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Transcriptional changes detected in fecal RNA of neonatal dairy calves undergoing a mild diarrhea are associated with inflammatory biomarkers.

ABSTRACT: After birth, a newborn calf has to adapt to an extrauterine life characterized by several physiological changes. In particular, maturation of the gastrointestinal tract in a new environment loaded with potential pathogens, which can predispose neonatal calves to develop diarrhea, and is a major cause of morbidity and mortality during the first 4 wks of life. We aimed to investigate the inflammatory adaptations at a transcriptomic level in the gastrointestinal (GI) tract to a mild diarrhea in neonatal dairy calves using RNA isolated from fresh fecal samples. Eight newborn Jersey male calves were used from birth to 5 wks of age and housed in individual pens. After birth, calves received 1.9 L of colostrum from their respective dams. Calves had ad-libitum access to water and starter grain (22% CP) and were fed twice daily a total of 5.6 L pasteurized whole milk. Starter intake, body weight (BW), fecal score, withers height (WH), and rectal temperature (RT) were recorded throughout the experiment. Blood samples were collected weekly for metabolic and inflammatory profiling from wk 0 to wk 5. Fresh fecal samples were collected weekly and immediately flash frozen until RNA was extracted using a Trizol-based method, and subsequently, an RT-qPCR analysis was performed. Orthogonal contrasts were used to evaluate linear or quadratic effects over time. Starter intake, BW, and WH increased over time. Fecal score was greatest (2.6 ± 0.3) during wk 2. The concentrations of IL-6, ceruloplasmin, and haptoglobin had a positive quadratic effect with maximal concentrations during wk 2, which corresponded to the maximal fecal score observed during the same time. The concentration of serum amyloid A decreased over time. The mRNA expression of the proinflammatory related genes TLR4, TNFA, IL8, and IL1B had a positive quadratic effect of time. A time effect was observed for the cell membrane sodium-dependent glucose transporter SLC5A1, for the major carbohydrate facilitated transporter SLC2A2, and water transport function AQP3, where SLC5A1 and AQP3 had a negative quadratic effect over time. Our data support the use of the fecal RNA as a noninvasive tool to investigate intestinal transcriptomic profiling of dairy calves experiencing diarrhea, which would be advantageous for future research including nutritional effects and health conditions.

SUBMITTER: Rosa F

PROVIDER: S-EPMC5786293 | biostudies-other | 2018

REPOSITORIES: biostudies-other

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Transcriptional changes detected in fecal RNA of neonatal dairy calves undergoing a mild diarrhea are associated with inflammatory biomarkers.

Rosa Fernanda F Busato Sebastiano S Avaroma Fatima C FC Linville Kali K Trevisi Erminio E Osorio Johan S JS Bionaz Massimo M

PloS one 20180126 1

After birth, a newborn calf has to adapt to an extrauterine life characterized by several physiological changes. In particular, maturation of the gastrointestinal tract in a new environment loaded with potential pathogens, which can predispose neonatal calves to develop diarrhea, and is a major cause of morbidity and mortality during the first 4 wks of life. We aimed to investigate the inflammatory adaptations at a transcriptomic level in the gastrointestinal (GI) tract to a mild diarrhea in neo ...[more]

PMID: 29373601

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Project description:Microbiota plays a critical role in the overall growth performance and health status of dairy cows, especially during their early life. Several studies have reported that fecal microbiome of neonatal calves is shifted by various factors such as diarrhea, antibiotic treatment, or environmental changes. Despite the importance of gut microbiome, a lack of knowledge regarding the composition and functions of microbiota impedes the development of new strategies for improving growth performance and disease resistance during the neonatal calf period. In this study, we utilized next-generation sequencing to monitor the time-dependent dynamics of the gut microbiota of dairy calves before weaning (1-8 weeks of age) and further investigated the microbiome changes caused by diarrhea. Metagenomic analysis revealed that continuous changes, including increasing gut microbiome diversity, occurred from 1 to 5 weeks of age. However, the composition and diversity of the fecal microbiome did not change after 6 weeks of age. The most prominent changes in the fecal microbiome composition caused by aging at family level were a decreased abundance of Bacteroidaceae and Enterobacteriaceae and an increased abundance of Prevotellaceae. Phylogenetic investigation of communities by reconstruction of unobserved states (PICRUSt) analysis indicated that the abundance of microbial genes associated with various metabolic pathways changed with aging. All calves with diarrhea symptoms showed drastic microbiome changes and about a week later returned to the microbiome of pre-diarrheal stage regardless of age. At phylum level, abundance of Bacteroidetes was decreased (p = 0.09) and that of Proteobacteria increased (p = 0.07) during diarrhea. PICRUSt analysis indicated that microbial metabolism-related genes, such as starch and sucrose metabolism, sphingolipid metabolism, alanine aspartate, and glutamate metabolism were significantly altered in diarrheal calves. Together, these results highlight the important implications of gut microbiota in gut metabolism and health status of neonatal dairy calves.

Project description:BackgroundDiarrhea is a major cause of morbidity and mortality in young calves, resulting in considerable economic loss for dairy farms. To determine if some gut microbes might have resistance to dysbiotic process with calf diarrhea by dictating the microbial co-occurrence patterns from birth to post-weaning, we examined the dynamic development of the gut microbiota and diarrhea status using two animal trials, with the first trial having 14 Holstein dairy calves whose fecal samples were collected 18 times over 78 d from birth to 15 d post-weaning and the second trial having 43 Holstein dairy calves whose fecal samples were collected daily from 8 to 18 days of age corresponding to the first diarrhea peak of trial 1.ResultsMetataxonomic analysis of the fecal microbiota showed that the development of gut microbiota had three age periods with birth and weaning as the separatrices. Two diarrhea peaks were observed during the transition of the three age periods. Fusobacteriaceae was identified as a diarrhea-associated taxon both in the early stage and during weaning, and Clostridium_sensu_stricto_1 was another increased genus among diarrheic calves in the early stage. In the neonatal calves, Prevotella_2 (ASV4 and ASV26), Prevotella_9 (ASV43), and Alloprevotella (ASV14) were negatively associated with Clostridium_sensu_stricto_1 (ASV48), the keystone taxa of the diarrhea-phase module. During weaning, unclassified Muribaculaceae (ASV28 and ASV44), UBA1819 (ASV151), Barnesiella (ASV497), and Ruminococcaceae_UCG-005 (ASV254) were identified being associated with non-diarrheic status, and they aggregated in the non-diarrhea module of co-occurrence patterns wherein unclassified Muribaculaceae (ASV28) and Barnesiella (ASV497) had a direct negative relationship with the members of the diarrhea module.ConclusionsTaken together, our results suggest that the dynamic successions of calf gut microbiota and the interactions among some bacteria could influence calf diarrhea, and some species of Prevotella might be the core microbiota in both neonatal and weaning calves, while species of Muribaculaceae might be the core microbiota in weaning calves for preventing calf diarrhea. Some ASVs affiliated with Prevotella_2 (ASV4 and ASV26), Prevotella_9 (ASV43), Alloprevotella (AVS14), unclassified Muribaculaceae (ASV28 and ASV44), UBA1819 (ASV151), Ruminococcaceae_UCG-005 (ASV254), and Barnesiella (ASV497) might be proper probiotics for preventing calf diarrhea whereas Clostridium_sensu_stricto_1 (ASV48) might be the biomarker for diarrhea risk in specific commercial farms.

Project description:Gastrointestinal disease (GI) is the most common illness in pre-weaned dairy calves. Studies have associated the fecal microbiome composition with health status, but it remains unclear how the microbiome changes across different levels of GI disease and breeds. Our objective was to associate the clinical symptoms of GI disease with the fecal microbiome. Fecal samples were collected from calves (n = 167) of different breeds (Holstein, Jersey, Jersey-cross and beef-cross) from 4-21 d of age. Daily clinical evaluations assessed health status. Calves with loose or watery feces were diagnosed with diarrhea and classified as bright-sick (BS) or depressed-sick (DS) according to behavior. Calves with normal or semiformed feces and no clinical illness were classified as healthy (H). One hundred and three fecal samples were obtained from consistently healthy calves and 64 samples were from calves with diarrhea (n = 39 BS; n = 25 DS). The V3-V4 region of 16S rRNA gene was sequenced and analyzed. Differences were identified by a linear-mixed effects model with a negative binomial error. DS and Jersey calves had a higher relative abundance of Streptococcus gallolyticus relative to H Holstein calves. In addition, DS calves had a lower relative abundance of Bifidobacterium longum and an enrichment of Escherichia coli. Species of the genus Lactobacillus, such as an unclassified Lactobacillus, Lactobacillus reuteri, and Lactobacillus salivarius were enriched in calves with GI disease. Moreover, we created a model to predict GI disease based on the fecal microbiome composition. The presence of Eggerthella lenta, Bifidobacterium longum, and Collinsella aerofaciens were associated with a healthy clinical outcome. Although lactobacilli are often associated with beneficial probiotic properties, the presence of E. coli and Lactobacillus species had the highest coefficients positively associated with GI disease prediction. Our results indicate that there are differences in the fecal microbiome of calves associated with GI disease severity and breed specificities.

Project description:Calf diarrhea is a leading cause of death in preweaning calves and it causes major economic losses to producers. Acidified milk has been shown to have beneficial effects on health and growth parameters in calves but there is little research into its effects on the microbiota, and few studies on the use of acidified colostrum. The purpose of this study was to compare how feeding acidified colostrum to calves at birth affects fecal microbiota from birth through 8 wk of age compared with calves fed nonacidified colostrum. In this study, 5 calves received acidified colostrum (treated group) and 5 calves received nonacidified colostrum (control group) at birth and at 12 h of age. All calves were subsequently fed acidified whole milk until weaning at 8 wk of age and had access to starter grain starting at d 3 and throughout the study. Fecal samples were collected at 24 h, 48 h, and at 1, 2, 3, 4, 5, 6, 7, and 8 wk of age. Samples were extracted for genomic DNA, PCR-amplified for the V1-V2 region of the 16S rRNA bacteria gene, sequenced, and analyzed using QIIME2. Bacterial richness (estimated by number of observed species) and bacterial diversity (estimated by Shannon diversity index) differed between time points but not between treatment groups, and both increased over time. Weighted and unweighted UniFrac analysis showed differences between bacterial communities across time points and treatments. Across all time points (lmer test), 6 bacterial genera were different between treatments: Faecalibacterium and unclassified Clostridiaceae were more abundant, whereas Atopobium, Collinsella, CF231, and unclassified Veillonellaceae were less abundant in treated versus control calves. Faecalibacterium is a butyrate-producing bacterium that has been linked to decreased prevalence of diarrhea in calves. Our results indicate that there is considerable flux in the calf microbiome through the neonatal period and weaning transition but that feeding acidified colostrum followed by acidified whole milk allowed early colonization of Faecalibacterium. Further studies are needed to verify the positive benefits of promoting Faecalibacterium on improving the health of preweaning calves.

Dataset Information

Transcriptional changes detected in fecal RNA of neonatal dairy calves undergoing a mild diarrhea are associated with inflammatory biomarkers.

Publications

Transcriptional changes detected in fecal RNA of neonatal dairy calves undergoing a mild diarrhea are associated with inflammatory biomarkers.

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