Xylose metabolism in the pig

Abstract

It is important to understand if, and to what extent, the pig can utilize xylose as an energy source if xylanase releases free xylose in the small intestine. The experimental objectives were to determine the effects of industry-relevant dietary xylose concentrations and adaptation time on xylose retention efficiency and metabolism, diet digestibility and energy value, nitrogen balance, and hindgut fermentation. Forty-eight pigs were housed in metabolism crates and randomly assigned to one of four treatments with increasing D-xylose levels (n = 12/treatment) in 2 replications of a 22-d experiment with 3 collection periods. The control diet was xylose-free (0%), to which either 2, 4, or 8% D-xylose was added. Adaptation effects were assessed during three fecal and urine collection periods: d 5-7, 12-14, and 19-21. On d 22, pigs from the 0 and 8% treatments were euthanized; cecal and colon digesta were collected. Dietary xylose did not affect the total tract digestibility of dry matter, gross energy, or crude protein (P>0.10). Digesta short chain fatty acids concentrations and molar proportions and cecal pH were not different (P>0.10). This experiment utilized a targeted metabolomics approach to characterize and quantify urine xylose and metabolite excretion. Xylose retention decreased from 60% to 47% to 41% when pigs were fed diets containing 2, 4, or 8% xylose, respectively. In the 4 and 8% treatments, xylose retention was greater in the 2nd and 3rd collection periods compared to the 1st. A comprehensive pathway for xylose metabolism was proposed and D-threitol was confirmed as the major urinary metabolite of xylose. In conclusion, pigs can metabolize xylose, but with considerably lower efficiency than glucose, and may be able to adapt with time to utilize xylose more efficiently.

Fig 1. Two-way heat map visualization and hierarchical clustering of urine metabolite distribution.

Pigs (n = 12/treatment) were fed diets containing either 0, 2, 4, or 8% D-xylose and 3 different collection periods were utilized to represent increasing adaptation time to treatment diets. The rows display the metabolites and the columns represent individual samples. Relative urinary metabolite excretion (g/d, log transformed) is represented in the heat map by colors, which correspond to the magnitude of difference when compared with the average value for the metabolite. Only metabolites significantly (adjusted P ≤ 0.05) impacted by treatment (% dietary xylose inclusion; 0, 2, 4, or 8%), collection period (1 = d 5–7, 2 = d 12–14, 3 = d 19–21), or their interaction are displayed. Significance was determined using two-way ANOVA.

Fig 2. Proposed xylose metabolic pathway.

Dietary D-xylose concentration (0, 2, 4, or 8%) linearly increased the urinary excretion of the compounds in bold font (P < 0.0001). Non-bolded compounds were not detected in urine samples. The color of the block arrow indicates average excretion amount of the compound in pigs from the 8% xylose treatment; red: 40 g/d, orange: 13 g/d, yellow: 0.3 g/d, white: < 0.2 g/d. Solid connecting arrows represent reactions confirmed in mammals and dashed connecting lines represent presumed reactions based on reactions occurring in microorganisms. Highlighted enzymes: 1) D-xylose 1-dehydrogenase (1.1.1.179), 2) L-gulonate 3-dehydrogenase (1.1.1.45), 3) D-erythrulose reductase (1.1.1.162), 4) aldose/aldehyde reductase (1.1.1.21), 5) L-xylulose reductase (1.1.1.10), 6) xylitol dehydrogenase (1.1.1.14), 7) xylulokinase (2.7.1.17), and 8) D-ribose dehydrogenase (1.1.1.115). The boxes indicate KEGG metabolic pathway classifications [36].

Fig 3. Allocation of urine gross energy (GE) from xylose, metabolites, and nitrogen (N)-containing compounds.

Pigs (n = 12/treatment) were fed diets containing either 0, 2, 4, or 8% D-xylose. The presented values are treatment averages across 3 different collection periods. The effect of treatment was significant for all variables (P ≤ 0.042). Dietary xylose concentration linearly impacted each variable (linear contrast P ≤ 0.012) except the unassociated fraction. Increasing dietary xylose concentration increased the urine GE (kJ/l) contributed from xylose (SEM = 17.4), threitol (SEM = 8.6), and the combination of all lesser metabolites (xylitol, xylonic acid, and xylulose; SEM = 0.3), but decreased the GE contributed from N-containing compounds (SEM = 17.0). The amount of urine GE unexplained by the xylose, its metabolites, or N-containing compounds (SEM = 45.3) was not different among the 0, 2, and 4% treatments (P ≥ 0.416) but was lower in the 8% treatment (P = 0.042).