Dietary Bioactive Lipid Compounds Rich in Menthol Alter Interactions Among Members of Ruminal Microbiota in Sheep.

Amlan K Patra,Robert Pieper,Sebastian Geiger,Zhongtang Yu,Tansol Park,Hannah-Sophie Braun,Jörg R Aschenbach

doi:10.3389/fmicb.2019.02038

Abstract

This study aimed to investigate the effects of two practically relevant doses of menthol-rich plant bioactive lipid compounds (PBLC) on fermentation, microbial community composition, and their interactions in sheep rumen. Twenty-four growing Suffolk sheep were divided into three treatments and were fed hay ad libitum plus 600 g/d of concentrate containing no PBLC (Control) or PBLC at low dose (80 mg/d; PBLC-L) or high dose (160 mg/d; PBLC-H). After 4 weeks on the diets, samples of ruminal digesta were collected and analyzed for short-chain fatty acid (SCFA), ammonia, and microbiota; microbiota being analyzed in the solid and the liquid digesta fractions separately. Ruminal SCFA and ammonia concentrations were not affected by the PBLC treatments. The microbiota in the solid fraction was more diverse than that in the liquid fraction, and the relative abundance of most taxa differed between these two fractions. In the solid fraction, phylogenetic diversity increased linearly with increased PBLC doses, whereas evenness (lowest in PBLC-L) and Simpson diversity index (greatest in PBLC-H) changed quadratically. In the liquid fraction, however, the PBLC supplementation did not affect any of the microbial diversity measurements. Among phyla, Chloroflexi (highest in PBLC-L) and unclassified_bacteria (lowest in PBLC-L) were altered quadratically by PBLC. Lachnospiraceae, Bacteroidaceae (increased linearly), BS11 (increased in PBLC-L), Christensenellaceae (decreased in PBLC treatments), and Porphyromonadaceae (increased in PBLC treatments) were affected at the family level. Among genera, Butyrivibrio increased linearly in the solid fraction, YRC22 increased linearly in the liquid fraction, whereas Paludibacter increased and BF311 increased linearly with increasing doses of PBLC in both fractions. The PBLC treatments also lowered methanogens within the classes Thermoplasmata and Euryarchaeota. Correlation network analysis revealed positive and negative correlations among many microbial taxa. Differential network analysis showed that PBLC supplementation changed the correlation between some microbial taxa and SCFA. The majority of the predicted functional features were different between the solid and the liquid digesta fractions, whereas the PBLC treatments altered few of the predicted functional gene categories. Overall, dietary PBLC treatments had little influence on the ruminal fermentation and microbiota but affected the associations among some microbial taxa and SCFA.

Highlights

Phytobiotics or plant bioactive molecules have been considered a new class of feed additives for livestock and poultry because of their several beneficial responses in animal production (Van Bibber-Krueger et al, 2016; Kumar et al, 2018; Szczechowiak et al, 2018)
Ruminal fermentation characteristics including pH, total short chain fatty acid (SCFA) concentrations and molar proportion of acetate, propionate, butyrate and other minor acids, and acetate to propionate ratio were not affected by the dietary plant bioactive lipid compounds (PBLC) supplementation (Table 2)
Various PBLC can influence the ruminal microbiota with consequences for fermentation, which may include an alteration of SCFA profile, inhibition of methane production, suppression of protein degradation and ammonia production, modification of fatty acid biohydrogenation, and mitigation of ruminal acidosis (Hutton et al, 2009; Patra, 2011; Cobellis et al, 2016)

Summary

Introduction

Phytobiotics or plant bioactive molecules have been considered a new class of feed additives for livestock and poultry because of their several beneficial responses in animal production (Van Bibber-Krueger et al, 2016; Kumar et al, 2018; Szczechowiak et al, 2018). Depending upon the type and amount of bioactive compounds used, beneficial biological effects may include modulation of ruminal fermentation (Calsamiglia et al, 2007; Mirzaei-Alamouti et al, 2016; Kazemi-Bonchenari et al, 2018), inhibition of methane production and protein degradation (Cobellis et al, 2016; Patra et al, 2017; Soltan et al, 2018), decreased growth of pathogenic microorganisms in the intestines, boosting of immunity, augmentation of antioxidant activities in the animal tissues (Chowdhury et al, 2018; Kumar et al, 2018), regulation of gastrointestinal nutrient transport and barrier function (Patra et al, 2018), improvement of growth performance (Kazemi-Bonchenari et al, 2018) and body condition (Hausmann et al, 2017, 2018), and increased quantity and quality of milk and meat (Hausmann et al, 2018; Smeti et al, 2018) Based on their molecular structures, these secondary plant compounds can be separated into several classes, namely, saponins, tannins, flavonoids, alkaloids, organosulfur compounds, terpenoids, and phenylpropanoids (Wink, 2003; Patra, 2012). Current EU regulations acknowledge that menthol supplementation is safe up to a concentration of 25 mg/kg complete feeding stuff and require detailed labeling where this concentration is exceeded (The European Commission, 2018)

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