Regulatory Effects of Maternal Intake of Microbial-Derived Antioxidants on Colonization of Microbiota in Breastmilk and That of Intestinal Microbiota in Offspring
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Microbial-Derived Antioxidant (MA)
2.2. Animal Experiment and Sample Collection
2.3. DNA Isolation and Sequencing
2.4. Data Processing
2.5. Sequence Analysis
2.6. Statistical Analysis
3. Results
3.1. The Production Performance of Female Rats
3.2. Sampling Timepoint and Sample Type Affect Microbiota Profile
3.3. Effect of Maternal MA Additive on the Colonization of Microbiota in Breastmilk and Maternal Ileum
3.4. Effect of Maternal MA Intake on Offspring Intestinal Microbiota
3.5. Compositional Differences between Treatments and over Time
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Appendix A
References
- Li, L.; Wang, H.; Dong, S.; Ma, Y. Supplementation with alpha-glycerol monolaurate during late gestation and lactation enhances sow performance, ameliorates milk composition, and improves growth of suckling piglets. J. Anim. Sci. Biotechnol. 2023, 14, 47. [Google Scholar] [CrossRef]
- Zhang, J.; Wang, J.; Ma, Z.; Fu, Z.; Zhao, Y.; Zeng, X.; Lin, G.; Zhang, S.; Guan, W.; Chen, F. Enhanced Antioxidative Capacity Transfer between Sow and Fetus via the Gut–Placenta Axis with Dietary Selenium Yeast and Glycerol Monolaurate Supplementation during Pregnancy. Antioxidants 2024, 13, 141. [Google Scholar] [CrossRef]
- Marseglia, L.; D’Angelo, G.; Manti, S.; Arrigo, T.; Barberi, I.; Reiter, R.J.; Gitto, E. Oxidative stress-mediated aging during the fetal and perinatal periods. Oxid. Med. Cell Longev. 2014, 2014, 358375. [Google Scholar] [CrossRef] [PubMed]
- Ipema, A.F.; Bokkers, E.A.; Gerrits, W.J.; Kemp, B.; Bolhuis, J.E. Providing live black soldier fly larvae (Hermetia illucens) improves welfare while maintaining performance of piglets post-weaning. Sci. Rep. 2021, 11, 7371. [Google Scholar] [CrossRef]
- Ma, L.; Zhou, B.; Liu, H.; Chen, S.; Zhang, J.; Wang, T.; Wang, C. Dietary rutin improves the antidiarrheal capacity of weaned piglets by improving intestinal barrier function, antioxidant capacity and cecal microbiota composition. J. Sci. Food Agric. 2024, 104, 6262–6275. [Google Scholar] [CrossRef]
- Wang, L.; Jiang, L.; Chu, Y.; Feng, F.; Tang, W.; Chen, C.; Qiu, Y.; Hu, Z.; Diao, H.; Tang, Z. Dietary Taurine Improves Growth Performance and Intestine Health via the GSH/GSSG Antioxidant System and Nrf2/ARE Signaling Pathway in Weaned Piglets. Antioxidants 2023, 12, 1852. [Google Scholar] [CrossRef]
- Zhu, L.H.; Zhao, K.L.; Chen, X.L.; Xu, J.X. Impact of weaning and an antioxidant blend on intestinal barrier function and antioxidant status in pigs1. J. Anim. Sci. 2012, 90, 2581–2589. [Google Scholar] [CrossRef]
- Bayr, H. Reactive oxygen species. Crit. Care Med. 2005, 33, S498–S501. [Google Scholar] [CrossRef] [PubMed]
- Tan, J.; McKenzie, C.; Potamitis, M.; Thorburn, A.N.; Mackay, C.R.; Macia, L. The role of short-chain fatty acids in health and disease. Adv. Immunol. 2014, 121, 91–119. [Google Scholar]
- Liou, G.; Storz, P. Reactive oxygen species in cancer. Free Radic. Res. 2010, 44, 479–496. [Google Scholar] [CrossRef]
- Thannickal, V.J.; Fanburg, B.L. Reactive oxygen species in cell signaling. Am. J. Physiol.-Lung Cell. Mol. Physiol. 2000, 279, L1005–L1028. [Google Scholar] [CrossRef] [PubMed]
- Turrens, J.F. Mitochondrial formation of reactive oxygen species. J. Physiol. 2003, 552 Pt 2, 335–344. [Google Scholar] [CrossRef] [PubMed]
- Dröge, W. Free radicals in the physiological control of cell function. Physiol. Rev. 2002, 82, 47–95. [Google Scholar] [CrossRef] [PubMed]
- Jiang, Z.; Lu, W.; Zeng, Q.; Li, D.; Ding, L.; Wu, J. High glucose-induced excessive reactive oxygen species promote apoptosis through mitochondrial damage in rat cartilage endplate cells. J. Orthop. Res. 2018, 36, 2476–2483. [Google Scholar] [CrossRef] [PubMed]
- Seifried, H.E.; Anderson, D.E.; Fisher, E.I.; Milner, J.A. A review of the interaction among dietary antioxidants and reactive oxygen species. J. Nutr. Biochem. 2007, 18, 567–579. [Google Scholar] [CrossRef] [PubMed]
- Luo, Z.; Xu, X.; Zhao, S.; Sho, T.; Luo, W.; Zhang, J.; Xu, W.; Hon, K.; Xu, J. Inclusion of microbe-derived antioxidant during pregnancy and lactation attenuates high-fat diet-induced hepatic oxidative stress, lipid disorders, and NLRP3 inflammasome in mother rats and offspring. Food Nutr. Res. 2019, 63. [Google Scholar] [CrossRef] [PubMed]
- Gao, Q.; Luo, Z.; Ma, S.; Yu, C.; Shen, C.; Xu, W.; Zhang, J.; Zhang, H.; Xu, J. Microbe-Derived Antioxidants Alleviate Liver and Adipose Tissue Lipid Disorders and Metabolic Inflammation Induced by High Fat Diet in Mice. Int. J. Mol. Sci. 2023, 24, 3269. [Google Scholar] [CrossRef]
- Sommer, F.; Bäckhed, F. The gut microbiota--masters of host development and physiology. Nat. Rev. Microbiol. 2013, 11, 227–238. [Google Scholar] [CrossRef]
- Wu, H.J.; Wu, E. The role of gut microbiota in immune homeostasis and autoimmunity. Gut Microbes 2012, 3, 4–14. [Google Scholar] [CrossRef]
- Carding, S.; Verbeke, K.; Vipond, D.T.; Corfe, B.M.; Owen, L.J. Dysbiosis of the gut microbiota in disease. Microb. Ecol. Health Dis. 2015, 26, 26191. [Google Scholar] [CrossRef]
- Gérard, P. Gut microbiota and obesity. Cell Mol. Life Sci. 2016, 73, 147–162. [Google Scholar] [CrossRef]
- Li, J.; Zhao, F.; Wang, Y.; Chen, J.; Tao, J.; Tian, G.; Wu, S.; Liu, W.; Cui, Q.; Geng, B.; et al. Gut microbiota dysbiosis contributes to the development of hypertension. Microbiome 2017, 5, 14. [Google Scholar] [CrossRef]
- An, R.; Wilms, E.; Masclee, A.A.; Smidt, H.; Zoetendal, E.G.; Jonkers, D. Age-dependent changes in GI physiology and microbiota: Time to reconsider? Gut 2018, 67, 2213–2222. [Google Scholar] [CrossRef]
- Duale, A.; Singh, P.; Al, K.S. Breast Milk: A Meal Worth Having. Front. Nutr. 2021, 8, 800927. [Google Scholar] [CrossRef]
- Matos, C.; Ribeiro, M.; Guerra, A. Breastfeeding: Antioxidative properties of breast milk. J. Appl. Biomed. 2015, 13, 169–180. [Google Scholar] [CrossRef]
- Wang, C.; Wei, S.; Liu, B.; Wang, F.; Lu, Z.; Jin, M.; Wang, Y. Maternal consumption of a fermented diet protects offspring against intestinal inflammation by regulating the gut microbiota. Gut Microbes 2022, 14, 2057779. [Google Scholar] [CrossRef]
- Cortes-Macías, E.; Selma-Royo, M.; García-Mantrana, I.; Calatayud, M.; González, S.; Martínez-Costa, C.; Collado, M.C. Maternal Diet Shapes the Breast Milk Microbiota Composition and Diversity: Impact of Mode of Delivery and Antibiotic Exposure. J. Nutr. 2021, 151, 330–340. [Google Scholar] [CrossRef]
- Deledda, A.; Annunziata, G.; Tenore, G.C.; Palmas, V.; Manzin, A.; Velluzzi, F. Diet-Derived Antioxidants and Their Role in Inflammation, Obesity and Gut Microbiota Modulation. Antioxidants 2021, 10, 708. [Google Scholar] [CrossRef]
- Cai, X.; Chen, X.L.; Yang, F.; Xu, J.X.; Gu, J.; Zhang, C. A Preliminary Research of Antioxidant Capacity by Micro-Derived Antioxidants In Vitro. Biotechnology 2011, 21, 84–87. [Google Scholar]
- Luo, Z.; Gao, Q.; Zhang, H.; Zhang, Y.; Zhou, S.; Zhang, J.; Xu, W.; Xu, J. Microbe-derived antioxidants attenuate cobalt chloride-induced mitochondrial function, autophagy and BNIP3-dependent mitophagy pathways in BRL3A cells. Ecotoxicol. Environ. Saf. 2022, 232, 113219. [Google Scholar] [CrossRef]
- Yu, C.; Wang, D.; Shen, C.; Luo, Z.; Zhang, H.; Zhang, J.; Xu, W.; Xu, J. Microbe-derived Antioxidants Enhance Lipid Synthesis by Regulating the Hepatic AMPKα-SREBP1c Pathway in Weanling Piglets. J. Nutr. 2024, 154, 1101–1108. [Google Scholar] [CrossRef] [PubMed]
- Shen, C.; Luo, Z.; Ma, S.; Yu, C.; Lai, T.; Tang, S.; Zhang, H.; Zhang, J.; Xu, W.; Xu, J. Microbe-Derived Antioxidants Protect IPEC-1 Cells from H2O2-Induced Oxidative Stress, Inflammation and Tight Junction Protein Disruption via Activating the Nrf2 Pathway to Inhibit the ROS/NLRP3/IL-1β Signaling Pathway. Antioxidants 2024, 13, 533. [Google Scholar] [CrossRef] [PubMed]
- Azara, C.R.; Maia, I.C.; Rangel, C.N.; Silva-Neto, M.A.; Serpa, R.F.; De Jesus, E.F.; Do Carmo, M.G.T.; Fialho, E. Ethanol intake during lactation alters milk nutrient composition and growth and mineral status of rat pups. Biol. Res. 2008, 41, 317–330. [Google Scholar] [CrossRef] [PubMed]
- Parada, A.E.; Needham, D.M.; Fuhrman, J.A. Every base matters: Assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ. Microbiol. 2016, 18, 1403–1414. [Google Scholar] [CrossRef] [PubMed]
- Bolyen, E.; Rideout, J.R.; Dillon, M.R.; Bokulich, N.A.; Abnet, C.C.; Al-Ghalith, G.A.; Alexander, H.; Alm, E.J.; Arumugam, M.; Asnicar, F.; et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 2019, 37, 852–857. [Google Scholar] [CrossRef] [PubMed]
- DeSantis, T.Z.; Hugenholtz, P.; Larsen, N.; Rojas, M.; Brodie, E.L.; Keller, K.; Huber, T.; Dalevi, D.; Hu, P.; Andersen, G.L. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 2006, 72, 5069–5072. [Google Scholar] [CrossRef]
- Dixon, P.M. VEGAN, a package of R functions for community ecology. J. Veg. Sci. 2003, 14, 927–930. [Google Scholar] [CrossRef]
- Lyons, K.E.; Shea CA, O.; Grimaud, G.; Ryan, C.A.; Dempsey, E.; Kelly, A.L.; Ross, R.P.; Stanton, C. The human milk microbiome aligns with lactation stage and not birth mode. Sci. Rep. 2022, 12, 5598. [Google Scholar] [CrossRef] [PubMed]
- Padilha, M.; Danneskiold-Samsøe, N.B.; Brejnrod, A.; Hoffmann, C.; Cabral, V.P.; Iaucci, J.D.M.; Sales, C.H.; Fisberg, R.M.; Cortez, R.V.; Brix, S.; et al. The Human Milk Microbiota is Modulated by Maternal Diet. Microorganisms 2019, 7, 502. [Google Scholar] [CrossRef]
- Chen, W.; Mi, J.; Lv, N.; Gao, J.; Cheng, J.; Wu, R.; Ma, J.; Lan, T.; Liao, X. Lactation Stage-Dependency of the Sow Milk Microbiota. Front. Microbiol. 2018, 9, 945. [Google Scholar] [CrossRef]
- Taylor, R.; Keane, D.; Borrego, P.; Arcaro, K. Effect of Maternal Diet on Maternal Milk and Breastfed Infant Gut Microbiomes: A Scoping Review. Nutrients 2023, 15, 1420. [Google Scholar] [CrossRef]
- Rovira, J.; Martínez, M.Á.; Mari, M.; Cunha, S.C.; Fernandes, J.O.; Marmelo, I.; Marques, A.; Haug, L.S.; Thomsen, C.; Nadal, M.; et al. Mixture of environmental pollutants in breast milk from a Spanish cohort of nursing mothers. Environ. Int. 2022, 166, 107375. [Google Scholar] [CrossRef] [PubMed]
- Aprea, G.; Del Matto, I.; Tucci, P.; Marino, L.; Scattolini, S.; Rossi, F. In Vivo Functional Properties of Dairy Bacteria. Microorganisms 2023, 11, 1787. [Google Scholar] [CrossRef] [PubMed]
- Čoklo, M.; Maslov, D.R.; Kraljević, P.S. Modulation of gut microbiota in healthy rats after exposure to nutritional supplements. Gut Microbes 2020, 12, 1779002. [Google Scholar] [CrossRef] [PubMed]
- Sindi, A.S.; Geddes, D.T.; Wlodek, M.E.; Muhlhausler, B.S.; Payne, M.S.; Stinson, L.F. Can we modulate the breastfed infant gut microbiota through maternal diet? FEMS Microbiol. Rev. 2021, 45, fuab011. [Google Scholar] [CrossRef] [PubMed]
- Lundgren, S.N.; Madan, J.C.; Emond, J.A.; Morrison, H.G.; Christensen, B.C.; Karagas, M.R.; Hoen, A.G. Maternal diet during pregnancy is related with the infant stool microbiome in a delivery mode-dependent manner. Microbiome 2018, 6, 109. [Google Scholar] [CrossRef]
Main Ingredient | Energy | Protein | Fats | Other |
corn, wheat | fish meal, chicken meal, yeast powder, soybean meal, alfalfa meal | vegetable oil, soybean oil | amino acids, vitamins, minerals | |
Nutritive Index | Crude Protein | Crude Fat | Carbohydrate | |
21.72% | 4.57% | 52.96% |
Group | Average Weight/g | Average Feed Intake During Pregnancy/g | Average Feed Intake in Lactation/g | Litter Size | Primary Litter Weight/g |
---|---|---|---|---|---|
Control | 311.24 ± 33.32 | 22.09 ± 1.83 | 308.90 ± 39.48 | 13.75 ± 2.45 | 88.89 ± 14.25 |
MA | 289.12 ± 18.04 *** | 17.46 ± 1.55 ** | 260.05 ± 31.47 * | 13,25 ± 2.99 | 85.40 ± 18.92 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Wu, D.; An, R.; Wang, D.; Jiang, L.; Huang, L.; Lu, T.; Xu, W.; Xu, J.; Zhang, J. Regulatory Effects of Maternal Intake of Microbial-Derived Antioxidants on Colonization of Microbiota in Breastmilk and That of Intestinal Microbiota in Offspring. Animals 2024, 14, 2582. https://doi.org/10.3390/ani14172582
Wu D, An R, Wang D, Jiang L, Huang L, Lu T, Xu W, Xu J, Zhang J. Regulatory Effects of Maternal Intake of Microbial-Derived Antioxidants on Colonization of Microbiota in Breastmilk and That of Intestinal Microbiota in Offspring. Animals. 2024; 14(17):2582. https://doi.org/10.3390/ani14172582
Chicago/Turabian StyleWu, Dangjin, Ran An, Di Wang, Luoxin Jiang, Liu Huang, Tenghui Lu, Weina Xu, Jianxiong Xu, and Jing Zhang. 2024. "Regulatory Effects of Maternal Intake of Microbial-Derived Antioxidants on Colonization of Microbiota in Breastmilk and That of Intestinal Microbiota in Offspring" Animals 14, no. 17: 2582. https://doi.org/10.3390/ani14172582