Effect of an intramammary lipopolysaccharide challenge on the hindgut microbial composition and fermentation of dairy cattle experiencing intermittent subacute ruminal acidosis

Abstract

Feeding grain-rich diets often results in subacute ruminal acidosis (SARA), a condition associated with ruminal dysbiosis and systemic inflammation. Yet, the effect of SARA on hindgut microbiota, and whether this condition is aggravated by exogenous immune stimuli, is less understood. Therefore, the aims of this study were to determine the effects of an intermittent high-grain SARA model on the hindgut microbial community, and to evaluate whether the effects of SARA on the fecal microbiome and fermentation were further affected by an intramammary lipopolysaccharide (LPS) challenge. A total of 18 early-lactating Simmental cows were divided into 3 groups (n = 6); 2 were fed a SARAinducing feeding regimen (60% concentrate), 1 was fed a control (CON) diet (40% concentrate). On d 30, 1 SARA group (SARA-LPS) and the CON group (CON-LPS) were intramammarily challenged with a single dose of 50 µg of LPS from Escherichia coli O26:B6, whereas the remaining 6 SARA cows (SARA-PLA) received a placebo. Using a longitudinal randomized controlled design, with grouping according to parity and days in milk), statistical analysis was performed with baseline measurements used as a covariate in a mixed model procedure. The SARA-inducing feeding challenge resulted in decreased fecal pH and increased butyrate as a proportion of total short-chain fatty acids in the feces. On d 30, SARA-challenged cows had decreased fecal diversity as shown by the Shannon and Chao1 indices and a decrease in the relative abundance of Euryarchaeota and cellulolytic genera, and numerical increases in the relative abundance of several Firmicutes associated with starch and secondary fermentation. The LPS challenge did not affect the fecal pH and short-chain fatty acids, but increased the Chao1 richness index in an interaction with the SARA challenge, and affected the relative abundance of Verrucomicrobia (1.13%), Actinobacteria (0.19%), and Spirochaetes (0.002%), suggesting an effect on the microbial ecology of the hindgut during SARA conditions. In conclusion, the SARA-inducing feeding regimen promoted important microbial changes at d 30, including reduced diversity and evenness compared with CON, whereas the external LPS challenge led to changes in the microbial community without affecting fecal fermentation properties.

Effects of high-grain diet feeding on mucosa-associated bacterial community and gene expression of tight junction proteins and inflammatory cytokines in the small intestine of dairy cattle

“…Furthermore, it is noteworthy that the LPS concentrations in the jejunum and ileum of the 2 groups of dairy cows were 154,020.5 endotoxin units (EU) per gram and 193,733.1 EU/g respectively, which were more than 400 times higher than the LPS concentration of 2,517.3 EU/g in the duodenum. Petri et al (2021) reported that the acidic conditions in the abomasum deactivate LPS. In general, these results indicate that the accumulation of LPS in the small intestine was physiologically independent of HG feeding, and the increase in LPS concentrations in the jejuna and ilea of the HG group may have been due to excessive fermentation and overgrowth of bacteria.…”

“…Grain-induced SARA may also increase the risk of low DMI and milk fat percentage as well as hepatic abscesses, laminitis, and other diseases, which could ultimately lead to significant financial losses in the dairy industry (Gozho et al, 2007;Kleen and Cannizzo, 2012). Previous studies have demonstrated that high-grain diets disrupt the balance of the epithelium-associated microbial communities and result in epithelial injury in the rumen and hindgut of dairy cattle (Li et al, 2012;Petri et al, 2021). However, little information is available about changes in the microbial communities and health of the small intestines of dairy cows fed high-grain diets (Nozière et al, 2014), despite Effects of high-grain diet feeding on mucosa-associated bacterial community and gene expression of tight junction proteins and inflammatory cytokines in the small intestine of dairy cattle the small intestine being the most important digesting and absorbing organ in the gastrointestinal tract.…”

Susceptibility of dairy cows to subacute ruminal acidosis is reflected in both prepartum and postpartum bacteria as well as odd- and branched-chain fatty acids in feces

“…We hypothesized these rumen pH differences could result in a distinct bacterial pattern in the hindgut (assessed by feces), as SARA is often associated with an increased amount of fermentable carbohydrates by-passing the rumen toward the hindgut, which could result in increased risk of hindgut acidosis, the development of diarrhea, and disturbance of hindgut bacteria [ 1 , 9 – 11 ]. In previous studies, a grain-induced SARA challenge reduced the richness, evenness, and diversity of bacteria, and increased the abundance of nonstructural carbohydrates degraders (e.g., Prevotella albensis ) in the feces [ 46 , 47 ]. In the current study, no differences were observed between the groups in alpha diversity of fecal bacteria (i.e., observed ASV, Faith_pd, Shannon index, or evenness index) on d 21 postpartum.…”

“…This may be another illustration of the less harsh SARA conditions in the current trial compared with experimental, grain-induced SARA or post-ruminal infusion of easily fermentable carbohydrates to induce hindgut acidosis [ 52 ]. In these trials, the decreased hindgut/fecal pH as observed in SARA cows compared with non-SARA cows [ 8 , 48 , 54 ] could have enhanced proliferation of pathogenic taxa, especially Escherichia as the most common fecal pathogen [ 46 , 55 – 57 ]. Thus, these results indicated that variation in reticular pH during a gradual build-up of the compound feed during a 3-week postpartum period was not associated with differences in fecal pH and VFA concentration, while some differences in the elative abundance of fecal genera were observed.…”

Effect of hydrogenated fat-embedded calcium gluconate on lactation performance in dairy cows

“…Historically, the rumen has been a key focus area for advancements in many aspects of ruminant nutrition, however there is growing interest in the role of the hindgut in relation to overall animal health and performance. Due to a variety of physiological and functional factors, the hindgut is typically considered to be less robust than the rumen with regards to maintaining gut barrier integrity (as recently reviewed by Sanz-Fernandez et al, 2020), and is thus more susceptible to dysbiosis, such as that resulting from acidotic events (e.g., Petri et al, 2021, van Gastelen et al, 2021. A preventative nutritional intervention worth exploring is the application of prebiotic compounds (Gibson et al, 2004) specifically targeting the hindgut, translating advancements from human nutrition and applications used in non-ruminant agricultural species (as reviewed by Gaggia et al, 2010, Uyeno et al, 2015.…”