*Bill Mahanna, Ph.D., Dipl ACAN, is a collaborative faculty member at Iowa State University and a board-certified nutritionist for DuPont Pioneer based in Johnston, Iowa. To expedite answers to questions concerning this article or to submit ideas for future articles, please direct inquiries to Feedstuffs, Bottom Line of Nutrition, 7900 International Dr., Suite 650, Bloomington, Minn. 55425, or email [email protected]
I ADDRESSED the topic of microbial efficiency and energy spilling more than a year ago, but a paper by Dr. Tim Hackmann at the recent Florida Ruminant Nutrition Symposium reinvigorated my interest and added more insight.
My interest in this topic is somewhat borne out of personal frustration with inputting individual feedstuff analyses into various models that balance nutrients but struggle at predicting a feedstuff's associative effects on the yield of ruminal microbial biomass and, ultimately, herd production levels.
Ruminal fermentation is a process whereby microbes convert carbohydrates and other substances to volatile fatty acids (VFAs) and generate adenosine triphosphate (ATP). The ability of microbes to survive (maintenance) and reproduce is driven by the energy from ATP hydrolysis (Russell, 2002).
Rumen microbes are not particularly efficient with the ATP energy they harvest from fermentation, directing as little as 33% of the ATP towards synthesis of microbial protein (Hackmann, 2014). Directing more ATP to protein synthesis would increase yields of microbial biomass and improve the efficiency of the entire diet.
When bacteria grow slowly, a large portion of this energy is used to maintain cells. Fiber-digesting bacterial species have a lower maintenance energy requirement than non-fiber carbohydrate (NFC)-digesting bacteria. However, fiber-digesting bacteria grow more slowly than NFC-digesting bacteria, and the rapid growth by NFC populations minimizes their overall maintenance expenditures and heat production (Feedstuffs, Dec. 10, 2012).
Microbial growth rates increase with increased ruminal feed passage rates. This reduces the negative impact of maintenance costs given that, during low growth rates of 5% per hour, maintenance can account for more than 30% of energy expended but only 10% during higher growth rate conditions of 20% per hour (Hackmann, 2014).
The overall efficiency of microbial cell growth is estimated to be about 12%, with the remaining 88% dissipated as heat (Russell, 2007). This loss of energy as heat is one example of microbial energy spilling (loss).
Excess energy can be stored by microbes in the form of glycogen, which has essentially the same structure as starch (Hall, 2012). While glycogen can be mobilized for later growth needs, it is a wasteful process because ATP is irreversibly spent to synthesize glycogen (Hackmann, 2014).
The energy toll to store carbohydrate as glycogen costs one ATP per hexose, which is 25-50% of the total ATP from the fermentation of a hexose (Hall, 2012).
Microbial glycogen storage has been shown to increase as rapidly available carbohydrate levels increase (Prins and Van Hoven, 1977). Conversely, glycogen levels have been shown to decrease as dietary protein is increased (McAllan and Smith, 1974), presumably because the synchrony of nutrients is allowing energy to be directed to microbial growth rather than glycogen storage.
There is also a need to better understand how ruminal passage rates affect the fate of microbial glycogen — whether it is fermented and recycled in the rumen or passed on to intestinal digestion (Hall, 2012).
While moderate excesses of energy can be stored as glycogen, large excesses may be burned off as heat in a microbial process called energy spilling. Some theorize that bacteria that spill energy may be better suited for rapid growth when nutrient limitations no longer exist.
While the evolutionary function of energy spilling is not fully understood, it is clear that spilling produces only heat and no microbial protein (Hackmann, 2014). If energy is in excess and microbial growth is limited by other dietary factors, e.g., amino acids or rumen-degradable protein (RDP), the rate of stationary (resting) cell metabolism can exceed maintenance levels by nearly 18-fold (Russell, 2007).
A shortfall of RDP may exist today in dairy diets with high corn silage inclusion levels. As corn silage increasingly replaces alfalfa or grass silage, replacing the RDP typically provided from alfalfa/grass silage becomes more of an issue.
Fine-tuning the RDP levels may be further challenged, given the commonly held concern of nutritionists and laboratories about the ability of the Borate-Buffer Method to accurately measure the soluble protein needed to fuel microbial growth.
Personal experience has shown me that improvements in herd production occurred when additional RDP was added to diets despite the Borate-Buffer Method indicating that an adequate soluble protein level was present in the diet, even though the microbial soluble protein method provided on the Fermentrics analysis showed lower-than-recommended levels.
Dietary RDP levels may also need adjusting throughout the feeding season in response to the increase in ruminal starch digestibility observed over time in ensiled corn silage and high-moisture grains.
Energy spilling is most common when cells are limited for nutrients other than energy, but even rapidly growing cells can spill a significant amount of energy (Russell, 2007). The author has observed an unexplained lack of microbial biomass yield in certain high-quality alfalfa silages, suggesting that there may be other growth-limiting factors besides nitrogen-based compounds. The only cells that do not seem to spill energy are those limited for energy (Russell, 2002).
Streptococcus bovis is typically associated with ruminal acidosis due to its unmatched growth rate when fermenting carbohydrate to lactate and reducing rumen pH to levels where only acid-tolerant lactobacillus can survive (Hackmann, 2014).
However, it is also known that non-growing S. bovis are capable of "spilling" as much ATP as is utilized by those that are rapidly growing (Russell, 2007). This is because S. bovis lacks the ability to store energy as glycogen, so spilling inevitably occurs when growth is limited from the futile cycle of protons out of the cell, only to return later (proton pump) with the net production of heat (Hackmann, 2014).
Although S. bovis is associated with high-concentrate diets, it is still present in high-forage diets and, thus, is a natural target for reduction in an attempt to improve overall dietary efficiency.
It is additionally known that other populations of microbial villains are also responsible for spilling energy even when lactate is not produced (Hackmann, 2014). To date, there has been limited success in reducing populations of rumen microbes known for their energy spilling tendencies through the use of antibiotics, bacteriophages or vaccines.
One area that merits more investigation involves in vitro evidence that live yeast (Saccharomyces cerevisiae) competes with S. bovis for carbohydrates, but it is not known how extensive the possible competitive inhibition is.
The Bottom Line
One approach to increasing the efficiency of ruminal microbial biomass production is to minimize the impact of bacterial maintenance expenditure, glycogen storage and energy spilling.
Laboratory methods, such as Fermentrics, that allow for direct measurement of microbial biomass can prove extremely helpful in understanding the associative effects of dietary ingredients and why some diets perform as predicted while others don't seem to elicit the expected response.
It may be that these associative effects are influencing whether ATP is being efficiently utilized for microbial growth, stored as glycogen for later use or wasted via energy spilling due to a lack of synchrony of dietary nutrients.
Hackmann, T.J. 2014. Strategies to improve rumen microbial efficiency. Proceedings of 25th Florida Ruminant Nutrition Symposium. Gainesville, Fla.
Hall, M.B. 2012. Protein and carbohydrate interactions in the rumen — Protein does what? Proceedings of 33rd Western Nutrition Conference. Sept. 19-20. Winnipeg, Man.
McAllan, A.B., and R.H. Smith. 1974. Carbohydrate metabolism in the ruminant: Bacterial carbohydrates formed in the rumen and their contribution to digesta entering the duodenum. Br. J. Nutr. 31:77-88.
Prins, R.A., and W. Van Hoven. 1977. Carbohydrate fermentation by the rumen ciliate Isotricha prostoma. Protistologica 13:549-556.
Russell, J.B. 2002. Rumen Microbiology & Its Role In Ruminant Nutrition. Cornell University.
Russell, J.B. 2007. Can the heat of ruminal fermentation be manipulated to decrease heat stress? Proceedings of 22nd Annual Southwest Nutrition & Management Conference. Feb. 22-23. Tempe, Ariz.