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,2
* Laboratory for Animal Nutrition and Animal Product Quality, Ghent University, Proefhoevestraat 10, 9090 Melle, Belgium
Institute of Grassland and Environmental Research, Plas Gogerddan, Aberystwyth, Ceredigion SY23 3EB, UK
1 Corresponding author: veerle.fievez{at}UGent.be
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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Key Words: rumen bacteria • fatty acid • odd- and branched-chain fatty acids
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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Interestingly, OBCFA patterns are of great value for the systematic differentiation of rumen bacteria (Ifkovitz and Ragheb, 1968; Miyagawa, 1982; Minato et al., 1988; Kaneda, 1991). This suggests that changes in the rumen microbial population are reflected in the OBCFA pattern of ruminal digesta (Vlaeminck et al., 2004). In addition, Keeney et al. (1962) suggested microbial OBCFA could provide a qualitative description of the proportions of different classes of microbes leaving the rumen.
The effects of lipid-supplemented diets on ruminal lipid metabolism and bacterial fatty acids are well documented (Bauchart et al., 1990; Hussein et al., 1995). Although the effect of dietary forage:concentrate ratio (F:C) on the rate of hydrogenation and the duodenal flow of fatty acids were previously examined (Latham et al., 1972; Kalscheur et al., 1997; Kucuk et al., 2001; Loor et al., 2004b), literature data describing the effects on the fatty acid composition of mixed rumen bacteria are scarce (Kucuk et al., 2001; Bas et al., 2003) and lacking for bacteria isolated from the liquid-associated bacteria (LAB) and solid-associated bacteria (SAB) phases of the rumen. In addition, few experiments describe the effect of diet on bacterial synthesis of OBCFA (Bas et al., 2003). Hence, to contribute to the literature data, rumen and duodenal bacteria were isolated and their fatty acid profiles determined during an experiment aimed at evaluating the effect of varying forage proportions on the efficiency of rumen N utilization (Moorby et al., accepted).
In the current paper, we firstly report the effect of F:C ratio on fatty acid content and composition of rumen bacteria isolated both from the liquid and solid phase of the rumen and from duodenal content. Secondly, we examined the relationship between bacterial and dietary fatty acids. For the latter purpose, data from the current experiment as well as literature data were used. In addition, OBCFA of SAB and LAB were used to i) estimate relative proportions of SAB and LAB in duodenal bacteria, and ii) illustrate shifts in the bacterial populations.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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. Average daily DM intake was 13.2, 15.5, 18.4, and 20.7 kg for diets with F:C ratios of 80:20, 65:35, 50:50, and 35:65, respectively (Moorby et al., 2006).
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Analyses
Bacterial samples (450 mg) were used for extraction, methylation of fatty acids, and GLC analysis of fatty acid methyl esters. Extraction and methylation of fatty acids was based on the methods described by Sukhija and Palmquist (1988). The internal standard (C23:0, 1.5 mg) was added before the extraction. The lipids were extracted using toluene (0.45 g in 2 mL) and transesterified to methyl esters by heating (70°C for 2 h, under nitrogen) with 3 mL of methanolic HCl. Samples were neutralized with 5 mL of 6% potassium carbonate, depigmented with 1 g of charcoal, dried with 1 g of anhydrous sodium sulfate, and the resultant fatty acid methyl esters analyzed by gas chromatography. Fatty acid methyl esters were analyzed by GLC (CP-3800, Varian Ltd., Walton-on-Thames, UK) using a 100 m x 0.25 mm CP-Sil 88 column (a chemically bound stationary phase; Varian), with helium as carrier gas. The split ratio was 1:30 with the split open throughout the run. The injector and detector were held at 250 and 255°C, respectively. A temperature gradient (starting at 70°C, increased at 20°C/min to 175°C, held for 25 min, increased at 2.5°C/min to 200°C, held for 2 min, increased at 20°C/min to 230°C, held for 8.5 min) was used to separate the fatty acid methyl esters. Fatty acid methyl esters were identified from external standards (ME61 fatty acid methyl ester mixture, Larodan Fine Chemicals AB, Malmö, Sweden; S37 Supelco 37 component FAME mix, Supelco, Poole, Dorset, UK; conjugated linoleic acids standard, Matreya, Philadelphia, PA), and quantified using the internal standard. Trans-10 C18:1 was not commercially available and was identified by order of elution as described by Griinari et al. (1998). The reported temperature gradient enabled an optimized separation of cis-9, trans-11 C18:2 and trans-10, cis-12 C18:2. However, the reported cis-9, trans-11 C18:2 may be overestimated because of other isomers that may coelute on the gas chromatography column (trans-7, cis-9 C18:2 and trans-8, cis-10 C18:2). The increase in this peak has been considered to exclusively reflect changes in cis-9, trans-11 C18:2. Furthermore, other C18:2-isomers, besides the reported cis-9, trans-11 C18:2 and trans-10, cis-12 C18:2, might be present in rumen bacteria (see Kucuk et al., 2001; Loor et al., 2004b), but these are not mentioned because our analytical method has not been optimized for identification of these isomers. At the time the experiment and analysis were running, we did not dispose of the external iso C14:0 and iso C16:0 standards. Accordingly, these fatty acids were not identified in the chromatograms and are not reported in the current paper, although bacterial concentrations might be in the range of anteiso C17:0 concentrations.
Data Set Derivation
Data from 10 feeding experiments with dairy cows (Legay-Carmier and Bauchart, 1989; Bauchart et al., 1990; Klusmeyer and Clark, 1991; Tice et al., 1994; Pantoja et al., 1996; Christensen et al., 1998; Dufour et al., 2004; combined with unpublished results of B. Vlaeminck, V. Fievez, and R. J. Dewhurst) and beef steers (Hussein et al., 1995; Elliott et al., 1999) were used to examine the relationship between dietary and bacterial fatty acids. These studies were selected based on the availability in the papers of the fatty acid composition of both the diet and mixed rumen bacteria. Studies reporting fatty acid data of LAB only were discarded. Legay-Carmier and Bauchart (1989), Bauchart et al. (1990), and Dufour et al. (2004) reported fatty acid composition of both LAB and SAB. For these studies, an average fatty acid composition (50/50) was calculated from both bacterial groups. In the study by Dufour et al. (2004), OBCFA were the only bacterial fatty acids reported, although total fatty acid profiles were analyzed in these samples. Hence, data reported by Dufour et al. (2004) were completed by the other fatty acids (B. Vlaeminck, V. Fievez, and R. J. Dewhurst, unpublished data) for introduction in the current data set. In addition, mean values from the current experiment (n = 4) were used, resulting in an overall data set of 50 observations. Bacterial C18:3n-3, C18:2n-6, and C16:0 were related to the dietary content of these fatty acids. Bacterial monounsaturated octadecenoic fatty acids (i.e., sum of cis- and trans-C18:1 isomers) and C18:0 were related to the sum of their dietary precursors (i.e., C18:3n-3, C18:2n-6, cis-9 C18:1, and C18:0).
Calculations
Proportions of SAB and LAB in duodenal bacteria were estimated using a linear programming approach. The Solver function of Excel was used to apportion duodenal bacteria among SAB and LAB from each cow in each period according to the following equation:
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where Xi are the individual OBCFA (i.e., iso C15:0, anteiso C15:0, C15:0, iso C17:0, anteiso C17:0, and C17:0), duodenal bacteria(Xi), SAB(Xi), and LAB(Xi) are the content of fatty acid Xi in duodenal bacteria, SAB, and LAB, respectively (g/kg of DM), and A and B are the proportions of SAB and LAB, respectively. The Solver function of Excel was used to minimize the sums of squares of the differences between the observed and model estimates of bacterial OBCFA. To evaluate the validity of this approach, observed and estimated (based on the SAB/LAB proportions derived from the linear programming) duodenal fatty acid proportions were compared by the concordance correlation coefficient for all fatty acids (Lin, 1989).
Statistical Analyses
All statistical analyses were performed using SPSS 12.0 (SPSS Software for Windows, release 12.0, SPSS, Inc., Chicago, IL).
The effect of dietary treatment on fatty acid content and composition of SAB and LAB were analyzed according to
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where Yijkl is the individual observation, µ is the overall mean, Ti is the effect of dietary treatment, Bj is the effect of bacterial isolate (SAB vs. LAB), TBij is the interaction between treatment and bacterial isolate, Ck is the effect of cow, BCjk is the interaction between bacterial isolate and cow, Pl is the effect of experimental period, and 
ijkl is the residual error. Effect of cow was treated as a random effect. Treatment comparisons were the linear and quadratic effect of increasing proportion of dietary forage. Treatment effects were considered significant at P < 0.05.
The effect of dietary treatment on fatty acid content and composition of duodenal bacteria and proportion of SAB and LAB in duodenal bacteria were analyzed according to
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where Yijk is the individual observation, µ is the overall mean, Ti is the effect of dietary treatment, Pj is the effect of experimental period, Ck is the effect of cow, and ijk is the residual error. Effect of cow was treated as a random effect. Treatment comparisons were the linear and quadratic effect of increasing proportion of dietary forage. Treatment effects were considered significant at P < 0.05.
The relationship of dietary to bacterial fatty acids was evaluated using the mixed model procedure with the inclusion of the random effect of study as described by St-Pierre (2001). Observed bacterial fatty acids were adjusted for the study effects according to St-Pierre (2001). To avoid bias due to the incorporation of unpublished results (current study and unpublished results of B. Vlaeminck, V. Fievez, and R. J. Dewhurst) in the database, statistical analysis was performed both with and without these unpublished data. Slopes and intercepts of the equations, obtained with or without unpublished results, did not differ significantly (P > 0.5), which can be considered validation of the unpublished data, and justifies their incorporation in the database.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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. Total fatty acid content of SAB was 1.6 to 2.8 times higher than that of LAB and decreased with increasing F:C ratio. Diet showed no effect on proportions of the 2 major fatty acids, C16:0 and C18:0. Stearic acid was enriched in SAB, whereas C16:0 was more abundant in LAB. On a DM basis, both fatty acids were higher in SAB and increased with proportion of concentrate (data not shown). Increasing proportions of concentrate generally increased bacterial concentration of unsaturated C18-fatty acids. However, cis-15 C18:1 and C18:3n-3 linearly decreased with increasing concentrate, whereas trans-11 C18:1 remained constant. Trans-6–8 C18:1 and trans-10 C18:1 increased with increasing proportion of dietary concentrate with a higher increase in LAB compared with SAB. No differences were observed in trans-12 C18:1, cis-9 C18:1, and C18:3n-3 between LAB and SAB, whereas the latter were enriched in trans-11 C18:1 and cis-9, trans-11 C18:2. Total OBCFA accounted for 5.9 and 17.0% of the fatty acids in SAB and LAB, respectively, and increased with increasing proportion of dietary forage.
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). However, cis-9, trans-11 C18:2 in duodenal microbes was substantially lower compared with the values found in bacteria isolated from the rumen. In addition, whereas no diet effect was found for trans-11 C18:1 in bacterial isolates from the rumen, trans-11 C18:1 in duodenal microbes initially decreased as dietary forage decreased, and then increased with higher levels of concentrate, resulting in a significant quadratic effect. As shown by the dissimilarity matrix (data not shown), the fatty acid profile of duodenal bacteria was more related to the fatty acid profile of SAB than that of LAB (P < 0.001).
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Observed fatty acid composition of duodenal bacteria and fatty acid composition, as calculated from SAB and LAB fatty acid composition, and SAB/LAB proportions, as estimated by linear programming, were compared by the concordance correlation coefficient. In general, observed and estimated OBCFA compositions were closely related as shown by the high concordance correlation coefficients (anteiso C15:0 = 0.946; C15:0 = 0.936; iso C15:0 = 0.870; C17:0 = 0.804; and iso C17:0 = 0.818). The concordance correlation coefficients were low for C18:0 (0.150) and trans-11 C18:1 (0.231), and were moderate for anteiso C17:0 (0.533) and C18:3n-3 (0.537). Concordance correlation coefficients values for other fatty acids (i.e., C14:0, C16:0, trans-10 C18:1, cis-9 C18:1, C18:2n-6) were all higher then 0.600.
Relationship of Dietary Fatty Acids with Rumen Bacterial Fatty Acids
Relationhips between dietary fatty acids and fatty acids of rumen bacteria are presented in Figure 1. Total fatty acid content was strongly related to dietary fatty acid content (Figure 1A). In contrast, no relationship was found between dietary and bacterial C18:3n-3 (P = 0.161; Figure 1B), whereas bacterial C18:2n-6 was only moderately related with dietary C18:2n-6 (P = 0.081; Figure 1C). Relationships of bacterial content (g/kg of DM) of C18:1 fatty acids and C18:0 and their dietary precursors were closer than for the other fatty acids (Figure 1D and 1E).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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Incorporation of Dietary Fatty Acids
An increase in fatty acid content with an increasing proportion of concentrate in rumen bacteria is in accordance with results from Czerkawski (1976) who stated that the increase in bacterial fatty acid content was linked to an increase in dietary concentrate due to its higher lipid content. Combining current experimental and literature data showed that an increase in dietary fatty acids of 10 g/kg of DM results in an increased bacterial fatty acid content of 8.06 g/kg of DM (Figure 1A
). It is not known whether this increase results from incorporation or physical adsorption on the cell envelope of fatty acids. However, incorporation is a process certainly to be considered because removal of fatty acids through washing the cells with hexane or sodium hydroxide was not successful (Harfoot et al., 1974). Indeed, Bauchart et al. (1990) reported incorporation by bacteria of fatty acids as intracellular lipid droplets, whereas others showed a significant proportion of radioactive C18:2n-6 and C18:3n-3 to be incorporated into bacterial polar lipids (Hawke, 1971; Demeyer et al., 1978). However, the current study, combined with some published data, shows that bacterial C18:3n-3 and C18:2n-6 contents is not related or is only moderately related to dietary C18:3n-3 and C18:2n-6. Because the anaerobic pathway of bacterial fatty acid biosynthesis is not capable of introducing more than one double bond per fatty acid (Russell and Nichols, 1999), it is suggested that rumen bacteria readily incorporate C18:2n-6 and C18:3n-3 up to 3.06 and 1.12 g/kg of DM, respectively (Figure 1, panels B and C). These results are in agreement with the findings of Bauchart et al. (1990), who stated that rumen bacteria preferentially and proportionally incorporate C18:2n-6 over C18:3n-3. This finding may help to partially explain the well-known higher rate of hydrogenation observed for C18:3n-3 vs. C18:2n-6.
Demeyer et al. (1978) showed part of the radioactivity of C18:2n-6 to be recovered in monounsaturated C18 fatty acids in the bacterial phospholipid fraction, suggesting that hydrogenated fatty acids are incorporated. This might explain the increasing proportion of trans-10 C18:1 in rumen bacteria with low F:C ratio. Indeed, the increase in rumen trans-10 C18:1 with decreasing F:C is consistent with previous reports reviewed by Bauman and Griinari (2003), in which high-grain diets shifted the hydrogenation pathway of C18:2n-6 away from cis-9, trans-11 C18:2 and trans-11 C18:1 toward trans-10, cis-12 C18:2 and trans-10 C18:1. Increasing proportions of concentrate increased the ratio trans-10 C18:1 to trans-11 C18:1 in LAB and SAB, and this increase was 3.4 times higher in LAB than in SAB (Figure 2). Recently, Kim et al. (2002) found that LAB produced more trans-10, cis-12 C18:2 when they were incubated with C18:2n-6 compared with SAB; even higher productions were observed when LAB were isolated from cattle fed a grain-based diet. The results suggest that the abundance of rumen bacteria capable of producing trans-10, cis-12 C18:2 and trans-10 C18:1 is higher in LAB compared with SAB and increases both in SAB and LAB with increasing proportion of dietary concentrate. However, no significant quantities of trans-10, cis-12 C18:2 were found in SAB and LAB. Loor et al. (2004a) found no differences in the concentration of trans-10, cis-12 C18:2 between SAB and LAB (0.1 g/100 g of fatty acids). It is possible that trans-10, cis-12 C18:2 is produced in the extracellular matrix around bacteria, but not extensively incorporated as was suggested for cis-9, trans-11 C18:2 (Kim et al., 2005). Recent in vitro research demonstrated that oleic acid could be isomerized to several trans C18:1 isomers (Mosley et al., 2002; AbuGhazaleh et al., 2005). It is possible that isomerization of cis-9 C18:1, rather than hydrogenation of trans-10, cis-12 C18:2, was responsible for the higher bacterial concentration of trans-10 C18:1 with higher dietary proportions of concentrate. Nevertheless, AbuGhazaleh et al. (2005) found that trans monoene isomers, derived from oleic acid, showed a double bond primarily at positions C7, C9, and C14. Moreover in these in vitro studies, more than 75% of trans-10 C18:1 was derived from the hydrogenation of C18:2n-6, which accounted for only 9% of the dietary fatty acids. In the current experiment, C18:2n-6 represented more than 25% of the dietary fatty acids. Consequently, it is unlikely that a major part of the bacterial trans-10 C18:1 was derived from the isomerization of cis-9 C18:1 rather than the hydrogenation of C18:2n-6. Nevertheless, the increased intake in both dietary cis-9 C18:1 and C18:2n-6 with decreasing F:C ratio makes it difficult to distinguish between the isomerization of cis-9 C18:1 or hydrogenation of trans-10, cis-12 C18:2 as the main factor driving bacterial trans-10 C18:1.
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Bacterial OBCFA
Microbial odd-chain fatty acids (C15:0 and C17:0) are formed through elongation of propionate or valerate, whereas precursors of branched-chain fatty acids (iso C14:0, iso C15:0, iso C16:0, iso C17:0, anteiso C15:0, anteiso C17:0) are branched-chain amino acids (valine, leucine, and isoleucine) and their corresponding branched short-chain carboxylic acids (isobutyric, isovaleric, and 2-methyl butyric acids; Kaneda, 1991). Although the OBCFA profile of many cultivable rumen bacteria has been reported (Ifkovitz and Ragheb, 1968; Minato et al., 1988; Miyagawa, 1982), only a limited number of selected species have been studied and it is not feasible to attempt to describe the species composition of rumen samples from the OBCFA profile. Nevertheless, such noncultural techniques, based on the analysis of bacterial lipids, offer the prospect of detecting shifts in the rumen microbial ecology in response to, for example, dietary shifts (Dehority and Orpin, 1988). Differences between SAB and LAB in chemical composition (Merry and McAllan, 1983) and enzyme activity (Williams and Strachan, 1984; Michalet-Doreau et al., 2001) demonstrate that the distribution of bacterial species is different in the liquid and solid phases of the rumen (Michalet-Doreau et al., 2001). This is in agreement with the current analysis of OBCFA, which suggests that the species composition of the adherent population differs from that of the liquid phase. The higher concentration of anteiso C15:0 in LAB is in agreement with results reported by Dufour et al. (2004) and Kim et al. (2005). Although total concentration of OBCFA decreased with decreasing F:C, a lower proportion of dietary concentrate decreased the proportion of anteiso C15:0 in total OBCFA in duodenal bacteria. Recently, Bas et al. (2003) found a similar decrease in the relative abundance of anteiso C15:0 in total OBCFA in rumen bacteria when goats were fed decreasing proportions of concentrate. Combining the results reported by Bas et al. (2003) with the results of the current experiment indicated that the forage proportion was strongly related to the concentration of anteiso C15:0 in total OBCFA (rpearson = (0.771, P = 0.009, n = 10). Decreasing F:C ratios also linearly reduced iso C15:0. Although not measured in the current study, a similar effect might be expected on the iso C14:0 and iso C16:0 proportions, because a strong correlation (R2 = 0.97 to 0.98) has been observed between proportions of iso fatty acids with a chain length of 14 to 16 carbons in mixed rumen bacteria (Bas et al., 2003). In the latter study, reporting the fatty acid composition of mixed rumen bacteria, amounts of iso C14:0 and iso C16:0 were about 43 and 54%, respectively, of the iso C15:0 concentration.
Increasing the F:C ratio is usually beneficial for the pool of SAB because more fibrolytic bacteria attach to forage particles (Weimer et al., 1999). Indeed, the estimated proportion of SAB increased from 64.7 to 74.8% with increasing proportion of dietary forage. Faichney (1980) reported that the proportion of SAB in the rumen reached 90% in sheep fed roughage only, whereas it declined to 50% for steers fed equal proportions of forage and concentrate (Merry and McAllan, 1983). Increasing proportions of SAB with increasing F:C might reflect both the increased attachment to forage particles (Weimer et al., 1999) as well as a decreased growth rate of LAB by substrate limitation (Bates et al., 1985). Indeed, the decreased ratio of cytosine:N in LAB (0.070, 0.064, 0.057, and 0.055 for F:C of 36:65, 50:50, 65:35, and 80:20, respectively; SEM = 0.003; P = 0.009) and adenine:N (0.095, 0.091, 0.081, and 0.081 for F:C of 36:65, 50:50, 65:35, and 80:20, respectively; SEM = 0.002; P = 0.003) with increasing F:C suggests a decreased growth rate of LAB under these circumstances (Bates et al., 1985). In addition, these ratios also suggest a lower growth rate of SAB (0.043 and 0.059 for cytosine:N and adenine:N, respectively) compared with LAB, which was not affected by dietary treatment (P > 0.20). These findings are in line with the results reported by Bates et al. (1985). Interestingly, bacterial growth rate showed a strong negative relationship with bacterial concentration of iso C17:0 (rpearson = –0.729 and –0.823 for cytosine:N and adenine:N, respectively, P < 0.001, n = 32).
The changes in anteiso C15:0 and iso C17:0 were probably a reflection of the shifts in the bacterial population. In general, increasing the concentrate proportion increases the relative importance of amylolytic bacteria (e.g., Prevotella ruminicola, Ruminobacter amilophilus, Succinivibrio dextrinosolvens; Dehority and Orpin, 1988), which are enriched in anteiso C15:0 (Ifkovitz and Ragheb, 1968; Minato et al., 1988; Miyagawa, 1982). Similarly, the cellulolytic bacteria Ruminococcus flavefaciens and Butyrivibrio fibrisolvens are enriched in iso C17:0, whereas the amylolytic bacteria Selenomonas ruminantium, Ruminobacter amilophilus, and Succinivibrio dextrinosolvens contain little iso C17:0 (Ifkovitz and Ragheb, 1968; Minato et al., 1988; Miyagawa, 1982). Hence, the results suggest LAB are enriched in amylolytic bacteria and show a higher growth rate compared with SAB. However, the high abundance of anteiso C15:0 in some strains of the cellulolytic bacteria Butyrivibrio fibrisolvens and the low content of this fatty acid in Selenomonas ruminantium as well as the high content of iso C17:0 in some strains of Prevotella ruminicola (Ifkovitz and Ragheb, 1968; Minato et al., 1988; Miyagawa, 1982) illustrates the difficulty in describing the bacterial composition of rumen samples at the species level based on the OBCFA profile. Nevertheless, the strong relationships suggest that OBCFA, in particular anteiso C15:0 and iso C17:0, might be used as a tool to evaluate nutrient supply to rumen bacteria.
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CONCLUSIONS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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Analysis of OBCFA suggested the presence of different bacterial populations in the solid and liquid phases of the rumen. Using this variation in the OBCFA pattern, relative proportions of both bacterial fractions in duodenal bacteria could be estimated by linear programming, and showed that increasing F:C increased relative proportions of SAB in duodenal bacteria. In addition, the strong relationship of anteiso C15:0 and iso C17:0 with the dietary proportion of forage and bacterial growth rate, respectively, suggests that OBCFA might be used as tool to evaluate nutrient supply to rumen bacteria.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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FOOTNOTES |
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Received for publication September 1, 2005. Accepted for publication January 3, 2006.
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; n = 4), unpublished data from B. Vlaeminck, V. Fievez, and R. J. Dewhurst (
; n = 6), and published data (n = 40) of rumen bacteria isolated from the rumen of dairy cows (
; 
; 