Maternal Malic Acid May Ameliorate Oxidative Stress and Inflammation in Sows through Modulating Gut Microbiota and Host Metabolic Profiles during Late Pregnancy.
L-malic acid; gut microbiota; late pregnancy; metabolic; sow; Cell Biology; Clinical Biochemistry; Molecular Biology; Biochemistry; Physiology
Abstract :
[en] Sows suffer oxidative stress and inflammation induced by metabolic burden during late pregnancy, which negatively regulates reproductive and lactating performances. We previously found that L-malic acid (MA) alleviated oxidative stress and inflammation and improved reproductive performances in sows. However, the mechanism underlying the MA's positive effects remains unexplored. Here, twenty Large White × Landrace sows with similar parity were randomly divided into two groups and fed with a basal diet or a diet supplemented with 2% L-malic acid complex from day 85 of gestation to delivery. The gut microbiome, fecal short-chain fatty acids, and untargeted serum metabolome were determined. Results showed that Firmicutes, Bacteroidota, and Spirochaetota were the top abundant phyla identified in late pregnancy for sows. Maternal MA supplementation modulated the composition but not the richness and diversity of gut microbiota during late pregnancy. Correlation analysis between gut microbiota and antioxidant capacity (or inflammation indicators) revealed that unclassified_f_Ruminococcaceae, unclassified_f_Lachnospiraceae, UCG-002, norank_f_norank_o_RF3, and Lactobacillus might play a role in anti-oxidation, and Lachnospiraceae_XPB1014_group, Lachnospiraceae_NK4A136_group, UCG-002, unclassified_f_Ruminococcaceae, Candidatus_Soleaferrea, norank_f_UCG-010, norank_f_norank_o_RF39, and unclassified_f_Lachnospiraceae might be involved in the anti-inflammatory effect. The improved antioxidant and inflammation status induced by MA might be independent of short chain fatty acid changes. In addition, untargeted metabolomics analysis exhibited different metabolic landscapes of sows in the MA group from in the control group and revealed the contribution of modified amino acid and lipid metabolism to the improved antioxidant capacity and inflammation status. Notably, correlation results of gut microbiota and serum metabolites, as well as serum metabolites and antioxidant capacity (or inflammation indicators), demonstrated that differential metabolism was highly related to the fecal microorganisms and antioxidant or inflammation indicators. Collectively, these data demonstrated that a maternal dietary supply of MA can ameliorate oxidative stress and inflammation in sows through modulating gut microbiota and host metabolic profiles during late pregnancy.
Disciplines :
Agriculture & agronomy
Author, co-author :
Chen, Meixia ✱; Institute of Animal Husbandry and Veterinary Medicine, Beijing Academy of Agriculture and Forestry Sciences, Beijing 100097, China
Zhao, Ying ✱; Université de Liège - ULiège > TERRA Research Centre
Li, Shuang; College of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, China
Chang, Zhuo; Beijing General Station of Animal Husbandry, Beijing 100107, China
Liu, Hui; Institute of Animal Husbandry and Veterinary Medicine, Beijing Academy of Agriculture and Forestry Sciences, Beijing 100097, China
Zhang, Dongyan; Institute of Animal Husbandry and Veterinary Medicine, Beijing Academy of Agriculture and Forestry Sciences, Beijing 100097, China
Wang, Sixin; Institute of Animal Husbandry and Veterinary Medicine, Beijing Academy of Agriculture and Forestry Sciences, Beijing 100097, China
Zhang, Xin ; State Key Laboratory of Animal Nutrition and Feeding, College of Animal Science and Technology, China Agricultural University, Beijing 100193, China
Wang, Jing; Institute of Animal Husbandry and Veterinary Medicine, Beijing Academy of Agriculture and Forestry Sciences, Beijing 100097, China
✱ These authors have contributed equally to this work.
Language :
English
Title :
Maternal Malic Acid May Ameliorate Oxidative Stress and Inflammation in Sows through Modulating Gut Microbiota and Host Metabolic Profiles during Late Pregnancy.
Berchieri-Ronchi C.B. Kim S.W. Zhao Y. Correa C.R. Yeum K.J. Ferreira A.L.A. Oxidative stress status of highly prolific sows during gestation and lactation Animal 2011 5 1774 1779 10.1017/S1751731111000772
Zhang Q. Li J. Cao M. Li Y. Zhuo Y. Fang Z. Che L. Xu S. Feng B. Lin Y. Dietary supplementation of Bacillus subtilis PB6 improves sow reproductive performance and reduces piglet birth intervals Anim. Nutr. 2020 6 278 287 10.1016/j.aninu.2020.04.002 33005761
Oliviero C. Heinonen M. Valros A. Peltoniemi O. Environmental and sow-related factors affecting the duration of farrowing Anim. Reprod. Sci. 2010 119 85 91 10.1016/j.anireprosci.2009.12.009 20053511
Ruediger K. Schulze M. Post-farrowing stress management in sows by administration of azaperone: Effects on piglets performance J. Anim. Sci. 2012 90 2331 2336 10.2527/jas.2011-4661 22287670
Black J. Mullan B. Lorschy M. Giles L. Lactation in the sow during heat stress Livest. Prod. Sci. 1993 35 153 170 10.1016/0301-6226(93)90188-N
Silanikove N. Shapiro F. Shinder D. Acute heat stress brings down milk secretion in dairy cows by up-regulating the activity of the milk-borne negative feedback regulatory system BMC Physiol. 2009 9 13 10.1186/1472-6793-9-13 19563620
Romero-Haro A.A. Alonso-Alvarez C. Oxidative stress experienced during early development influences the offspring phenotype Am. Nat. 2020 196 704 716 10.1086/711399 33211561
Shao Y. Zhou J. Xiong X. Zou L. Kong X. Tan B. Yin Y. Differences in Gut Microbial and Serum Biochemical Indices Between Sows with Different Productive Capacities During Perinatal Period Front. Microbiol. 2019 10 3047 10.3389/fmicb.2019.03047
Hayakawa T. Masuda T. Kurosawa D. Tsukahara T. Dietary administration of probiotics to sows and/or their neonates improves the reproductive performance, incidence of post-weaning diarrhea and histopathological parameters in the intestine of weaned piglets Anim. Sci. J. 2016 87 1501 1510 10.1111/asj.12565
Koren O. Goodrich J.K. Cullender T.C. Spor A. Laitinen K. Bäckhed H.K. Gonzalez A. Werner J.J. Angenent L.T. Knight R. Host remodeling of the gut microbiome and metabolic changes during pregnancy Cell 2012 150 470 480 10.1016/j.cell.2012.07.008
Cheng C. Wei H. Yu H. Xu C. Jiang S. Peng J. Metabolic syndrome during perinatal period in sows and the link with gut microbiota and metabolites Front. Microbiol. 2018 9 1989 10.3389/fmicb.2018.01989 30197635
Wang H. Ji Y. Yin C. Deng M. Tang T. Deng B. Ren W. Deng J. Yin Y. Tan C. Differential analysis of gut microbiota correlated with oxidative stress in sows with high or low litter performance during lactation Front. Microbiol. 2018 9 1665 10.3389/fmicb.2018.01665
Wang H. Hu C. Cheng C. Cui J. Ji Y. Hao X. Li Q. Ren W. Deng B. Yin Y. Unraveling the association of fecal microbiota and oxidative stress with stillbirth rate of sows Theriogenology 2019 136 131 137 10.1016/j.theriogenology.2019.06.028 31255919
Tan C. Wei H. Ao J. Long G. Peng J. Inclusion of konjac flour in the gestation diet changes the gut microbiota, alleviates oxidative stress, and improves insulin sensitivity in sows Appl. Environ. Microbiol. 2016 82 5899 5909 10.1128/AEM.01374-16 27474722
Macpherson A.J. de Agüero M.G. Ganal-Vonarburg S.C. How nutrition and the maternal microbiota shape the neonatal immune system Nat. Rev. Immunol. 2017 17 508 517 10.1038/nri.2017.58
Li Q. Yang S. Chen F. Guan W. Zhang S. Nutritional strategies to alleviate oxidative stress in sows Anim. Nutr. 2022 9 60 73 10.1016/j.aninu.2021.10.006
Reyes-Camacho D. Vinyeta E. Pérez J.F. Aumiller T. Criado L. Palade L.M. Taranu I. Folch J.M. Calvo M.A. Van der Klis J.D. Phytogenic actives supplemented in hyperprolific sows: Effects on maternal transfer of phytogenic compounds, colostrum and milk features, performance and antioxidant status of sows and their offspring, and piglet intestinal gene expression J. Anim. Sci. 2020 98 skz390 10.1093/jas/skz390
Wu N. Zhang J. Chen Y. Xu Q. Song P. Li Y. Li K. Liu H. Recent advances in microbial production of L-malic acid Appl. Microbiol. Biotechnol. 2022 106 7973 7992 10.1007/s00253-022-12260-y
Yousefi M. Ghafarifarsani H. Raissy M. Yilmaz S. Vatnikov Y.A. Kulikov E.V. Effects of dietary malic acid supplementation on growth performance, antioxidant and immunological parameters, and intestinal gene expressions in rainbow trout, Oncorhynchus mykiss Aquaculture 2023 563 738864 10.1016/j.aquaculture.2022.738864
Zhang L. Zhang P. Xia C. Cheng Y. Guo X. Li Y. Effects of malic acid and citric acid on growth performance, antioxidant capacity, haematology and immune response of Carassius auratus gibelio Aquacult. Res. 2020 51 2766 2776 10.1111/are.14616
Zhang X. Chen M. Yan E. Wang Y. Ma C. Zhang P. Yin J. Dietary malic acid supplementation induces skeletal muscle fiber-type transition of weaned piglets and further improves meat quality of finishing pigs Front. Nutr. 2022 8 825495 10.3389/fnut.2021.825495 35145985
Yan E. Wang Y. He L. Guo J. Zhang X. Yin J. Effects of dietary l-malic acid supplementation on meat quality, antioxidant capacity and muscle fiber characteristics of finishing pigs Foods 2022 11 3335 10.3390/foods11213335
Zhang P. Jiang G. Wang Y. Yan E. He L. Guo J. Yin J. Zhang X. Maternal consumption of l-malic acid enriched diets improves antioxidant capacity and glucose metabolism in offspring by regulating the gut microbiota Redox Biol. 2023 67 102889 10.1016/j.redox.2023.102889 37741046
Wang G. Wang X. Ma Y. Cai S. Yang L. Fan Y. Zeng X. Qiao S. Lactobacillus reuteri improves the development and maturation of fecal microbiota in piglets through mother-to-infant microbe and metabolite vertical transmission Microbiome 2022 10 211 10.1186/s40168-022-01336-6
Hedemann M. Flummer C. Kristensen N. Theil P. Metabolic profiling of plasma from sows before parturition and during lactation using a liquid chromatography–mass spectrometry-based approach J. Anim. Sci. 2012 90 200 202 10.2527/jas.53911
Newbern D. Freemark M. Placental hormones and the control of maternal metabolism and fetal growth Curr. Opin. Endocrinol. Diabetes Obes. 2011 18 409 416 10.1097/MED.0b013e32834c800d
Palm M. Axelsson O. Wernroth L. Larsson A. Basu S. Involvement of inflammation in normal pregnancy Acta Obstet. Gynecol. Scand. 2013 92 601 605 10.1111/aogs.12093
Pereira R.D. De Long N.E. Wang R.C. Yazdi F.T. Holloway A.C. Raha S. Angiogenesis in the placenta: The role of reactive oxygen species signaling Biomed. Res. Int. 2015 2015 814543 10.1155/2015/814543
Liu H. Hou C. Li N. Zhang X. Zhang G. Yang F. Zeng X. Liu Z. Qiao S. Microbial and metabolic alterations in gut microbiota of sows during pregnancy and lactation FASEB J. 2019 33 4490 4501 10.1096/fj.201801221RR
Zhou P. Zhao Y. Zhang P. Li Y. Gui T. Wang J. Jin C. Che L. Li J. Lin Y. Microbial mechanistic insight into the role of inulin in improving maternal health in a pregnant sow model Front. Microbiol. 2017 8 2242 10.3389/fmicb.2017.02242
Kim M. Morrison M. Yu Z. Status of the phylogenetic diversity census of ruminal microbiomes FEMS Microbiol. Ecol. 2011 76 49 63 10.1111/j.1574-6941.2010.01029.x
Becker A.A. Hesta M. Hollants J. Janssens G.P. Huys G. Phylogenetic analysis of faecal microbiota from captive cheetahs reveals underrepresentation of Bacteroidetes and Bifidobacteriaceae BMC Microbiol. 2014 14 43 10.1186/1471-2180-14-43
Komaroff A.L. The microbiome and risk for obesity and diabetes JAMA 2017 317 355 356 10.1001/jama.2016.20099
Wang Z. Chen Y. Wang W. Huang C. Hu Y. Johnston L. Wang F. Dietary supplementation with fine-grinding wheat bran improves lipid metabolism and inflammatory response via modulating the gut microbiota structure in pregnant sow Front. Microbiol. 2022 13 835950 10.3389/fmicb.2022.835950
He J. Guo H. Zheng W. Xue Y. Zhao R. Yao W. Heat stress affects fecal microbial and metabolic alterations of primiparous sows during late gestation J. Anim. Sci. Biotechnol. 2019 10 84 10.1186/s40104-019-0391-0
Li Y. Liu H. Zhang L. Yang Y. Lin Y. Zhuo Y. Fang Z. Che L. Feng B. Xu S. Maternal dietary fiber composition during gestation induces changes in offspring antioxidative capacity, inflammatory response, and gut microbiota in a sow model Int. J. Mol. Sci. 2019 21 31 10.3390/ijms21010031 31861629
Zhao Y. Huang Y. Gao K. Wen X. Hu S. Wang L. Jiang Z. Xiao H. Maternal resveratrol regulates the growth performance, antioxidant capacity, and intestinal health of suckling piglets through intestinal microorganisms at high summer temperatures Front. Nutr. 2022 9 971496 10.3389/fnut.2022.971496 36159472
Ramsay T. Arfken A. Summers K. Enteroendocrine peptides, growth, and the microbiome during the porcine weaning transition Anim. Microbiome 2022 4 56 10.1186/s42523-022-00206-8 36401290
Li H. Ma L. Li Z. Yin J. Tan B. Chen J. Jiang Q. Ma X. Evolution of the Gut Microbiota and Its Fermentation Characteristics of Ningxiang Pigs at the Young Stage Animals 2021 11 638 10.3390/ani11030638
Ali Q. Ma S. Farooq U. Niu J. Li F. Li D. Wang Z. Sun H. Cui Y. Shi Y. Pasture intake protects against commercial diet-induced lipopolysaccharide production facilitated by gut microbiota through activating intestinal alkaline phosphatase enzyme in meat geese Front. Immunol. 2022 13 1041070 10.3389/fimmu.2022.1041070
Ayyanna R. Ankaiah D. Arul V. Anti-inflammatory and antioxidant properties of probiotic bacterium Lactobacillus mucosae AN1 and Lactobacillus fermentum SNR1 in Wistar albino rats Front. Microbiol. 2018 9 3063 10.3389/fmicb.2018.03063
Donaldson G.P. Lee S.M. Mazmanian S.K. Gut biogeography of the bacterial microbiota Nat. Rev. Microbiol. 2016 14 20 32 10.1038/nrmicro3552 26499895
Kang C. Wang B. Kaliannan K. Wang X. Lang H. Hui S. Huang L. Zhang Y. Zhou M. Chen M. Gut microbiota mediates the protective effects of dietary capsaicin against chronic low-grade inflammation and associated obesity induced by high-fat diet mBio 2017 8 e00470-17 10.1128/mBio.00470-17 28536285
Owens L.A. Colitti B. Hirji I. Pizarro A. Jaffe J.E. Moittié S. Bishop-Lilly K.A. Estrella L.A. Voegtly L.J. Kuhn J.H. A Sarcina bacterium linked to lethal disease in sanctuary chimpanzees in Sierra Leone Nat. Commun. 2021 12 763 10.1038/s41467-021-21012-x 33536429
Nakamura S. Spirochete flagella and motility Biomolecules 2020 10 550 10.3390/biom10040550
Mølbak L. Klitgaard K. Jensen T.K. Fossi M. Boye M. Identification of a novel, invasive, not-yet-cultivated Treponema sp. in the large intestine of pigs by PCR amplification of the 16S rRNA gene J. Clin. Microbiol. 2006 44 4537 4540 10.1128/JCM.01537-06 17005743
Wen X. Wan F. Wu Y. Liu L. Liu Y. Zhong R. Chen L. Zhang H. Caffeic acid supplementation ameliorates intestinal injury by modulating intestinal microbiota in LPS-challenged piglets Food Funct. 2023 14 7705 7717 10.1039/D3FO02286B 37547959
Wang Z. Li X. Zhang L. Wu J. Zhao S. Jiao T. Effect of Oregano Oil and Cobalt Lactate on Sheep In Vitro Digestibility, Fermentation Characteristics and Rumen Microbial Community Animals 2022 12 118 10.3390/ani12010118 35011223
Qiu K. He W. Zhang H. Wang J. Qi G. Guo N. Zhang X. Wu S. Bio-Fermented Malic Acid Facilitates the Production of High-Quality Chicken via Enhancing Muscle Antioxidant Capacity of Broilers Antioxidants 2022 11 2309 10.3390/antiox11122309
Macfarlane S. Macfarlane G.T. Regulation of short-chain fatty acid production Proc. Nutr. Soc. 2003 62 67 72 10.1079/PNS2002207
Layden B.T. Angueira A.R. Brodsky M. Durai V. Lowe W.L. Jr. Short chain fatty acids and their receptors: New metabolic targets Transl. Res. 2013 161 131 140 10.1016/j.trsl.2012.10.007
Konikoff T. Gophna U. Oscillospira: A central, enigmatic component of the human gut microbiota Trends Microbiol. 2016 24 523 524 10.1016/j.tim.2016.02.015
Keren N. Konikoff F.M. Paitan Y. Gabay G. Reshef L. Naftali T. Gophna U. Interactions between the intestinal microbiota and bile acids in gallstones patients Environ. Microbiol. Rep. 2015 7 874 880 10.1111/1758-2229.12319 26149537
Fan Q. Du E. Chen F. Tao W. Zhao N. Huang S. Guo W. Huang J. Wei J. Maternal Magnolol Supplementation during Pregnancy and Lactation Promotes Antioxidant Capacity, Improves Gut Health, and Alters Gut Microbiota and Metabolites of Weanling Piglets Metabolites 2023 13 797 10.3390/metabo13070797 37512505
Koh A. De Vadder F. Kovatcheva-Datchary P. Bäckhed F. From dietary fiber to host physiology: Short-chain fatty acids as key bacterial metabolites Cell 2016 165 1332 1345 10.1016/j.cell.2016.05.041 27259147
Monnerie S. Comte B. Ziegler D. Morais J.A. Pujos-Guillot E. Gaudreau P. Metabolomic and lipidomic signatures of metabolic syndrome and its physiological components in adults: A systematic review Sci. Rep. 2020 10 669 10.1038/s41598-019-56909-7 31959772
Hu Z. Feng L. Jiang Q. Wang W. Tang X. Yin Y. Intestinal tryptophan metabolism in disease prevention and swine production Anim. Nutr. 2023 15 364 374 10.1016/j.aninu.2023.08.002 38058568
Wlodarska M. Luo C. Kolde R. d’Hennezel E. Annand J.W. Heim C.E. Krastel P. Schmitt E.K. Omar A.S. Creasey E.A. Indoleacrylic acid produced by commensal peptostreptococcus species suppresses inflammation Cell Host Microbe 2017 22 25 37.e26 10.1016/j.chom.2017.06.007 28704649
Liu M. Wang Y. Xiang H. Guo M. Li S. Liu M. Yao J. The Tryptophan Metabolite Indole-3-Carboxaldehyde Alleviates Mice with DSS-Induced Ulcerative Colitis by Balancing Amino Acid Metabolism, Inhibiting Intestinal Inflammation, and Improving Intestinal Barrier Function Molecules 2023 28 3704 10.3390/molecules28093704 37175112
Tremaroli V. Bäckhed F. Functional interactions between the gut microbiota and host metabolism Nature 2012 489 242 249 10.1038/nature11552
Cheng H. Wang M. Su J. Li Y. Long J. Chu J. Wan X. Cao Y. Li Q. Lipid Metabolism and Cancer Life 2022 12 784 10.3390/life12060784
Van Meer G. Voelker D.R. Feigenson G.W. Membrane lipids: Where they are and how they behave Nat. Rev. Mol. Cell Biol. 2008 9 112 124 10.1038/nrm2330
Chen Y.J. Zhang T.Y. Luo L. Shi Y.Q. Bai F.J. Jiang D.N. Impact of Dietary L-Malic Acid Supplementation on Growth, Feed Utilization, Ash Deposition, and Hepatic Lipid Metabolism of Juvenile Genetically Improved Farmed Tilapia, Oreochromis niloticus J. World Aquacult. Soc. 2017 48 563 573 10.1111/jwas.12388
Watanabe S. Togashi S.-i. Takahashi N. Fukui T. L-tryptophan as an antioxidant in human placenta extract J. Nutr. Sci. Vitaminol. 2002 48 36 39 10.3177/jnsv.48.36 12026186
Xu K. Liu H. Bai M. Gao J. Wu X. Yin Y. Redox properties of tryptophan metabolism and the concept of tryptophan use in pregnancy Int. J. Mol. Sci. 2017 18 1595 10.3390/ijms18071595
Nikolaus S. Schulte B. Al-Massad N. Thieme F. Schulte D.M. Bethge J. Rehman A. Tran F. Aden K. Häsler R. Increased tryptophan metabolism is associated with activity of inflammatory bowel diseases Gastroenterology 2017 153 1504 1516.e1502 10.1053/j.gastro.2017.08.028 28827067
Zhang L. Tan C. Xin Z. Huang S. Ma J. Zhang M. Shu G. Luo H. Deng B. Jiang Q. Uplc-orbitrap-ms/ms combined with biochemical analysis to determine the growth and development of mothers and fetuses in different gestation periods on Tibetan sow model Front. Nutr. 2022 9 836938 10.3389/fnut.2022.836938 35425793
Yang P. Deng F. Yuan M. Chen M. Zeng L. Ouyang Y. Chen X. Zhao B. Yang Z. Tian Z. Metabolomics reveals the defense mechanism of histidine supplementation on high-salt exposure-induced hepatic oxidative stress Life Sci. 2023 314 121355 10.1016/j.lfs.2022.121355 36596407
Rojas D.B. de Andrade R.B. Gemelli T. Oliveira L.S. Campos A.G. Dutra-Filho C.S. Wannmacher C.M.D. Effect of histidine administration to female rats during pregnancy and lactation on enzymes activity of phosphoryltransfer network in cerebral cortex and hippocampus of the offspring Metab. Brain Dis. 2012 27 595 603 10.1007/s11011-012-9319-5 22638695
Chen M. Zhao Y. Ji H. Li L. Liu H. Wang S. Zhang D. Yin J. Wang J. Zhang X. Chenodeoxycholic Acid Improves Embryo Implantation and Metabolic Health through Modulating Gut Microbiota–Host Metabolites Interaction during Early Pregnancy Antioxidants 2023 13 8 10.3390/antiox13010008
Chen M. Zhang B. Cai S. Zeng X. Ye Q. Mao X. Zhang S. Zeng X. Ye C. Qiao S. Metabolic disorder of amino acids, fatty acids and purines reflects the decreases in oocyte quality and potential in sows J. Proteom. 2019 200 134 143 10.1016/j.jprot.2019.03.015 30951908
Huang T. Wu Y. Huang L. Lin R. Li Z. Wang X. Wu P. Huang L. Mechanism of the Effect of Compound Anoectochilus roxburghii (Wall.) Lindl. Oral Liquid in Treating Alcoholic Rat Liver Injury by Metabolomics Drug Des. Devel. Ther. 2023 17 3409 3428 10.2147/DDDT.S427837 38024538
Heidari R. Mohammadi H. Ghanbarinejad V. Ahmadi A. Ommati M.M. Niknahad H. Jamshidzadeh A. Azarpira N. Abdoli N. Proline supplementation mitigates the early stage of liver injury in bile duct ligated rats J. Basic. Clin. Physiol. Pharmacol. 2018 30 91 101 10.1515/jbcpp-2017-0221 30205645
