Rumen microbes ferment dietary carbohydrates and protein to obtain ATP, which in turn is the major source of energy required for microbial growth. The two major reactions of rumen fermentation are volatile fatty acids (VFA) and microbial cells; the former are a primary source of metabolizable energy and the latter the primary source of metabolizable amino acids for maintenance and milk synthesis. The efficiency with which dietary nutrients are converted to energy and protein for tissues and milk synthesis varies considerably and is not high. Much of the inefficiency seems to occur in the rumen and is related to ‘decisions’ made by the microbial community as a direct consequence of variations in nutrient availability and/or conditions in the rumen. Better understanding of the basic aspects of rumen fermentation will identify strategies for improving efficiency of converting feed energy and protein into end products.
Efficiency does not imply maximum intake or maximum production but rather the proportion of the intake nutrient (input) that is recovered as useful product (Baumgardt, 1967). Gross or net efficiency (Brody, 1945), total or partial efficiency (Kleiber, 1961) are terms that are used to explain biological and more particularly, energetic efficiency. In the calculation of efficiency there are costs associated with the digestion and absorption of nutrients during the process of ruminal fermentation. Some of the biggest costs are associated with microbial maintenance, heat production and disposal of equivalents as methane during fermentation. The goal, of course, is to make more nutrients available for productive functions (milk, muscle) and reduce losses during digestion and metabolism. Decisions made at the cellular level to channel nutrient toward one pathway over the other are mediated by a complex process which includes the genetic potential of individual animals. However, the inherent fermentative losses can be high and variable resulting in a large fluctuation in the make-up of absorbed nutrient supply to the animal. The pattern of nutrient supply may play a critical role in the choice of pathway for metabolite use and hence the efficiency of use of the nutrient (Van Soest, 1963).
FERMENTATION IN THE RUMEN
Carbohydrate use and ATP generation
Given the anaerobic fermentation and the associated inherent losses, only a small fraction (10 -12%) of the potential aerobic ATP yield from hexose is realized in the rumen (Hungate, 1966). The processes that generate energy require energy. Growth and maintenance of microbial cells, VFA and other end products of fermentation are a source of nutrients to the animal but also place a limit on productive efficiency. The choices we have as ruminant nutritionists are: 1) maximize nutrients from the rumen, 2) manipulate rumen function to increase nutrient capture and, 3) promote rumen by-pass to optimize nutrient supply. Carbohydrates are the predominant source of energy (ATP) in the rumen and much is known about the predominant pathways of carbohydrate metabolism, however, estimation of ATP yield is still arbitrary.
Figure 1. Interrelationship between carbohydrate fermentation (ATP generation) and microbial cell growth (Bergen and Yokoyama, 1977).
Diversity of microbial populations, competitive metabolic pathways and the ability of microbes to adapt to their environment make quantitative estimation of end products extremely difficult.
Diet is perhaps the most important variable affecting microbial fermentation. The impact of changing the dietary forage to concentrate ratio on digestion kinetics is well documented. The alteration in VFA profiles and dietary induced shifts in rumen pH are well known phenomena and their impact on animal function are widely accepted. However, we know little about the effect of diet changes on microbial adjustments and the energetic consequences in terms of efficiency of nutrient use. Microbes alter their growth depending upon the substrate, pH and rate of passage from the rumen and they will do that by changing the end products of fermentation. Microbes may choose less efficient metabolic pathways to reduce maintenance cost and register a net increase in growth.
Microbial protein, Methane production and Fermentative heat loss
It is very difficult to determine the true impact of a reduction in the inherent fermentative energy losses on animal performance. In this regard, the two sources of ruminal energy loss that have received most focus are the heat of fermentation (HF) and methane production (MP). Heat of fermentation is an estimate of the energy lost as heat due to inefficiencies in microbial metabolic activities and it does not include the energy cost of cell maintenance. The HF can range from 3 to 12% of the gross energy of feed (Blaxter, 1962). Methane comprises between 20 and 30% of total gases produced in the rumen and can represent a significant feed energy loss (Johnson and Johnson, 1995). Both these sources of energy loss are variable and are markedly influenced by feed intake and feed quality. Furthermore, it is believed that fermentation and microbial growth may not be tightly coupled processes resulting in dissipation of heat (Russell, J. B. 1986).
Microbial protein synthesis is limited by the amount of energy available in the rumen (Hungate, 1966).
Microbes provide the majority of the metabolizable protein to the animal and the only mechanism for non-protein nitrogen use. Improving animal productivity requires a better understanding of the quantitative aspects of microbial protein synthesis. It was originally believed that microbial growth was directly proportional to the ATP generated from energy substrates in the rumen with a YATP constant of 10.5g (Bauchop and Elsden, 1960, Hungate, 1966). Later it was proposed that YATP was not a constant but depended on the growth rate and maintenance requirements of the microbes (Stouthamer and Bettenhaussen, 1973, Isaacson et al., 1975). Microbial efficiencies are increased under rapid growth conditions (increased dilution rate) due to a reduction in maintenance energy.
Figure 2 and 3. Relationship between true ruminally degraded OM, microbial N flow to the duodenum and microbial efficiency (Oba and Allen, 2003).
Figure 4. Effect of starch passage rate on microbial efficiency (Oba and Allen, 2003).
Figure 5. Relationship between rumen pH and bacterial N flow (Bach et al., 2005).
This results in variable YATP values over the physiological range of ruminal conditions. At reduced growth rates, a greater proportion of energy is used for VFA production and the protein to energy ratio is compromised since a smaller proportion of energy is used for microbial protein. Maintenance requirements vary among microorganisms as well as within the same microbe depending upon various factors. Any change in fermentative activity could result in large fluctuations in microbial maintenance requirements (Warner, 1965). Increasing feed intake decreases microbial maintenance costs by increasing passage (dilution) rates with a subsequent improvement in efficiencies. However, any time feed intake is increased one needs to be cautious with regards to digestibility, and potential changes in fermentation end products (Isaacson et al., 1975). This highlights the need to better understand post ruminal supply of nutrients and energetic efficiency.
Manipulation of Ruminal Fermentation
Addition of feed additives is a common occurrence to alter rumen fermentation with an attempt to improve animal productivity. Among several, ionophores have been used for decades in ruminant diets to improve energetic efficiency (Russell and Strobel, 1989). The ionophore induced improvement in animal performance is explained in terms of their selective action on the gram positive bacteria in the rumen. Ionophores enhance the capture of feed carbon as propionate rather than methane resulting in the improvement in feed energy utilization. Ionophores inhibit lactic acid production and reduce amino acid deamination resulting in a more favorable rumen pH and enhanced N use. Organic acids are another class of feed additives used to enhance ruminal fermentation. Whereas ionophores inhibit certain bacteria, organic acids exert their influence by stimulating specific microbes (Nisbet and Martin, 1993). Irrespective of their mode of action, organic acids too increase propionate, lower lactic acid and methane by rumen microbes.
Methane has received renewed attention in recent years due to its impact as a greenhouse gas. Hence, mechanisms to inhibit methane production and capture a greater proportion of the feed carbon for use by the animal and thereby reduce the amount expelled into the environment have been a major focus of several research programs. It is common to introduce feed ingredients or additives that lower methane with a concomitant shift in other end products primarily to propionate. This net utilization of H2 for propionate production has been used to demonstrate improved energetic efficiency. Others have argued that methanogens serve as an essential electron sink for all microbes thereby maintaining a low partial pressure of H2 in the rumen which in turn promotes maximal yields of ATP to support microbial growth. Hence, inhibition of methane would reduce net ATP yield and decrease net microbial growth. However, inhibition of methane has been shown to interfere with rumen function by depressing the net energy value for ground maize (Cole and McCroskey, 1975). This anomaly has been explained by the fact that not only is methane formation a direct sink for electrons which generates ATP but methanogens enhance ATP yield per unit of substrate by sparing carbon compound electron acceptors (Hungate, 1966; Demeyer and Van Nevel, 1975). There are compelling arguments on both sides and we still do not have a clear understanding of the relationship between channeling carbons and reducing equivalents away from methane production. Some of the discrepancies may be related to the fact that methods that lower methane may also alter ruminal conditions like passage rates and pH which confound interpretation of microbial growth kinetics.
Nutrient Synchrony – Simple Concept Complex Approach
Figure 6. Effect of microbial growth rate on yield of rumen bacteria from various feed components (Sniffen and Robinson, 1987).
Figure 7. Effect of different rates of digestion upon cumulative extent and time.
Efficiency of N use by ruminants is very low and much of that inefficiency occurs initially in the rumen. Readily fermentable carbohydrates (starch and sugars) are more efficient at utilization of ammonia N for microbial growth when compared with the structural carbohydrates (cellulose) (Stern and Hoover, 1979) however, the optimal ratio of fermentable carbohydrates to ammonia N is not well known. In addition to the amounts of nutrient, the timing of nutrient supply is also important. Proteolysis at rates greater than microbial protein synthesis reduce the use of dietary N and sufficient amounts of rapidly fermentable carbohydrate do not seem to lower ruminal ammonia levels which can be well above minimal concentrations. Conversely, during periods of excess carbohydrate fermentation, microbial protein synthesis has been shown to decrease (Nocek and Russell, 1988). Nutrient synchrony is attractive however attempts to coordinate fermentation of carbohydrate and N fractions in the rumen have been variable and unexpected (Kim et al., 1999a and b; Newbold and Rust, 1992). Given the complex and diverse nature of the rumen microbes synchronizing nutrient supply for all populations would be an impossible task. Furthermore, ruminants recycle tremendous amounts of N from the lower gut into the rumen thereby impacting N supply during periods of deficiency. Attempts to synchronize dietary carbohydrate and N fractions in the rumen can be affected by the recycling of nutrients as well as the changing ruminal conditions (pH and flow rates).
PLANT – MICROBE – ANIMAL INTERFACE
Efficiency of production increases with feed intake. An increase in intake also increases passage through the rumen. Digestibility of feed may be compromised at high intakes due to reduced retention times of digestible matter in the rumen. With low quality forages reducing particle size by grinding, chopping increases the potential for increased microbial digestion in the rumen. Esophageal data collected from animals fed different forages from several different studies indicate that larger particle size when compared to medium or smaller particles, from good quality forage, was associated with greater gains (Figure 8; Burns and Sollenberger, 2002). This observation is significant since typically, larger particle lengths of fiber increase residence times in the rumen and subsequent digestion but reduce intake. If one looks at the plant – microbe interface it is ostensible that the physical-chemical nature of quality fiber with larger particles allows greater microbial attachment and lesser time for fiber fermentation resulting in greater rates of passage of the larger particles. The greater attachment of microbes to the larger particles would increase the flow of microbial protein.
Figure 8. Relationship between steer average daily gains and digestible dry matter (CB = coastal bermudagrass, SG = switchgrass, FGR=rotationally stocked flaccid grass, FG = Flaccidgrass, and TF = tall fescue).
Maintenance requirements are affected by various factors and feed intake makes a significant contribution (Figure 9; Baldwin, et al., 1980). Increases in the relative body weight of the energy consuming tissues (gut and liver) increase total body energy expenditure. Figure 8 suggests that animals that could handle greater nutrient intakes without experiencing an increase in tissue size would lower their maintenance requirements significantly
Figure 9. Relationship between energy intake, maintenance energy and change in organ weight.
The cost of feeding is a significant factor in the economic viability of our animal industry. With the current surge in biofuel production feed costs have soared and are projected to remain high. Stricter regulations are forcing farmers to minimize the waste of nutrients and their subsequent impact on the environment. Over the years, we have made substantial progress in maximizing nutrient use for milk and meat production. Today, it is even more urgent to understand the feed-microbe-animal interface. Although, the complexities of the rumen microbial ecology seem daunting two factors seem paramount in achieving greater nutrient efficiency. Intake and feed quality, particularly forage nutritive value, are critical for maximizing nutrient use and efficiency of production. Knowing the nutrients in our feed and better predicting what our animals will consume will be essential to minimize losses from nutrient waste. Animals seem to respond to nutrient supply. Maintaining a healthy rumen will sustain a relatively constant pattern of nutrient supply to the animal which in turn should optimize efficiency of nutrient use.
Presented at the 24th Annual Southwest Nutrition and Management Conference, Tempe, Arizona.
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