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Effects of a twin strain of Saccharomyces cerevisiae live cells on mixed ruminal microorganism fermentation in vitro¹

Z. A. Lila^*, N. Mohammed^*, T. Yasui, Y. Kurokawa^*, S. Kanda^* and H. Itabashi^*,2

^* Faculty of Agriculture, Tokyo University of Agriculture and Technology, Tokyo, Japan, and and Research and Development Department, Bussan Biotech Co., Ltd., Tokyo, Japan

Abstract

This experiment was designed to investigate the effects of different concentrations (0, 0.33, 0.66, 0.99, and 1.32 g/L) of a twin-strain of Saccharomyces cerevisiae live cells on in vitro mixed ruminal microorganism fermentation of corn starch, soluble potato starch, and sudangrass hay (60.5%, DM basis) plus concentrate mixture (39.5%, DM basis). Ruminal fluid was collected from two dairy cows, mixed with phosphate buffer (1:2), and incubated (30 mL) anaerobically at 38°C for 6 and 24 h with or without yeast supplement, using 200 mg (DM basis) of each substrate. Medium pH, ammonia-N, and numbers of protozoa were unaffected (P = 0.38) by yeast cells in all substrates. Molar proportion of acetate was unchanged (P = 0.56) with cornstarch and soluble potato starch, but increased quadratically (P = 0.02) with hay plus concentrate by treatment. Addition of yeast cells caused a linear increase of total VFA (P = 0.008) in all substrates. Excluding the soluble potato starch, supplementation of S. cerevisiae resulted in a quadratic increase of propionate (P = 0.01), with a quadratic decrease (P = 0.04) of acetate:propionate. When soluble potato starch was used as a substrate, a linear increase (P = 0.006) of the molar proportion of propionate and a quadratic decrease (P = 0.007) in acetate:propionate was observed by treatment. Molar proportion of butyrate was unchanged (P = 0.35) with cornstarch and soluble potato starch, whereas it decreased linearly (P = 0.007) with hay plus concentrate by yeast cell supplementation. When cornstarch and soluble potato starch were used as a substrate, minor VFA were decreased (P = 0.05) by treatment. Accumulation of lactate was linearly decreased by treatment (P = 0.007) in all substrates. During incubation with hay plus concentrate, IVDMD was linearly increased (P = 0.006), whereas production of methane (linear; P = 0.02) and accumulation of hydrogen was decreased (quadratic; P = 0.005) by treatment after 24 h. These results showed that a twin strain of S. cerevisiae live cells stimulated in vitro mixed ruminal microorganism fermentation with decreased lactate, and a small decrease of methane and hydrogen with hay plus concentrate.

Key Words: Methane • Probiotics • Protozoa • Ruminal Fermentation • Twin Strain of Saccharomyces cerevisiae

Introduction

Based on growing concern over the use of antibiotics and other growth promoters in the animal feed industry, interest in the effects of microbial feed additives on animal performance has increased. Some of the benefits associated with Saccharomyces cerevisiae include increased DM and NDF digestion (Williams et al., 1991; Carro et al., 1992) and milk production (Williams et al., 1991; Piva et al., 1993; Kung et al., 1997). Yeast cultures also have been shown to stimulate utilization of hydrogen by ruminal acetogenic bacteria (Chaucheyras et al., 1995). Wallace and Newbold (1992) reported that the responses of yeast culture are highly variable and apparently influenced by the composition of the diet.

Saccharomyces cerevisiae (Yea-Sacc 1026; Alltech Biotechnology Center, Nicholasville, KY) increased the number of ruminal total bacteria and cellulolytic bacteria (Newbold et al., 1995), increased the proportion of propionate (Mutsvangwa et al., 1992; Newbold et al., 1995), and decreased lactate concentration (Newbold et al., 1990). Another S. cerevisiae culture (Diamond V XP; Diamond V Mills, Inc., Indianapolis, IN) stimulated the growth of the cellulolytic bacteria, Fibrobacter succinogenes and Ruminococcus albus (Nisbet and Martin, 1991; Callaway and Martin, 1997), and increased the proportion of propionate (Sullivan and Martin, 1999) and lactate uptake by Selenomonas ruminantium (Martin and Nisbet, 1992). Recently, Lynch and Martin (2002) reported that the Diamond V XP yeast culture and live cells of S. cerevisiae (PMX70SBK; Saf Agri, Indianapolis, IN) did not affect propionate concentration, whereas lactate concentration decreased with S. cerevisiae live cells. This study was conducted to evaluate the effects of a twin strain of S. cerevisiae live cells (Yea-Sacc Twin Strain 8417 and 1026) on in vitro mixed ruminal microorganism fermentation of ground corn, soluble potato starch, and sudangrass hay plus concentrate.

Materials and Methods

Substrates and Additives
Soluble potato starch and cornstarch (Wako Pure Chemical Industries, Ltd., Tokyo, Japan), and sudangrass hay plus concentrate (1.5:1) mixture were used as substrates on a DM basis for in vitro incubation. Live S. cerevisiae cells (Yea-Sacc Twin Strain 8417 and 1026 [YST], Bussan Biotech Co. Ltd. Tokyo, Japan) were used as a probiotics, and contained 5 x 10⁹ live organisms/g, plus the carrier (medium) on which it was grown. The carrier contained 28% CP, 14% crude fiber, 6% crude fat, and 8% ash (DM basis). The sudangrass hay plus concentrate mixture was ground in a high-speed grinder (Retsch ZM 100, Haan, Germany) to pass through a 1-mm screen. The chemical composition of the sudangrass hay and concentrate mixture is shown in Table 1.

Determination of the Number of Total Viable Counts and Cellulolytic Bacteria
After 24 h of incubation, a 1-mL sample was collected, and serial 10-fold dilutions in an anaerobic mineral solution (Bryant and Burkey, 1953) were prepared. The Hungate (1969) anaerobic technique was used to prepare media and to cultivate microorganisms. Total viable counts were determined in roll-tubes (triplicate) with the complete medium described by Leedle and Hespell (1980). Cellulolytic bacteria were cultivated in Halliwell and Bryant (1953) medium. Dilutions of 10⁶ to 10⁹ were used to cultivate total viable bacteria and cellulolytic bacteria. One milliliter of diluted sample from each tube was used to inoculate 5 mL of culture media in Hungate tubes. Counts (five tubes for each dilution) were estimated by the most probable number method (Alexander, 1982). The existence of cellulolytic bacteria was assumed by the degradation of a filter paper strip (qualitative filter paper No. 1, ashless; Toyo Roshi Kaisha, Ltd., Tokyo; Morvan et al., 1996).

Analyses
At the end of incubation, total gas was measured by insertion of the glass syringe needle through the butyl rubber stopper, and a volume of gas exceeding 1 atmospheric pressure was measured through the displacement of the syringe plunger (Callaway and Martin, 1996). The gas was injected back into the serum bottle, and a 0.5-mL sample of gas was removed from each bottle with a gas-tight syringe, and methane and hydrogen were measured by a gas chromatograph (model GC-8A, Shimadzu Co., Ltd., Kyoto, Japan) using a molecular sieve 5A column (1.6 m x 3.2 mm i.d., 60 to 80 mesh, Shinwakako, Kyoto, Japan) and thermal conductivity detector (column temperature = 60°C, injector and detector temperature = 80°C). The carrier gas (Ar) flow rate was 50 mL/min. The bottles were uncapped, and pH was immediately determined in the culture fluid with a portable pH meter (ATC pH meter Piccolo2, Hannah Instruments, Arvore-Vila do Conde, Portugal). One milliliter of the incubated fluid was diluted with 4 mL of methylgreen-formalin-saline (formalin, 100 mL; NaCl, 8.5 g; methyl green, 0.3 g; and distilled H₂O, 900 mL), and protozoa were counted using a Fuchs-Rosenthal counting chamber as described previously (Ogimoto and Imai, 1981). For analysis of ammonia-N and VFA, 1 mL of 25% meta-phosphoric acid (wt/vol) was added to 5 mL of fermentation fluid, and stored at –30°C until analyzed. One milliliter of thawed fermentation fluid was centrifuged (10,000 x g for 10 min at 4°C), and VFA were analyzed by gas chromatography (model GC-14B, Shimadzu Co. Ltd.) using a Thermon-3000 5% Shincarbon A column (1.6 m x 3.2 mm i.d., 60 to 80 mesh, Shinwakako) and a flame ionization detector (column temperature = 130°C, injector and detector temperature = 200°C). The carrier gas (N₂) flow rate was 50 mL/min. Ammonia-N was determined by a microdiffusion method (Conway, 1962). One milliliter of thawed sample was centrifuged (27,000 x g for 20 min at 4°C), filtered (0.45 µm pore size), and the lactic acid was analyzed by HPLC (Shimadzu Co. Ltd.) using a Shodex Rspak KC-811 column (8 mm i.d. x 300 mm length; Showa Denko, Tokyo, Japan). The mobile phase used for isocratic elution was 3 mM HClO₄. The flow-rate was 1.0 mL/min, column temperature was 50°C, and the monitoring wavelength was 210 nm, with a UV absorbance detector. To determine IVDMD, the bottles’ contents were transferred into a tube and centrifuged at 11, 000 xg for 15 min at 4°C after 24 h incubation. The supernatants were passed through a filter paper (qualitative filter paper No. 1, ashless; Tokyo Roshi Kaisha Ltd., Tokyo, Japan), washed twice with distilled water and once with acetone, and then dried to a constant weight at 105°C. The IVDMD was calculated as the original weight of hay plus concentrate DM (added in each incubation) minus dry residue weight (after incubation) divided by the original sample weight. These values were then multiplied by 100 to derive the percentage of IVDMD.

Statistical Analyses
Data were analyzed using the GLM procedure of SAS (SAS Inst., Inc. Cary, NC). The statistical model included the fixed effects of treatment, replication (day), the interaction of treatment x day and the time effect. The model as fitted was as follows:

where y_ijk = the dependent variable, m = overall mean, T_i = treatment effect (i = 1, ..., 5), R_j = replication effect (j = 1,2,3), TR_ij = interaction effect, e_ij = random residual error, and H_k = time effect (k = 1, 2). Total viable bacteria, cellulolytic bacteria, protozoa, and concentration of lactate were analyzed using the following model:

where m, T, and R are as defined above. Linear and quadratic contrasts examined the effect of increasing YST concentration. Data are presented as least squares means, and the contrast P-values are the observed significance levels and are considered statistically different when P < 0.05. Differences of P < 0.15 to P < 0.05 are discussed as trends.

Results

In the absence of added substrates, YST had no effect on medium pH, ammonia-N, minor VFA, protozoa, hydrogen, and methane (Table 2). The concentration of total VFA in the medium and the concentration CH₄ in the total gas fluctuated with time (P = 0.03). Total VFA was linearly increased (P = 0.04) by YST. Molar proportion of acetate tended to decrease (P = 0.07) quadratically, whereas the proportion of propionate increased (P = 0.05) linearly, and the proportion of butyrate tended to be increase linearly (P = 0.08) with YST. Total gas production tended to increase (P = 0.08) quadratically with YST.

No effect of yeast treatment on pH was observed in this experiment. In vitro and in vivo effects of S. cerevisiae on ruminal pH has been varied. Results of in vitro studies suggested that Yea-Sacc 1026 strain (25 g/kg of diet; Newbold et al., 1995) and Diamond V XP yeast culture (0.35 to 0.73 g/L; Sullivan and Martin, 1999; Lynch and Martin, 2002) did not modify mean pH. In contrast, Williams et al. (1991) reported that S. cerevisiae NCYC 1026 (10 g/d; Nutfield, Surrey, U.K.) also decreased the individual variability of pH in dairy cows fed energy-rich diets. Martin and Nisbet (1992) reported that the utilization of lactic acid by ruminal bacteria S. ruminantium was enhanced by Diamond V XP yeast culture, thereby maintaining a constant pH. Ammonia-N concentration was not modified by the addition of YST, which was similar to the results of Yea-Sacc 1026 in vitro (Newbold et al., 1995). In an in vivo study, Chademana and Offer (1990) and Newbold et al. (1995) reported that Yea-Sacc 1026 did not affect ruminal ammonia-N concentration in sheep fed the supplement at 4 g/d and 1.3 g/kg of diet, respectively. Erasmus et al. (1992) and Mutsvangwa et al. (1992) found a similar effect in lactating dairy cows (10 g/d) and in bulls (8 to 10 g/d). Decrease of lactate concentration with YST is consistent with the results of Yea-Sacc 1026 in sheep (4 g/d; Newbold et al., 1990). Other yeast culture (Diamond V XP) also decreased the lactate concentration in vitro (Callaway and Martin, 1997; Sullivan and Martin, 1999). Total gas was increased with YST; this may have resulted from the increased production of propionate because carbon dioxide is produced when propionate is made by some ruminal bacteria via the succinate:propionate pathway (Wolin and Miller, 1988). Ciliate protozoa were composed of Entodinium spp., Dasytricha sp., and Isotricha sp. The total number and composition of protozoa were not affected by treatment. Few experiments have dealt with the effect of direct-fed microbials on the protozoa population. Kumar et al. (1994) and Newbold et al. (1995) reported that S. cerevisiae did not modify protozoa in buffalo and in sheep, respectively. In contrast, Plata et al. (1994) reported that supplementation of S. cerevisiae in steers (10 g/d) resulted in an increase in the number of total protozoa.

Other major effects of YST on ruminal fermentation included increased concentrations of propionate and total VFA. Published reports of the effect of yeast culture on concentrations of VFA are variable. Chademana and Offer (1990) reported that Yea-Sacc 1026 had no effect on total VFA or VFA composition, but others found stimulation in the proportion of propionate at the expense of acetate (Newbold et al., 1990) or even an increase in the proportion of acetate (Mutsvangwa et al., 1992). Supplementation of other yeast cultures (Diamond V XP) to lactating dairy cows (114 g/d; Harrison et al., 1988) and steers (14.8 g/d; Adams et al., 1981) also increased the proportion of propionate, whereas proportions of acetate and isovalerate and acetate:propionate ratios were lower. In view of the variability in the response of ruminal VFA concentrations to yeast culture, Wallace and Newbold (1992) concluded that it was unlikely that the production benefits seen when yeast culture is added to the diet arise from changes in the stoichiometry of VFA formation.

The IVDMD of hay plus concentrate was increased with YST. In vivo studies reported that supplementation of Yea-Sacc 1026 did not affect the apparent digestibility of DM, OM, NDF, and CP of hay plus concentrate at different ratios, but did tend to be higher with the control diet (Chademana and Offer, 1990). Previous studies (Dowson, 1990; Williams et al., 1991) have reported that the stimulation of cellulose degradation by yeast culture is associated with a decreased lag time, which results in increased initial rates of digestion, but not in increased extent of digestion by ruminal microorganisms. Williams et al. (1991) reported that yeast culture stimulated DM digestion in the rumen of hay-fed steers when barley was absent. They attributed this difference to a stabilization of ruminal pH by yeast culture in animals receiving barley. In a subsequent study, Newbold et al. (1995) reported that some yeast cultures increased the number of total and cellulolytic bacteria in the rumen and, in some cases, increased cellulose degradation. They also suggested that S. cerevisiae culture stimulated the rate rather than the extent of fiber digestion by ruminal microorganisms. In a later experiment, Callaway and Martin (1997) reported that Diamond V XP yeast culture filtrate increased cellulose disappearance as much as 11% after 24 h of incubation, but no change in cellulose disappearance was found after 48 or 72 h when incubated with predominant ruminal bacteria F. succinogenes and R. flavefaciens. They concluded that the S. cerevisiae culture filtrate stimulated the initial rate of cellulose degradation by these two predominant cellulolytic bacteria without influencing the extent of degradation.

In the present study, YST also increased the numbers of total viable bacteria and cellulolytic bacteria. Newbold et al. (1995) reported that Yea-Sacc 1026 increased the numbers of total viable bacteria and cellulolytic bacteria both in vitro and in vivo studies. Increased bacterial numbers in the rumen have been one of the most consistently reported effects in animals fed another yeast culture, Diamond V XP (Wiedmeier et al., 1987; Harrison et al., 1988). It has been suggested that increased bacterial flora in animals fed S. cerevisiae is central to the action of yeast in the rumen, and increased bacterial population leads to an increase in both the degradation of fiber in the rumen and the flow of microbial protein from the rumen (Wallace and Newbold, 1992). The increase in bacterial numbers in our study with cornstarch and soluble potato starch was relatively small compared with hay plus concentrate, which might have been the result of the induction of cellulolytic bacteria growth in the presence of forage.

In the presence of ground corn and soluble potato starch, YST had no effect on the concentration of hydrogen and methane. But after 24 h of incubation with hay plus concentrate, there was a small decrease in methane with increasing concentration of YST. Methane production was also decreased by Yea-Sacc 1026 in vitro (Mutsvangwa et al., 1992). Recent research reported that the live cells of S. cerevisiae (PMX70SBK; Saf Agri) decreased methane significantly from alfalfa hay (Lynch and Martin, 2002). The decrease in methane production may be due to the utilization of metabolic hydrogen by acetogenic bacteria to produce acetate in the present study. Coculture of S. cerevisiae strain (CNCM I-1077, Institut Pasteur, Paris, France) with methanogen and acetogen, enhanced the metabolism of acetogenic strain and its acetate production, which supports the present results (Chaucheyras et al., 1995).

Footnotes

¹ This study was supported in part by a grant-in-aid (No. 02521) for scientific research from the Ministry of Education, Science, Sports, and Culture in Japan.

² Correspondence: Saiwai 3-5-8, Fuchu-shi, Laboratory of Agricultural Production Technology, Tokyo 183-8509 (fax: +81-42-367-5801; e-mail: hita{at}cc.tuat.ac.jp).

Received for publication July 21, 2003. Accepted for publication March 1, 2004.

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Lila, Z. A. Articles by Itabashi, H. Search for Related Content PubMed PubMed Citation Articles by Lila, Z. A. Articles by Itabashi, H.