Effect of environmental factors and influence of rumen and hindgut biogeography on bacterial communities in steers

Abstract

Feces from cattle production are considered important sources of bacterial contamination of food and the environment. Little is known about the combined effects of arctic temperatures and fodder tannins on rumen and hindgut bacterial populations. Individual rumen liquor and rectal fecal samples from donor steers fed either alfalfa silage or sainfoin (Onobrychis viciifolia Scop.) silage and water ad libitum were collected weekly on the first three sampling days and fortnightly afterwards. The daily ambient temperatures were registered and averaged to weekly mean temperatures. Steers fed sainfoin silage had lower (P < 0.05) concentrations of branched-chain volatile fatty acids (VFA) than those fed alfalfa silage. All VFA concentrations were higher (P < 0.001) in rumen liquor samples than in fecal samples. The interaction of sample type and diet showed a significant effect (P < 0.05) on the proportions of the bacterial community that were from the phyla Proteobacteria and Verrucomicrobia. Ambient temperature had an indirect effect (P < 0.05) on the phylum Firmicutes, as it affected its proportional balance. The bacterial population diversity in samples appeared to decrease concurrently with the ambient temperature. The phylum Firmicutes explained the first principal component at 64.83 and 42.58% of the total variance in rumen liquor and fecal samples, respectively. The sample type had a larger effect on bacterial communities than diet and temperature. Certain bacterial populations seemed to be better adapted than others to environmentally adverse conditions, such as less access time to nutrients due to higher motility and rate of passage of digesta caused by extreme temperatures, or antimicrobials such as tannins, possibly due to an influence of their biogeographical location within the gut.

FIG. 1.

Phylogenetic tree based on the proportions of the phyla detected in the bacterial communities in the rumen liquor (RumLiq) and fecal (Faec) samples of steers fed either alfalfa silage or sainfoin silage, by T-RFLP analysis. Relationships were based on data from 16S rRNA gene sequences. The paired fractions on the y axis indicate rumen liquor sampling observations (upper fractions) and fecal sampling observations (lower fractions). The denominators in these values are the proportions of the total number of observations in the cluster; numerators are the total numbers of the predominant sampling observations.

FIG. 2.

Fluctuation of the ambient temperature (°C) that beef steers experienced during the present experiment.

FIG. 3.

Effect of ambient temperature on the proportions of phylum Firmicutes and its order Lactobacillales in bacterial communities in fecal and rumen liquor samples from steers fed either alfalfa silage or sainfoin silage. Histograms show results for fecal samples from steers fed alfalfa silage (A), rumen liquor samples from steers fed alfalfa silage (B), fecal samples from steers fed sainfoin silage (C), and rumen liquor samples from steers fed sainfoin silage (D). Firmicutes is a bacterial phylum; Lactobacillales is a bacterial order under class Bacilli belonging to phylum Firmicutes.

FIG. 4.

Three-dimensional scatter plot of the first and second principal components calculated on the natural log-transformed proportions of the taxons in the bacterial communities detected in the rumen liquor and fecal samples of steers fed on either sainfoin silage or alfalfa silage. Principal component data were plotted against ambient temperature. PC1, principal component 1 (x axis); PC2, principal component 2 (y axis); z axis, ambient temperature. Symbols denote results for groups in pens as follows: square, pen 1; circle, pen 2; plus sign, pen 3; diamond, pen 4. Colors of symbols represent weeks during the sampling: yellow, week 1; blue, week 2; brown, week 3; pink, week 4; black, week 5; orange, week 6. Steers in pens 1 and 3 were fed sainfoin silage, while steers in pens 2 and 4 were fed alfalfa silage. Blue contour color denotes rumen liquor samples (A), and red contour color denotes fecal samples (B).