Some Factors Affecting Fermentation Capacity and

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1 APPLIED MICROBIOLOGY, Sept. 1969, p Copyright 1969 American Society for Microbiology Vol. 18, No. 3 Printed in U.S.A. Some Factors Affecting Fermentation Capacity and Net Growth of Rumen Microorganisms MANAL ZAKI EL-DIN AND K. EL-SHAZLY Faculty of Agriculture, University of Alexandria, Egypt, United Arab Republic Received for publication 23 January 1969 The fermentation rate of rumen microorganisms obtained from a sheep fed on hay was determined at different hours after feeding. The highest rate of fermentation was obtained immediately after feeding whereas the lowest rate was always before feeding. The effect of adding glucose, sucrose, and starch alone or in combination with urea, sodium citrate, or succinic acid on the maximal fermentation rate was studied. In no case was the maximal fermentation rate greater than that obtained in the presence of concentrate and straw. An investigation on the effect of C/N ratios, dilution, and substrate concentration on the net growth of rumen microorganisms was undertaken. The highest net growth value was obtained with a C/N ratio of 16.5 to 17.5, which is the ratio found for the ration fed to the animal. It was possible to increase net growth approximately threefold by using the proper dilution and fivefold by using the proper feed concentration. A method for measuring the microbial growth in the rumen was proposed by el-shazly and Hungate (9) based on the changes in fermentation capacity taking place within a short period of incubation of rumen contents. The diaminopimelic acid in the same rumen samples was estimated. The growth measurements by the two methods were in good agreement (10). Zaki el-din and el-shazly (14) produced evidence of the reliability of the method in measuring the bacterial and protozoal growth. The present paper describes factors affecting the net growth rates of rumen microorganisms, e.g., C/N ratio, dilution, and substrate concentration. MATERIALS AND METHODS 313 Animals and sampling. The experiments were carried out by using two fistulated sheep fed on berseem hay (2 kg once in the morning) or concentrate plus wheat straw in the ratio 3:1 (1 kg once in the morning). The concentrate mixture consisted of undecorticated cottonseed cake and rice bran in the ratio 1:1 plus calcium hydroxide and 1% common salt. Collection and preparation of samples were done as described previously (14). The rate of fermentation was measured at different times after feeding on samples obtained from the sheep fed hay. Measurements of maximal fermentation rate and net growth. Maximal fermentation rates and net growth rates of rumen microorganisms were determined by the method of el-shazly and Hungate (9) as modified by Zaki el-din and el-shazly (14). The effects of substrate concentration, sodium bicarbonate, and type of carbohydrate (glucose, sucrose, and starch, 5 to 10 g alone or together with urea, sodium citrate, and succinic acid) on maximal fermentation rate were tested. Effect of carbon-nitrogen ratio on net growth. Rumen samples (about 200 g) obtained through the rumen fistula from a sheep fed concentrate plus straw were collected at different hours after feeding. Urea or starch were added to samples (200 g) to alter the C/N ratio, and the net growth rate was compared with that in samples without these additions. The effect of C/N ratio on net growth was also studied on one large sample divided into several small samples (50 g); to each sample, urea or starch was added to study the whole range of C/N ratios in one experiment. Carbon was determined by the method of Walkley (12) utilizing o-phenanthroline as indicator. Nitrogen was determined by the Kjeldahl method according to the official methods of the Association of Official Agricultural chemists (7). In the above experiments the range of C/N ratios used was obtained by using samples collected at different times. Effect of dilution on net growth. The effect of diluting the rumen sample with mineral solutions A and B (1) on the net growth was studied in the following experiments. The maximal fermentation rate was measured in the usual manner on a 50-g rumen sample. Similar samples were incubated for 1 hr with different volumes of the mineral solution. After 1 hr of incubation the maximal rate of fermentation was determined after making the final volume 200 ml with mineral solution. Effect of feed concentration on net growth. The effect of adding different amounts of ground concentrate plus straw from the same ration consumed by the animal on the net growth values was tested on rumen

2 314 ZAKI EL-DIN AND EL-SHAZLY APPL. MICROBIOL. samples obtained before and after feeding. The optimum dilution level found from the previous experiments was employed throughout these trials. The initial maximal fermentation rate was first measured, then several subsamples (about 50 g each of rumen contents) were incubated for 1 hr with the following concentrations of the feed: 0, 5, 10, 15, 20, and 25 g. At the end of the incubation period, the feed was increased to 20 g, and the mineral solution to 200 ml. The final maximal rate of fermentation was then determined, and net growth was estimated. RESULTS Normal rates of fermentation. The fermentation rates vary with time after feeding. The highest rate was obtained immediately after feeding (15 to 30 min), whereas the lowest rate was found before feeding (Fig. 1). c 10r E 6 c,a, c 2 0ca Ltn t rime FROM FEEDING (hr) FIG. 1. Fermentation rates of rumen samples collected from a fistulated sheep fed berseem hay. Different curves represent different days. TABLE 1. Factors affecting maximal rates of fermentation. The effect of rumen sample concentration, feed concentration, dilution, and sodium bicarbonate concentration on the maximal rates of fermentation were studied and found similar to those found by el-shazly and Hungate (9). The effect of adding glucose, sucrose, and starch alone or in combination with urea, sodium citrate, or succinic acid was compared with that of adding the feed. In no case was the maximal rate of fermentation greater than that obtained in the presence of concentrate plus straw (Table 1). Net growth rates of rumen microorganisms. Figure 2 shows typical curves of maximal fermentation rates before and after 1 hr of incubation at 39 C. From the difference of the slopes of TIME (min ) TIME nmin) FIG. 2. Normal and maximal rates offermentation at two different intervals afterfeeding sheep on concentrate plus straw, 3: 1. The effect of adding glucose, sucrose, and starch alone or in combination with urea, sodium citrate, or succinic acid on the maximal fermentation rate Maximal rate Substrate Concna No. of runs of fermentation (usliters/g/min) Concentrate + straw Concentrate + glucose Concentrate + glucose Glucose Glucose Glucose + urea Glucose + urea Glucose + sodium citrate Glucose + succinic acid Glucose + succinic acid Sucrose Sucrose Starch Starch Starch + sodium citrate Starch + sodium citrate * Concentration is expressed in grams per 200 ml of buffer.

3 VOL. 18, 1969 NET GROWTH RATES OF RUMEN MICROORGANISMS 315 the two curves the net growth was calculated. The net growth (per cent per hour) for these curves was 62 when the sample was collected 2 hr after feeding, and 17 when the sample was collected 0.5 hr after feeding. Effect of C/N ratios on the net growth rates of rumen microorganisms. The net growth rates in the first experiment (results not reported) differed widely from one trial to another, but it was obvious that C/N ratios close to those found in the feed consumed by the animal gave highest net growth rates. This was confirmed in three experiments whereby urea or starch or both were added in different concentrations to portions of the same rumen sample, thus altering the C/N ratio. The highest net growth values were found when the C/N ratio was between 16.5 and 17.5 (Fig. 3) or close to the values of the C/N ratio in the feed the animal was consuming. The mean value of total N of 11 rumen samples obtained from a sheep (60 kg) fed on concentrate plus straw 3:1 was g per 100 g of dry matter. Effect of dilution on net growth rates. Dilution :k 5_.-~ 0 0: x 25/ DILUTION (ml.) FIG. 4. Effect of dilution on the net growth rate of rumen microorganisms obtained from a sheep fed concentrate plus straw. urea per 100 g of rumen contents and 1.95 to 7.6 g of starch per 100 g of rumen contents. 15. of the rumen sample about 3 times (150 ml of I.\:mineral solution to 50 g of rumen sample) gave J 5. xt the highest net growth value (Fig. 4); a higher *x dilution caused a slight drop in the net growth rate of rumen microorganisms. Effect of feed concentration on net growth rates. The results (Fig. 5) indicate that 15 g of feed (concentrate plus straw, 3:1) gave the highest net K. 15_. growth rate (increased approximately 5 times). A higher concentration of the feed (20 or 25 g) caused a drop in the net growth rate of rumen 25-. microorganisms. In two other experiments where samples were collected after feeding and the initial maximal fermentation rates were high (of 35- i C/23 1I 5 16 the order of 140,liters per g per min), the addition of substrate to the fermentation media in vitro CIN RA TRX resulted in depression rather than improvement of FIG. 3. Effect of changing C/N aratios by using urea net growth. or starch or both on the net growth of rumen microorganisms obtained from sheep fed concentrate plus DISCUSSION straw in three different experiments. 0, to 2.7 g of urea per 100 g of rumen contents and 0.97 to 6.0 g of The fermentation rates vary with time from starch per 100 g of rumen contents; X, 0.4 to 2.14 g of feeding; the highest rate was obtained immedi- urea per 100 g of rumen contents and 1.8 to 7.2 g of starch per 100 g of rumen 0.85 to 1.8 g of ately after feeding (Fig. 1). This was because of the readily fermentable carbohydrates present in the ration. A second smaller peak was observed about 6 to 8 hr after feeding and probably repre-

4 316 ZAKI EL-DIN AND EL-SHAZLY APPL. MICRoBIoL. Z 55 o ~ 2hrafter feeding o-o Before feeding FEED CONCENTRATION Fio. 5. Effect of concentration of feed on the net growth rate of rumen microorganisms obtained from a sheep fed concentrate plus straw in two different experiments. sents a second phase of fermentation of fibrous material (11). The lowest rate of fermentation coincided with the time before feeding. The microorganisms die progressively with time of fasting (4). The feed consumed by the animal gave the highest fermentation capacity when added to the rumen sample in vitro. The highest net growth rates were found when the C/N ratio was between 16.5 and 17.5 (Fig. 3) and close to the ratio in the feed which the animal was consuming. The addition of urea and starch together to keep the C/N ratio similar to the feed did not change the net growth rate. It is not surprising that the best growth rate of rumen microorganisms coincided with the C/N ratio of the feed. It has been long known that it takes some time for the rumen microorganisms to adapt to the feed. The mean value of total N in the rumen contents from a sheep (weighing 60 kg) fed concentrate plus straw (3:1) was 2.47 i 0.24 g to 100 g of dry matter, which is equivalent to 1.56 to 2.06 g of microbial N. Weller et al. (13) found that 63 to 83% of total N was microbial and that 68% of the microbial N was bacterial. Bacteria have a nitrogen content 10.5% of dry weight (2), whereas protozoa may have a lower nitrogen content, 6.8% (5); therefore, an average microbial N of 9.32% is indicated (68 X X = 9.32),whichyields 16.7 to 22.1 g of microbialcells/ 100 g of dry matter or 117 to 155 g (taking the dried rumen contents of the sheep as 700 g). The average net growth rate equals 12.6% per hr (Table 4 of reference 14); in 24 hr it amounts to 302%. The microbial cells formed in 24 hr would equal 353 to 468 g. Hungate (2) calculated a value of 175 g for sheep (40 kg) fed hay. The results of studies to determine the effect of dilution with Hungate's mineral mixtures A and B (1) on the net growth rate indicated that a dilution of about three times that of the rumen sample (150 ml of mineral solution to 50 g of rumen sample) gave the highest net growth rate. An increase of from 2.6 to 3.4 times was obtained due to this dilution. A higher dilution caused a slight drop in the net growth rate of rumen microorganisms. The effect of dilution is probably due to reduction of concentration of end products. When the ideal dilution was used and the substrate (concentrate plus straw, 3:1) concentration was varied, 15 g of the feed for every 50 g of the sample gave the highest growth rate of rumen microorganisms. It was possible in this work, by adjusting C/N ratio, dilution, and substrate concentration, to increase the net growth rate in vitro about fivefold. It is therefore suggested that it might be economical to propagate rumen microbial cells in vitro under ideal conditions to obtain microbial food rich in protein of high biological value (5) from low quality roughage and concentrates, including urea and some minerals. Purser and Buechler (8) showed that bacterial and protozoal cells contain about 10% lysine, which is one of the limiting amino acids in plant proteins. Theoretically, based on net growth rate results (Fig. 5), it is possible to produce 0.5 to 0.95 x 103 kg (dry weight) of microbial cells per hr from 103 kg (dry weight) of rumen microorganisms (which could be contributed from about 104 kg or more of dry rumen contents). From the results of volatile fatty acid (VFA) production (Table 3 of ref. 14) of 50 Emoles of VFA per 100 g of wet rumen contents per min, assuming ratios of acetic to propionic to butyric of the order of 70:20:10, it could be calculated that 10 kg of dry rumen contents (or 105 kg of wet rumen contents) would yield 126, 44.4, and 26.4 kg per hr of the acids, respectively, and roughly 16kg of methane. Under conditions of maximum fermentation, the rates of acid and gas production would be accelerated (probably fivefold) and a greater yield would be indicated. It is expected that when incubation takes place for more than 1 hr the net growth rate

5 VOL. 18, 1969 NET GROWTH RATES OF RUMEN MICROORGANISMS 317 will decrease unless ideal conditions of dilution, feed concentration, and C/N ratio could be regulated as the process of fermentation proceeds. LITERATURE CITED 1. Hungate, R. E The anaerobic mesophilic cellulolytic bacteria. Bacteriol. Rev. 14: Hungate, R. E Quantitative aspects of the rumen fermentation, p Physiology of digestion in the ruminant. In R. W. Dougherty (ed.), Butterworth, Inc., Washington D.C. 3. McNaught, M. L., E. C. Owen, K. M. Henry, and S. K. Kon The utilization of non-protein nitrogen in the bovine rumen. 8. The nutritive value of the proteins ofpreparations of dried rumen bacteria, rumen protozoa and brewers yeast for rats. Biochem. J. 56: Meiske, J. C., R. L. Salsbury, J. A. Hoefer, and R. W. Luecke The effect of starvation and subsequent refeeding on some activities of rumen microorganisms in vitro. J. Animal Sci. 17: Naga, M. M. A., and K. el-shazly The metabolic characterization of the ciliate protozoon Ediplodinium medium from the rumen of buffalo. J. Gen. Microbiol. 53: Naga, M. M. A.. and K. el-shazly Activities of rumen microorganisms in water buffalo (Bos bubalus L.) and native cows. J. Dairy Research, In press. 7. Official methods of analysis of the association of official agricultural chemists. Association of Official Agricultural Chemists, Washington D.C Purser, D. B., and S. M. Buechler Amino acid composition of rumen organisms. J. Dairy Sci. 49: el-shazly, K., and R. E. Hungate Fermentation capacity as a measure of net growth of rumen microorganisms. Appl. Microbiol. 13: el-shazly, K., and R. E. Hungate Method for measuring diaminopimelic acid in total rumen contents and its application to the estimation of bacterial growth. Appl. Microbiol. 14: Walker, D. L Energy metabolism and rumen microorganisms, p In R. W. Dougherty (ed.), Physiology of digestion in the ruminant. Butterworth, Inc., Washington D.C. 12. Walkley, A A critical examination of a rapid method for determining organic carbon in soils - effect of variations in digestion conditions and of inorganic soil constituents. Soil Sci. 63: Weller, R. A., F. W. Gray, and A. F. Pilgrim The conversion of plant nitrogen to microbial nitrogen in the rumen of the sheep. Brit. J. Nutr. 12: Zaki el-din, M., and K. el-shazly Evaluation of a method of measuring fermentation rates and net growth of rumen microorganisms. Appl. Microbiol. 17: Downloaded from on March 30, 2019 by guest

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