkgo are its leaves source plants such as yucca and quillaja for the use of for medicinal use (China) and its nuts for food (Japan). ruminant feed has been demonstrated [33, 34]. Table 3 Leaf extracts for medicinal use are even exported to shows functionality of saponins of tea seed, tea seed European countries and also evaluated as a rumen modi- meal and other source plants (Thai blueberry, fenugreek, fier [30]. Ginkgo fruit is a byproduct in the process of and mangosteen). A series of studies on tea seed sapo- ginkgo nut separation (unsuitable for human food use nins revealed that the addition of tea seed saponins to in due to its peculiar smell), yielding ca. 2,600 metric vitro cultures killed up to 79 % of protozoa. Moreover, t/yr in Japan, accounted for 230% of nut production in vivo experiments (feeding of tea seed saponin to [31]. Therefore, biomass of ginkgo fruit is much lambs at 3 g/d) showed that the relative number of smaller in comparison with CNSL. In this regard, use for rumen protozoa to rumen bacteria was reduced by 41% feed additive might be limited locally. after 72 d of tea saponin administration [35]. Using de- The main phenolic of ginkgo is anacardic acid, but it naturing gradient gel electrophoresis (DGGE) analysis, a has different alkyl groups in comparison with those of significantly lower diversity in protozoa was reported cashew (C13:0, C15:1 and C17:1 for ginkgo vs. C15:1, [36], indicating that the antiprotozoal activity of tea sapo- C15:2 and C15:3 for cashew). An in vitro evaluation of nins might not be transient. Although an exception was ginkgo fruit extract as a rumen modifier using batch and observed by Ramirez-Restrepo [37], negative effect of tea RUSITEC systems showed that the extract decreased saponins on rumen protozoa is consistent regardless of in methane production in a dose-dependent manner and vitro and in vivo conditions, and considered as one of microbial responses were similar to those observed for main factors to modulate rumen fermentation in relation CNSL (Tables 1 and 2), though such potency depends to bacterial and archaeal changes as discussed below. on the cultivar (Oh et al. unpublished results). The most The effect of tea saponins on the ruminal abundance potent phenolic for bacterial selection was anacardic of methanogenic archaea was not significant, while they acid, in particular monoenoic (15:1) anacardic acid. Our drastically decreased the expression of the methyl coen- MiSeq data suggest that ginkgo fruit extract greatly zyme M reductase gene (mcrA) in the rumen [38]. This modulates the microbiota of RUSITEC (Oh et al. unpub- suggests that selective inhibition of methanogens might lished results) similarly to what was found for CNSL be involved in the antiprotozoal action. Using defau- supplementation. nated and refaunated sheep, Zhou et al. [36] showed that Kobayashi et al. Journal of Animal Science and Biotechnology (2016) 7:70 Page 6 of 10 Table 3 Effect of selected agricultural byproducts containing saponins and other phenolics on dry matter (DM) digestibility, rumen fermentation parameters and microbial abundance Byproduct Main compounds Tested by Dosed at DM digestibility, % Total VFA, Inhibition, % Abundance, relative % Reference involved mmol/dL Methane Ammonia Protozoa Meth Fungi Fs Rf Ra Tea seed/seed meal Saponins Batch culture 0.4 mg/mL - ns 8.0 - 51.3 ns ↓↑ ns - [38] Feeding (sheep) 3 g/d - ns 10.6 13.2 43.2 ns ns ↓ ns ns [36] Feeding (steer) 0.24–0.38% of DMI - ns 15.6 - ns ns - ↑↓ ↑ [37] Feeding (growing lamb) 0.41% of DMI - ↑ 27.5 ns 41.1 ns ns - ns ns [35] Thai bllueberry seed Saponins Feeding (goat) 0.8–24% of DMI ns ns 2.2–8.0 ns ns - - - - - [46] Fenugreek seed Saponins Batch culture 0.14–0.29 mg/mL - ns 1.8–2.0 - 15.0–39.0 ↓↓ ↑ ↑ -[41] Mangosteen peel Saponins, tannins Feeding (dairy cow) 100–300 g/d - - 5.5–13.8 - 20.5–47.1 ↓ ns ns ns ns [47] Eucarypus leaf meal Cineol, cryptone etc. Feeding (swamp buffalo) 0.7–2.0% of DMI ns ↑ 8.4–13.9 12.7–33.9 5.5–22.0 - - - - - {51} Meth methanogen, Fs Fibrobacter succinogenes,Rf Ruminococcus flavefaciens,Ra Ruminococcus albus -, No data available ns, Not significantly changed ↑, Significantly increased ↓, Significantly decreased Dosage could not be expressed as % of dry matter intake (DMI) due to lack of data on feed intake Kobayashi et al. Journal of Animal Science and Biotechnology (2016) 7:70 Page 7 of 10 tea saponins reduce methane production by inhibiting fatty acid production toward more propionate and less protozoa, most likely in coordination with their suppres- acetate and butyrate. Methane production linearly de- sive effects on protozoa-associated methanogens. Indeed, creased (up to 8%) and nitrogen retention linearly in- the presence and functional significance of protozoa- creased (up to 45%) with seed meal supplementation associated methanogens has been demonstrated [39, 40]. level. Therefore, this byproduct might be an effective Saponins alter rumen microbial community with a de- modulator of rumen fermentation and ruminant nutri- crease in protozoa and fungi and increase in Fibrobacter tion, though the mechanisms involved are not clear. succinogenes [38, 41]. The latter can compensate for Feeding of mangosteen peel powder to lactating cows fiber digestion possibly depressed by the decreased num- (300 g/d) can decrease methane production by 14% with ber of fungi, leading to a fermentation change toward a drastic decrease of rumen protozoa, while other repre- less methane and more propionate, since protozoa and sentative rumen microbes are not affected [47]. Since fungi produce hydrogen, while F. succinogenes produces mangosteen contains not only saponins but also con- succinate as a propionate precursor. Recently, Belanche densed tannins, microbial and fermentation changes et al. [42] reported decreased diversity in the archaeal might be due to these two secondary metabolites. community by supplementation with ivy fruit saponins Polyphenols in chickpea husk (abundantly available in in RUSITEC fermenter: Methanomassilicocaaceae is southern and western Asia) exert antibacterial activity substituted by Methanobrevibacter, a theoretically less against mainly Gram-positive bacteria [48]. Rats fed chick- active community member even though it is predomin- pea husk at 5% level showed an altered hindgut bacterial ant in the rumen [43]. From these reports, it is apparent community based on different DGGE banding patterns that the mechanism involved in the modulation of [49]. The authors also found that chickpea husk extract rumen fermentation by saponins remains to be fully exhibited anti-oxidative activity measured as free radical characterized. Ruminal responses could differ depending scavenging activity and lipid peroxidation. In fact, rats fed on saponins that occur in a number of plants and com- chickpea husk had lower thiobarbituric acid reactive sub- prise a variety of molecules. Tea saponins are, as indi- stance (TBARS) values in their blood plasma, suggesting cated by a review article [34], one of the promising the potency of this byproduct as a health-promoting agent rumen modifier without negative influence on feed in- in animals [49]. These favorable effects of chickpea husk take and digestibility if supplemented properly (3–5 g/d are considered to be due to the presence of tannins that for goats and lambs). could have different impact depending on molecular spe- Tea byproducts also contain catechin that can increase cies (i.e. source plants, cultivars and growing region) [50]. the proportion of unsaturated fatty acids in goat meat Asia is the origin of many plants that are sources of [44], presumably through alterations in the rumen essential oils. As a byproduct of essential oil, leaf meal of microbiota. Another beneficial action of tea catechin is Eucalyptus camaldulensis is paid attention due to the to improve antioxidant status of beef, once the catechins ability to decrease rumen ammonia level (by 34%) when are ingested and absorbed by the animal. This was spec- fed to swamp buffaloes (120 g/d) possibly through the ulated by direct addition of tea catechins to beef [45]. action of 1,8-cineol [51]. Therefore, it is proposed as an- other possible manipulator of protein and amino acid Other byproducts degradation in the rumen, which might save feed nitro- Other materials potentially modulating rumen fermenta- gen. Since essential oils are generally expensive, their tion are also shown in Table 3. Fenugreek is cultivated byproducts (residue of oil extraction) such as the above in western and southern Asian regions, where it is used leaf meal is one option recommended for practical use. as a spice, seasoning, fragrance in the form of sprouts, New additive candidates from Asian agricultural and is also known as a source of saponins. Fenugreek byproducts have been explored for the use to decrease seed extract rich in saponin (0.29 mg/mL of diluted rumen methane and ammonia, in which in vitro evalu- rumen fluid) inhibits growth of protozoa and fungi and ation is often used for initial screening. This evaluation increases growth of fibrolytic bacteria, leading to 2% de- is quick, quantitative, and very useful to define mecha- crease of methane production in vitro [41], awaiting a nisms involved in the efficacy of candidate material. feeding assessment. However, as in vitro effect is always higher than in vivo The seeds of Thai blueberry, Antidesma thwaitesia- effect, final recommendation is to be made after detailed num Muell. Arg., containing condensed tannin, were evaluation by a series of feeding studies. evaluated as a ruminant feed [46]; goats fed the diet with this meal from the wine and juice industry (inclusion of Easily digestible fibers as boosters of fiber degraders 0.8–2.4% in DM) did not show any differences in feed Chickpea and lablab bean husks intake, digestibility, ruminal pH or ammonia-nitrogen, Fibers are not always efficiently degraded in the rumen while they showed a dose-dependent shift in short chain due to complexity of fiber structure and components Kobayashi et al. Journal of Animal Science and Biotechnology (2016) 7:70 Page 8 of 10 and less well optimized rumen microbiota. Recently, heavily colonized by F. succinogenes. Pure cultures of some easily degradable fibers have been proposed to several different strains of F. succinogenes revealed modulate rumen microbiota toward quick optimization growth stimulation after addition of the bean husks as of developing fiber-degrading consortia [52]. We have the sole carbon substrate. found that husks from a few species of local beans Finally, a digestion trial, in which each type of husk was (chickpea and lablab bean) show high potency in im- supplemented at 10%, was employed to evaluate them as proving rumen fermentation [52, 53]. The functionality digestion boosters for a rice straw-based diet [53]. The of these husks is summarized in Table 4. These fiber digestibility of acid detergent fiber was 3.1–5.5% greater in sources are considered a replaceable fibrous feed, as well diets supplemented with chickpea husk or lablab bean as a booster of the degradation of the main forage. In- husk than in the control. Total short chain fatty acid levels deed, these fiber sources can be characterized as easily were higher in sheep fed lablab bean husk-supplemented digestible [11, 12]. diet than in sheep fed other diets, while acetate levels were Easily digestible fiber sources might promote the rapid higher in lablab bean husk-supplemented diet than in the growth of fibrolytic microbial biomass, which in turn fa- control diet. Ruminal abundance of F. succinogenes was cilitates the digestion of the other fiber in the rumen. 1.3–1.5 times greater in diets supplemented with chickpea Ammonia-treated barley straw and hay [11] have been husk or lablab bean husk than the control diet. These used as sources of easily digestible cellulose and/or results suggest that bean husk supplementation might im- hemicellulose. Unmolassed sugar beet pulp [12, 54], cit- prove the nutritive value of a rice straw diet by stimulating rus pulp and dried grass [12], ammonia-treated rice the growth of fibrolytic bacteria, represented by F. succino- straw [55] and soybean hull [56] are also sources of eas- genes. Regarding the use of chickpea husk, selection of ily digestible fiber. However, their properties have not cultivar may be important, because some show a higher been fully characterized, especially in relation to the acti- content of tannin (e.g. chickpea husk from western Asia) vation of fibrolytic rumen microbes. that can inhibit fibrolytic bacteria and their enzymes. It is imperative to determine whether the rumen bac- teria that are activated by supplemental fiber correspond Soybean hull to the bacteria that are responsible for main forage Soybean hull (soybean husk) is one of a number of digestion [53]; otherwise, this fiber cannot be considered popular feed ingredients that are partly interchangeable a booster of main forage degradation. In this regard, with main forages (up to 25–30% of dry matter intake) local bean husks seem ideal for the enhancement of rice for lactating dairy cows without negatively affecting fer- straw digestion, as they increased the ruminal abundance mentation, digestion or production performance [67]. of the representative fibrolytic bacterium Fibrobacter Soybean hull activated representative rumen cellulolytic succinogenes [53], whose importance in the degradation and hemicellulolytic bacteria in a pure culture study, of grass forage such as rice straw is extensively studied and growth stimulation of Prevotella ruminocola was [57–64] and widely accepted [65, 66]. Sugar beet pulp, notable after incubation with the water soluble fraction another easily digestible fiber that finds popular use in of soybean hull (Yasuda et al. unpublished results). There- several countries, was eliminated by initial screening due fore, this familiar feed should be reevaluated for its po- to its failure to activate F. succinogenes [53]. tency in activating specific but important rumen bacteria Specific activation of F. succinogenes by selected mate- and further examined to optimize its usage. Soybean hull rials (chickpea husk and lablab bean husk) was con- also has unidentified functions that can modulate hindgut firmed in a series of in situ and in vitro studies [52, 53]. microbiota and fermentation in monogastric animals. Rats Quantitative PCR indicated that these fiber sources were fed a diet containing 5% soybean hull showed higher Table 4 Stimulation of growth of representative fibrolytic rumen bacteria by bean husks a b Rumen bacterial colonization Rumen bacterial abundance c 7 7 Fiber or husk, origin H/C ratio By qPCR, × 10 /mL By clone library, % By qPCR, × 10 /mL Fs Rf Ra Fs Rf Ra Fs Rf Ra Beet pulp, Japan 1.53 0.2 5.0 0.1 - - - - - - Rice straw, Japan 0.68 747.4 36.7 19.0 3.2 0.0 0.0 30.9 1.2 0.8 Chickpea, Myanmar 0.06 476.3 72.4 7.2 6.5 0.0 3.2 229.1 1.9 0.3 Lablab bean, Myanmar 0.38 1044.0 27.5 91.6 1.4 0.0 2.8 371.5 3.2 6.0 Data are based on Fuma et al. [52] and Ngwe et al. 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Journal of Animal Science and Biotechnology – Springer Journals

Published: Dec 15, 2016

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