| Literature DB >> 31608024 |
Ahmed Elolimy1,2,3, Abdulrahman Alharthi1,2, Mohamed Zeineldin4,5, Claudia Parys6, Ariane Helmbrecht6, Juan J Loor1,2,7.
Abstract
To our knowledge, most studies demonstrating the role of manipulating maternal nutrition on hindgut (i.e., large intestine) microbiota in the offspring have been performed in non-ruminants. Whether this phenomenon exists in cattle is largely unknown. Therefore, the objectives of the current study were to evaluate the impact of maternal post-ruminal supply of methionine during late-pregnancy in dairy cows on fecal microbiota and metabolome in neonatal calves, and their association with body development and growth performance during the preweaning period. To achieve this, heifer calves, i.e., neonatal female offspring, born to Holstein cows receiving either a control (CON) diet (n = 13) or CON plus rumen-protected methionine (MET; Evonik Nutrition & Care GmbH) during the last 28 days of pregnancy were used. Fecal samples from heifers were collected from birth until 6 weeks of age, i.e., the preweaning period. Fecal microbiota was analyzed with QIIME 2 whereas fecal metabolites were measured using an untargeted LC-MS approach. At birth, MET heifers had greater (P ≤ 0.05) BW, HH, and WH. During the preweaning period, no differences between groups were detected for starter intake (P = 0.77). However, MET heifers maintained greater (P ≤ 0.05) BW, HH and tended (P = 0.06) to have greater WH and average daily gain (ADG) (P = 0.10). Fecal microbiota and metabolome profiles through 42 days of age in MET heifers indicated greater capacity for hindgut production of endogenous antibiotics and enhanced hindgut functionality and health. Enhancing maternal post-ruminal supply of methionine during late-gestation in dairy cows has a positive effect on hindgut functionality and health in their offspring through alterations in the fecal microbiota and metabolome without affecting feed intake. Those alterations could limit pathogen colonization of the hindgut while providing essential nutrients to the neonate. Together, such responses contribute to the ability of young calves to achieve better rates of nutrient utilization for growth.Entities:
Keywords: calves; cows; gut; metabolomics; methionine; microbiota; prenatal; preweaning
Year: 2019 PMID: 31608024 PMCID: PMC6761860 DOI: 10.3389/fmicb.2019.02159
Source DB: PubMed Journal: Front Microbiol ISSN: 1664-302X Impact factor: 5.640
Nutrient composition and amino acid profiles (mean ± standard deviation) of milk replacer (Advance Excelerate, Milk Specialties, Carpentersville, IL, United States) and starter grain (Ampli-Calf Starter 20; Purina Animal Nutrition, Shoreview, MN, United States) fed during preweaning period to heifer calves born to cows offered a control diet (CON, n = 13) or CON supplemented with ethyl-cellulose rumen-protected methionine (MET, n = 13; Mepron® at 0.09% of diet DM; Evonik Nutrition & Care GmbH, Germany) during the last 28 days of pregnancy.
| DM, g/kg | 946 ± 11 | 908 ± 27 |
| CP, g/kg | 272 ± 44 | 209 ± 23 |
| Arginine | 0.84 ± 0.07 | 1.39 ± 0.03 |
| Histidine | 0.59 ± 0.02 | 0.55 ± 0.01 |
| Isoleucine | 1.60 ± 0.06 | 0.82 ± 0.01 |
| Leucine | 2.90 ± 0.07 | 1.52 ± 0.03 |
| Lysine | 2.30 ± 0.12 | 1.07 ± 0.02 |
| Methionine | 0.53 ± 0.02 | 0.29 ± 0.01 |
| Phenylalanine | 1.01 ± 0.02 | 0.98 ± 0.01 |
| Threonine | 1.83 ± 0.04 | 0.77 ± 0.02 |
| Valine | 1.59 ± 0.03 | 0.97 ± 0.01 |
| Aspartate | 2.89 ± 0.07 | 2.00 ± 0.05 |
| Alanine | 1.36 ± 0.03 | 0.97 ± 0.02 |
| Cysteine | 0.64 ± 0.02 | 0.34 ± 0.01 |
| Glutamate | 4.68 ± 0.15 | 1.07 ± 0.02 |
| Glycine | 0.60 ± 0.03 | 0.98 ± 0.01 |
| Proline | 1.64 ± 0.04 | 1.14 ± 0.02 |
| Serine | 1.47 ± 0.05 | 0.99 ± 0.03 |
Body measurements at birth in heifer calves born to cows offered a control diet (CON, n = 13) or CON supplemented with ethyl-cellulose rumen-protected methionine (MET, n = 13; Mepron® at 0.09% of diet DM; Evonik Nutrition & Care GmbH, Germany) during last 28 days of pregnancy.
| Body weight (kg) | 40.08b | 43.79a | 0.91 | 0.04 |
| Body length (cm) | 109.30 | 109.90 | 1.57 | 0.80 |
| Hip height (cm) | 78.43b | 82.32a | 0.64 | < 0.01 |
| Hip width (cm) | 16.14 | 15.66 | 0.39 | 0.43 |
| Wither height (cm) | 75.63b | 78.17a | 0.70 | 0.03 |
Body measurements and growth performance during preweaning period in heifer calves born to cows offered a control diet (CON, n = 13) or CON supplemented with ethyl-cellulose rumen-protected methionine (MET, n = 13; Mepron® at 0.09% of diet DM; Evonik Nutrition & Care GmbH, Germany) during last 28 days of pregnancy.
| 1 | 42.03 | 44.26 | 1.08 | 0.05 | <0.01 | 0.15 |
| 2 | 44.56 | 46.76 | 1.08 | |||
| 3 | 49.32 | 50.70 | 1.08 | |||
| 4 | 54.87 | 56.24 | 1.08 | |||
| 5 | 58.78 | 62.65 | 1.08 | |||
| 6 | 63.33 | 67.57 | 1.08 | |||
| 1 | 111.40 | 112.06 | 1.61 | 0.34 | <0.01 | 0.29 |
| 2 | 114.09 | 116.32 | 1.61 | |||
| 3 | 117.44 | 118.97 | 1.61 | |||
| 4 | 121.07 | 122.25 | 1.61 | |||
| 5 | 123.47 | 126.30 | 1.61 | |||
| 6 | 126.73 | 130.15 | 1.61 | |||
| 1 | 80.31 | 83.19 | 0.71 | 0.02 | <0.01 | 0.36 |
| 2 | 81.74 | 84.74 | 0.71 | |||
| 3 | 83.32 | 85.65 | 0.71 | |||
| 4 | 84.70 | 86.52 | 0.71 | |||
| 5 | 86.61 | 88.25 | 0.71 | |||
| 6 | 88.23 | 90.37 | 0.71 | |||
| 1 | 16.46 | 16.40 | 0.32 | 0.63 | <0.01 | 0.81 |
| 2 | 17.84 | 17.70 | 0.32 | |||
| 3 | 18.72 | 18.36 | 0.32 | |||
| 4 | 19.33 | 19.05 | 0.32 | |||
| 5 | 20.11 | 19.80 | 0.32 | |||
| 6 | 20.77 | 20.84 | 0.32 | |||
| 1 | 76.90 | 78.59 | 0.69 | 0.06 | <0.01 | 0.28 |
| 2 | 77.66 | 80.03 | 0.69 | |||
| 3 | 79.75 | 81.47 | 0.69 | |||
| 4 | 81.00 | 82.34 | 0.69 | |||
| 5 | 82.49 | 84.16 | 0.69 | |||
| 6 | 84.00 | 85.94 | 0.69 | |||
| 1 | 0.02 | 0.25 | 0.10 | 0.10 | <0.01 | 0.27 |
| 2 | 0.38 | 0.37 | 0.10 | |||
| 3 | 0.69 | 0.55 | 0.10 | |||
| 4 | 0.81 | 0.79 | 0.10 | |||
| 5 | 0.57 | 0.91 | 0.10 | |||
| 6 | 0.66 | 0.77 | 0.10 | |||
| Cumulative body weight gain (kg) | 37.99 | 42.88 | 1.92 | 0.08 | ||
| 1 | 0.01 | 0.00 | 0.11 | 0.77 | <0.01 | 0.97 |
| 2 | 0.07 | 0.02 | 0.11 | |||
| 3 | 0.27 | 0.19 | 0.11 | |||
| 4 | 0.40 | 0.42 | 0.11 | |||
| 5 | 0.50 | 0.58 | 0.11 | |||
| 6 | 0.99 | 1.06 | 0.11 | |||
| Cumulative starter DMI (kg) | 15.01 | 15.87 | 2.16 | 0.77 | ||
| Cumulative starter NDF intake (kg) | 5.97 | 6.21 | 0.45 | 0.71 | ||
| Overall FCR3 | 0.69 | 0.61 | 0.09 | 0.52 | ||
FIGURE 1Fecal microbiota at birth in heifer calves born to cows offered a control diet (CON, n = 13) or CON supplemented with ethyl-cellulose rumen-protected methionine (MET, n = 13; Mepron® at 0.09% of diet DM; Evonik Nutrition & Care GmbH, Germany) during the last 28 days of pregnancy. (A) Non-metric multidimensional scaling (NMDS) plot of fecal microbiota profile. (B) Alpha diversity indices. (C) Cladogram of LEfSe analysis shows the overrepresented microbial populations. Taxa are significant from LeFSe (P ≤ 0.05 and LDA cutoff > 3.0). (D) Histogram of the LDA scores reveals the most differentially regulated metabolic pathways in fecal microbiota at KEGG levels 3.
Relative abundance (%) of the overrepresented bacteria highlighted by LeFSe analysis (P ≤ 0.05 and LDA cutoff > 2.0) in feces at birth in heifer calves born to cows offered a control diet (CON, n = 13) supplemented with ethyl-cellulose rumen-protected methionine (MET, n = 13; Mepron® at 0.09% of diet DM; Evonik Nutrition & Care GmbH, Germany) compared with heifer calves born to cows offered a control diet (CON, n = 13) during the last 28 days of pregnancy.
| 1.244a | 0.177b | |
| 1.256a | 0.197b | |
| 0.000b | 0.018a | |
| 0.047b | 0.891a | |
| 0.000b | 0.217a | |
| 0.022a | 0.001b | |
| 0.041a | 0.006b | |
| 0.015a | 0.000b | |
| 2.287b | 3.837a | |
| 0.139a | 0.004b | |
| 0.066a | 0.000b | |
| 0.127a | 0.005b | |
| 2.087b | 3.593a | |
| 0.000b | 0.207a | |
| 0.000b | 0.130a | |
| 0.000b | 0.145a |
FIGURE 2Fecal microbiota during preweaning period in heifer calves born to cows offered a control diet (CON, n = 13) or CON supplemented with ethyl-cellulose rumen-protected methionine (MET, n = 13; Mepron® at 0.09% of diet DM; Evonik Nutrition & Care GmbH, Germany) during the last 28 days of pregnancy. (A) Non-metric multidimensional scaling (NMDS) plot of fecal microbiota profile. (B) Alpha diversity indices. (C) Cladogram of LEfSe analysis shows the overrepresented microbial populations. Taxa are significant from LeFSe (P ≤ 0.05 and LDA cutoff > 3.0). (D) Microbial functional predictions at KEGG levels 3.
Relative abundance (%) of the overrepresented bacteria highlighted by LeFSe analysis (P ≤ 0.05 and LDA cutoff > 2.0) in feces during preweaning period in heifer calves born to cows offered a control diet (CON, n = 13) supplemented with ethyl-cellulose rumen-protected methionine (MET, n = 13; Mepron® at 0.09% of diet DM; Evonik Nutrition & Care GmbH, Germany) compared with heifer calves born to cows offered a control diet (CON, n = 13) during the last 28 days of pregnancy.
| 3.992a | 2.749b | |
| 0.005a | 0.000b | |
| 0.049a | 0.030b | |
| 1.072b | 3.031a | |
| 0.000b | 0.005a | |
| 19.822b | 25.958a | |
| 0.021b | 0.063a | |
| 0.058b | 0.068a | |
| 0.044a | 0.035b |
FIGURE 3Fecal metabolome data at birth in heifer calves born to cows offered a control diet (CON, n = 13) or CON supplemented with ethyl-cellulose rumen-protected methionine (MET, n = 13; Mepron at 0.09% of diet DM; Evonik Nutrition & Care GmbH, Germany) during the last 28 days of pregnancy. (A) 3D scores plot of partial least square discriminant analysis (PLS-DA) model. (B,C) Upregulated and downregulated metabolic pathways in MET group at birth.
FIGURE 4Fecal metabolites most strongly influencing discrimination by partial least square discriminant analysis (PLS-DA) model at birth in heifer calves born to cows offered a control diet supplemented with ethyl-cellulose rumen-protected methionine (MET; Mepron at 0.09% of diet DM; Evonik Nutrition & Care GmbH, Germany) during the last 28 days of pregnancy. (A,B) Upregulated and downregulated fecal metabolites in MET group at birth.
Chemical taxonomy of metabolites most strongly influencing discrimination by the partial least squares discriminate analysis (PLS-DA) that were upregulated and downregulated in feces at birth in heifer calves born to cows offered a control diet (CON, n = 13) supplemented with ethyl-cellulose rumen-protected methionine (MET, n = 13; Mepron® at 0.09% of diet DM; Evonik Nutrition & Care GmbH, Germany) compared with heifer calves born to cows offered a control diet (CON, n = 13) during the last 28 days of pregnancy, following the conditions of VIP > 1.0 and |p-(corr)| ≥ 0.5.
| Increased in MET | 3,4-Dihydroxyphenylglycol | Benzenoids | Benzenediols |
| 2,5-Dichlorophenol | Benzenoids | Halobenzenes | |
| Phosphatidylcholine | Lipids and lipid-like molecules | Glycerophosphocholines | |
| Glycerol 3-phosphate | Lipids and lipid-like molecules | Glycerophosphates | |
| Prostaglandin E2 | Lipids and lipid-like molecules | Eicosanoids | |
| Epiandrosterone | Lipids and lipid-like molecules | Androstane steroids | |
| Sphinganine 1-phosphate | Lipids and lipid-like molecules | Phosphosphingolipids | |
| Flavin mononucleotide | Nucleosides, nucleotides, and analogues | Flavin nucleotides | |
| Cytidylic acid | Nucleosides, nucleotides, and analogues | Pyrimidine ribonucleotides | |
| Sphingoid | Organic nitrogen compounds | Amines | |
| Glucuronide | Organic oxygen compounds | Carbohydrates and carbohydrate conjugates | |
| Organic oxygen compounds | Carbohydrates and carbohydrate conjugates | ||
| Epimelibiose | Organic oxygen compounds | Carbohydrates and carbohydrate conjugates | |
| Riboflavin | Organoheterocyclic compounds | Alloxazines and isoalloxazines | |
| Ascorbic acid | Organoheterocyclic compounds | Furanones | |
| Decreased in MET | Pyrogallic acid | Benzenoids | Phenols and derivatives |
| Phenylglyoxylic acid | Benzenoids | Benzoyl derivatives | |
| Squalene | Lipids and lipid-like molecules | Triterpenoids | |
| Linoleic acid | Lipids and lipid-like molecules | Lineolic acids and derivatives | |
| Desoxycortone | Lipids and lipid-like molecules | Hydroxysteroids | |
| 9,10-DHOME | Lipids and lipid-like molecules | Fatty acids and conjugates | |
| Ceramide | Lipids and lipid-like molecules | Ceramides | |
| Estradiol-17beta 3-glucuronide | Lipids and lipid-like molecules | Steroidal glycosides | |
| Gamolenic acid | Lipids and lipid-like molecules | Lineolic acids and derivatives | |
| 13-OxoODE | Lipids and lipid-like molecules | Lineolic acids and derivatives | |
| Uridine | Nucleosides, nucleotides, and analogues | Pyrimidine nucleosides | |
| Guanosine triphosphate | Nucleosides, nucleotides, and analogs | Purine ribonucleotides | |
| Cyclic AMP | Nucleosides, nucleotides, and analogues | Cyclic purine nucleotides | |
| Cysteinylglycine | Organic acids and derivatives | Amino acids, peptides, and analogues | |
| Naringenin | Phenylpropanoids and polyketides | Flavans | |
FIGURE 5Fecal metabolome data during preweaning period in heifer calves born to cows offered a control diet (CON, n = 13) or CON supplemented with ethyl-cellulose rumen-protected methionine (MET, n = 13; Mepron at 0.09% of diet DM; Evonik Nutrition & Care GmbH, Germany) during the last 28 days of pregnancy. (A) 3D scores plot of partial least square discriminant analysis (PLS-DA) model. (B,C) Upregulated and downregulated metabolic pathways in MET group during preweaning period.
FIGURE 6Fecal metabolites most strongly influencing discrimination by partial least square discriminant analysis (PLS-DA) model during preweaning period in heifer calves born to cows offered a control diet supplemented with ethyl-cellulose rumen-protected methionine (MET; Mepron at 0.09% of diet DM; Evonik Nutrition & Care GmbH, Germany) during the last 28 days of pregnancy. (A,B) Upregulated and downregulated fecal metabolites in MET group during preweaning period.
Chemical taxonomy of metabolites most strongly influencing discrimination by the partial least squares discriminate analysis (PLS-DA) that were upregulated and downregulated in feces during preweaning period in heifer calves born to cows offered a control diet (CON, n = 13) supplemented with ethyl-cellulose rumen-protected methionine (MET, n = 13; Mepron® at 0.09% of diet DM; Evonik Nutrition & Care GmbH, Germany) compared with heifer calves born to cows offered a control diet (CON, n = 13) during the last 28 days of pregnancy, following the conditions of VIP > 1.0 and |p-(corr)| ≥ 0.5.
| Increased in MET | 9- | Lipids and lipid-like molecules | Retinoids |
| 13-OxoODE | Lipids and lipid-like molecules | Lineolic acids and derivatives | |
| Isofucosterol | Lipids and lipid-like molecules | Stigmastanes and derivatives | |
| Xanthosine | Nucleosides, nucleotides, and analogues | Purine nucleosides | |
| Thiomethyladenosine | Nucleosides, nucleotides, and analogs | 5′-deoxy-5′-thionucleosides | |
| Organic acids and derivatives | Amino acids, peptides, and analogs | ||
| Organic acids and derivatives | Amino acids, peptides, and analogs | ||
| Fumaric acid | Organic acids and derivatives | Dicarboxylic acids and derivatives | |
| cis-Aconitic acid | Organic acids and derivatives | Tricarboxylic acids and derivatives | |
| Ascorbic acid | Organoheterocyclic compounds | Furanones | |
| (R)-Lipoate | Organoheterocyclic compounds | Lipoic acids and derivatives | |
| Biotin | Organoheterocyclic compounds | Biotin and derivatives | |
| Neopterin | Organoheterocyclic compounds | Pterins and derivatives | |
| Indoleacetaldehyde | Organoheterocyclic compounds | Indoles | |
| Hydroxyphenyllactic acid | Phenylpropanoids and polyketides | Phenylpropanoic acids | |
| Decreased in MET | 9,10-DHOME | Lipids and lipid-like molecules | Fatty acids and conjugates |
| Phthalic acid | Benzenoids | Benzoic acids and derivatives | |
| Estradiol-17beta 3-glucuronide | Lipids and lipid-like molecules | Steroidal glycosides | |
| 2-Lysolecithin | Lipids and lipid-like molecules | Glycerophosphocholines | |
| Diglyceride | Lipids and lipid-like molecules | Lineolic acids and derivatives | |
| Eicosenoic acid | Lipids and lipid-like molecules | Fatty acids and conjugates | |
| Alpha-Tocotrienol | Lipids and lipid-like molecules | Quinone and hydroquinone lipids | |
| Gamma-Aminobutyric acid (GABA) | Organic acids and derivatives | Amino acids, peptides, and analogs | |
| Organic acids and derivatives | Amino acids, peptides, and analogs | ||
| 3-Hydroxy- | Organic oxygen compounds | Carbonyl compounds | |
| Inositol phosphate | Organic oxygen compounds | Alcohols and polyols | |
| Galactose 1-phosphate | Organic oxygen compounds | Carbohydrates and carbohydrate conjugates | |
| Formyl- | Organic oxygen compounds | Carbonyl compounds | |
| Riboflavin | Organoheterocyclic compounds | Alloxazines and isoalloxazines | |
| Thiamine pyrophosphate | Organoheterocyclic compounds | Pyrimidines and pyrimidine derivatives | |