Hops (Humulus lupulus L.) Bitter Acids: Modulation of Rumen Fermentation and Potential As an Alternative Growth Promoter

Abstract

Antibiotics can improve ruminant growth and efficiency by altering rumen fermentation via selective inhibition of microorganisms. However, antibiotic use is increasingly restricted due to concerns about the spread of antibiotic-resistance. Plant-based antimicrobials are alternatives to antibiotics in animal production. The hops plant (Humulus lupulus L.) produces a range of bioactive secondary metabolites, including antimicrobial prenylated phloroglucinols, which are commonly called alpha- and beta-acids. These latter compounds can be considered phyto-ionophores, phytochemicals with a similar antimicrobial mechanism of action to ionophore antibiotics (e.g., monensin, lasalocid). Like ionophores, the hop beta-acids inhibit rumen bacteria possessing a classical Gram-positive cell envelope. This selective inhibition causes several effects on rumen fermentation that are beneficial to finishing cattle, such as decreased proteolysis, ammonia production, acetate: propionate ratio, and methane production. This article reviews the effects of hops and hop secondary metabolites on rumen fermentation, including the physiological mechanisms on specific rumen microorganisms, and consequences for the ruminant host and ruminant production. Further, we propose that hop beta-acids are useful model natural products for ruminants because of (1) the ionophore-like mechanism of action and spectrum of activity and (2) the literature available on the plant due to its use in brewing.

Keywords: alternatives to antibiotics; antimicrobial growth promoter; feed efficiency; phytochemicals; plant secondary metabolites; rumen microbiology.

Figure 1

Simplified schematic of amino-nitrogen cycling the rumen. Processes are labeled: (1) proteolysis by microorganisms, (2) “by-pass” protein not deconstructed in the rumen, (3) deamination by microorganisms, and (4) assimilation by microorganisms for anabolic purposes. Used with permission (84).

Figure 2

Structures of hops bitter acids and biosynthetic precursors.

Figure 3

Structures of hops prenylated flavonoids.

Figure 4

Growth of Selenomonas ruminantium (circles) and Megasphaera elsdenii (triangles) in part (A), and Streptococcus bovis (squares) in part (B). Green symbols indicate hops extract (30 ppm β-acid) was added prior to inoculation. Data adapted from Ref. (83).

Figure 5

Effect of hops extract, containing 45% beta-acids (a mixture of lupulone, colupulone, and adlupulone) on ammonia production by washed (uncultivated) cell suspensions from the goat rumen. Ammonia production from peptides (triangles) or amino acids (circles) after 24 h incubation (39°C) are shown. Error bars indicate SEM. Asterisks indicate treatments that are different than the 0 ppm control. Data adapted from Ref. (84).

Figure 6

Ammonia production by mixed rumen microbes. Washed cell suspensions were incubated with peptides and amino acids. No addition (open circles), 10 µmol l^–1 monensin (blue squares), 2% w/v dried hops cones (green squares), and hops extract (60 ppm beta-acid) (green circles). Data adapted from Ref. (85).

Figure 7

The effect of hops β-acids on the growth and survival of Peptostreptococcus anaerobius (blue bars), Clostridium sticklandii (gold bars), or Clostridium aminophilum (red bars). The incubations (24 h) were carried out at pH 6.7 (A) or pH 5.6 (B), and the dashed lines indicate initial viable cell number. Extract composition is as described in Figure 5. Data adapted from Ref. (85).

Figure 8

Effect of hops β-acids on transmembrane monovalent cation gradients of the HAB, Clostridium sticklandii. The intracellular pH (squares) and intracellular potassium (circles) of energized cell suspensions. Open symbols are controls. Green symbols indicate suspensions to which β-acids were added at 0 min. Data adapted from Ref. (85).