Alginate oligosaccharides (AOS); Boars; Gut microbiota; Heat stress; Semen quality
Abstract :
[en] Heat stress is a serious problem that affects animal husbandry by reducing growth and reproductive performance of animals. Adding plant extracts to the diet is an effective way to help overcome this problem. Alginate oligosaccharide (AOS) is a natural non-toxic antioxidant with multiple biological activities. This study analyzed the potential mechanism of AOS in alleviating heat stress and improving semen quality in boars through a combination of multiple omics tools. The results indicated that AOS could significantly increase sperm motility (P < 0.001) and sperm concentration (P < 0.05). At the same time, AOS improved the antioxidant capacity of blood and semen, and increased blood testosterone (P < 0.05) level. AOS could improve the metabolites in sperm, change the composition of gut microbiota, increase the relative abundance of beneficial bacteria such as Pseudomonas (P < 0.01), Escherichia-Shigella (P < 0.05), Bifidobacterium (P < 0.01), reduce the relative abundance of harmful bacteria such as Prevotella_9 (P < 0.05), Prevotellaceae_UCG-001 (P < 0.01), and increase the content of short chain fatty acids. Proteomic results showed that AOS increased proteins related to spermatogenesis, while decreasing heat shock protein 70 (P < 0.05) and heat shock protein 90 (P < 0.01). These results were verified using immunofluorescence staining technology. There was a good correlation among sperm quality, sperm metabolome, sperm proteome, and gut microbiota. In conclusion, AOS can be used as a feed additive to increase the semen quality of boars to enhance reproductive performance under heat stress.
Disciplines :
Animal production & animal husbandry
Author, co-author :
Zhou, Yexun ; Université de Liège - ULiège > TERRA Research Centre ; State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, 100193, P. R. China
Wei, Zeou; State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, 100193, P. R. China ; School of Agriculture and Food Science, University College Dublin, Belfeld, Dublin 4, Ireland
Tan, Jiajian; YangXiang Joint Stock Company, Guigang, 53700, China
Sun, Haiqing; YangXiang Joint Stock Company, Guigang, 53700, China
Jiang, Haidi; YangXiang Joint Stock Company, Guigang, 53700, China
Gao, Yang; College of Life Science, Baicheng Normal University, Baicheng, 137000, Jilin, China. 179692058@qq.com
Zhang, Hongfu; State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, 100193, P. R. China. zhanghongfu@caas.cn
Schroyen, Martine ; Université de Liège - ULiège > Département GxABT > Animal Sciences (AS)
Language :
English
Title :
Alginate oligosaccharide supplementation improves boar semen quality under heat stress.
We would like to thank the Beijing Yung biotechnology Co., Ltd for technical support, and the Qingdao Bozhi Technology Co., Ltd. for providing the feed additive AOS. We also thank the Yangxiang Joint Stock Company for providing experimental conditions.This research was supported by the funding of CAAS of Agricultural Science and Technology Innovation Program (CAAS-ZDRW202006-02, ASTIPIAS07) and the State Key Laboratory of Animal Nutrition (2004DA125184G2102).
Baro Graf C, Ritagliati C, Stival C et al (2020) Everything you ever wanted to know about PKA regulation and its involvement in mammalian sperm capacitation. Mol Cell Endocrinol 518:110992. https://doi.org/10.1016/j.mce.2020.110992
Belhadj Slimen I, Najar T, Ghram A et al (2016) Heat stress effects on livestock: molecular, cellular and metabolic aspects, a review. J Anim Physiol Anim Nutr (berl) 100:401–412. https://doi.org/10.1111/jpn.12379
Bibbò S, Ianiro G, Giorgio V et al (2016) The role of diet on gut microbiota composition. Eur Rev Med Pharmacol Sci 20:4742–4749
Bland EJ, Keshavarz T, Bucke C (2004) The influence of small oligosaccharides on the immune system. Carbohydr Res 339:1673–1678. https://doi.org/10.1016/j.carres.2004.05.009
Bucak MN, Keskin N, Taşpınar M et al (2013) Raffinose and hypotaurine improve the post-thawed Merino ram sperm parameters. Cryobiology 67:34–39. https://doi.org/10.1016/j.cryobiol.2013.04.007
Cao XW, Lin K, Li CY et al (2011) A review of WHO laboratory manual for the examination and processing of human semen (5th edition). Zhonghua Nan Ke Xue 17:1059–1063
Cayli S, Sakkas D, Vigue L et al (2004) Cellular maturity and apoptosis in human sperm: creatine kinase, caspase-3 and Bcl-XL levels in mature and diminished maturity sperm. Mol Hum Reprod 10:365–372. https://doi.org/10.1093/molehr/gah050
Chalmel F, Rolland AD (2015) Linking transcriptomics and proteomics in spermatogenesis. Reproduction 150:R149–R157. https://doi.org/10.1530/rep-15-0073
Chang Q, Cai H, Wei L et al (2022) Chitosan oligosaccharides alleviate acute heat stress-induced oxidative damage by activating ERK1/2-mediated HO-1 and GSH-Px gene expression in breast muscle of broilers. Poult Sci 101:101515. https://doi.org/10.1016/j.psj.2021.101515
Chen JQ, Li YS, Li ZJ et al (2018) Dietary l-arginine supplementation improves semen quality and libido of boars under high ambient temperature. Animal 12:1611–1620. https://doi.org/10.1017/s1751731117003147
Chen R, Xu Y, Wu P et al (2019) Transplantation of fecal microbiota rich in short chain fatty acids and butyric acid treat cerebral ischemic stroke by regulating gut microbiota. Pharmacol Res 148:104403. https://doi.org/10.1016/j.phrs.2019.104403
Cramer MN, Gagnon D, Laitano O et al (2022) Human temperature regulation under heat stress in health, disease, and injury. Physiol Rev 102:1907–1989. https://doi.org/10.1152/physrev.00047.2021
Dervishi E, Yang T, Dyck MK et al (2021) Heritability and genetic correlations of plasma metabolites of pigs with production, resilience and carcass traits under natural polymicrobial disease challenge. Sci Rep 11:20628. https://doi.org/10.1038/s41598-021-99778-9
Falkeborg M, Cheong LZ, Gianfico C et al (2014) Alginate oligosaccharides: enzymatic preparation and antioxidant property evaluation. Food Chem 164:185–194. https://doi.org/10.1016/j.foodchem.2014.05.053
Farahani L, Tharakan T, Yap T et al (2021) The semen microbiome and its impact on sperm function and male fertility: a systematic review and meta-analysis. Andrology 9:115–144. https://doi.org/10.1111/andr.12886
Francou MM, Hombrebueno JR, De Juan J (2012) Identification and cellular location of glutamine synthetase in human sperm. Cell Tissue Res 350:183–187. https://doi.org/10.1007/s00441-012-1465-x
Gachet C, Prat M, Burucoa C et al (2022) Spermatic microbiome characteristics in infertile patients: impact on sperm count, mobility, and morphology. J Clin Med 11(6):1505. https://doi.org/10.3390/jcm11061505
Garcia DN, Hense JD, Zanini BM et al (2023) Dasatinib and quercetin increase testosterone and sperm concentration in mice. Physiol Int 110:121–134. https://doi.org/10.1556/2060.2023.00192
Gasbarrini G, Montalto M, Santoro L, Curigliano V, D’Onofrio F, Gallo A, Visca D, Gasbarrini A (2008) Intestine: organ or apparatus? Dig Dis 26:92–95. https://doi.org/10.1159/000116765
Ge LQ, Xia T, Huang B et al (2016) Suppressing male spermatogenesis-associated protein 5-like gene expression reduces vitellogenin gene expression and fecundity in Nilaparvata lugens Stål. Sci Rep 6:28111. https://doi.org/10.1038/srep28111
Goto H, Nakashima M, Nakashima H et al (2022) Heat acclimation ameliorated heat stress-induced acute kidney injury and prevented changes in kidney macrophages and fibrosis. Am J Physiol Renal Physiol 323:F243–F254. https://doi.org/10.1152/ajprenal.00065.2022
Gruhot TR, Rempel LA, White BR et al (2020) The effect of varicocele on semen quality in boars exposed to heat stress. Transl Anim Sci 4:293–298. https://doi.org/10.1093/tas/txaa003
Guo Z, Lv L, Liu D et al (2018) Effects of heat stress on piglet production/performance parameters. Trop Anim Health Prod 50:1203–1208. https://doi.org/10.1007/s11250-018-1633-4
Guo L, Wu Y, Wang C et al (2020) Gut microbiological disorders reduce semen utilization rate in duroc boars. Front Microbiol 11:581926. https://doi.org/10.3389/fmicb.2020.581926
Han H, Zhou Y, Xiong B et al (2022) Alginate oligosaccharides increase boar semen quality by affecting gut microbiota and metabolites in blood and sperm. Front Microbiol 13:982152. https://doi.org/10.3389/fmicb.2022.982152
Hao Y, Feng Y, Yan X et al (2022) Gut microbiota-testis axis: FMT improves systemic and testicular micro-environment to increase semen quality in type 1 diabetes. Mol Med 28:45. https://doi.org/10.1186/s10020-022-00473-w
Hawkins CL, Davies MJ (2019) Detection, identification, and quantification of oxidative protein modifications. J Biol Chem 294:19683–19708. https://doi.org/10.1074/jbc.rev119.006217
He Q, Han C, Huang L et al (2020) Astragaloside IV alleviates mouse slow transit constipation by modulating gut microbiota profile and promoting butyric acid generation. J Cell Mol Med 24:9349–9361. https://doi.org/10.1111/jcmm.15586
Hu J, Lin S, Zheng B, Cheung PCK (2018) Short-chain fatty acids in control of energy metabolism. Crit Rev Food Sci Nutr 58:1243–1249. https://doi.org/10.1080/10408398.2016.1245650
Jannatifar R, Parivar K, Roodbari NH et al (2019) Effects of N-acetyl-cysteine supplementation on sperm quality, chromatin integrity and level of oxidative stress in infertile men. Reprod Biol Endocrinol 17:24. https://doi.org/10.1186/s12958-019-0468-9
Kumar M, Ratwan P, Dahiya SP et al (2021) Climate change and heat stress: impact on production, reproduction and growth performance of poultry and its mitigation using genetic strategies. J Therm Biol 97:102867. https://doi.org/10.1016/j.jtherbio.2021.102867
Li Z, Li Y, Zhou X et al (2017) Preventive effects of supplemental dietary zinc on heat-induced damage in the epididymis of boars. J Therm Biol 64:58–66. https://doi.org/10.1016/j.jtherbio.2017.01.002
Lin Y, Wang K, Che L et al (2022) The improvement of semen quality by dietary fiber intake is positively related with gut microbiota and SCFA in a boar model. Front Microbiol 13:863315. https://doi.org/10.3389/fmicb.2022.863315
Liu Y, Zhang L, Li W et al (2019) The sperm-associated antigen 6 interactome and its role in spermatogenesis. Reproduction 158:181–197. https://doi.org/10.1530/rep-18-0522
Liu L, Wang M, Gong N et al (2021) Se improves GPX4 expression and SOD activity to alleviate heat-stress-induced ferroptosis-like death in goat mammary epithelial cells. Anim Cells Syst (seoul) 25:283–295. https://doi.org/10.1080/19768354.2021.1988704
Liu C, Jiang F, Xing Z et al (2022) Efficient delivery of curcumin by alginate oligosaccharide coated aminated mesoporous silica nanoparticles and in vitro anticancer activity against colon cancer cells. Pharmaceutics 14(6):1166. https://doi.org/10.3390/pharmaceutics14061166
Lu S, Na K, Wei J et al (2022) Alginate oligosaccharides: The structure-function relationships and the directional preparation for application. Carbohydr Polym 284:119225. https://doi.org/10.1016/j.carbpol.2022.119225
Lundy SD, Sangwan N, Parekh NV et al (2021) Functional and taxonomic dysbiosis of the gut, urine, and semen microbiomes in male infertility. Eur Urol 79:826–836. https://doi.org/10.1016/j.eururo.2021.01.014
Luo L, Zhang S, Wu J et al (2021) Heat stress in macrofungi: effects and response mechanisms. Appl Microbiol Biotechnol 105:7567–7576. https://doi.org/10.1007/s00253-021-11574-7
Madsen MD, Madsen P, Nielsen B et al (2018) Macro-environmental sensitivity for growth rate in Danish Duroc pigs is under genetic control. J Anim Sci 96:4967–4977. https://doi.org/10.1093/jas/sky376
Marnett LJ (2000) Oxyradicals and DNA damage. Carcinogenesis 21:361–370. https://doi.org/10.1093/carcin/21.3.361
Minami K, Arai-Aso MM, Ogura-Kodama Y et al (2020) Characteristics of bull sperm acrosome associated 1 proteins. Anim Reprod Sci 218:106479. https://doi.org/10.1016/j.anireprosci.2020.106479
Mrudulakumari Vasudevan U, Lee OK, Lee EY (2021) Alginate derived functional oligosaccharides: recent developments, barriers, and future outlooks. Carbohydr Polym 267:118158. https://doi.org/10.1016/j.carbpol.2021.118158
Nordberg J, Arnér ES (2001) Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radic Biol Med 31:1287–1312. https://doi.org/10.1016/s0891-5849(01)00724-9
Olaniyi KS, Badejogbin OC, Saliu SB et al (2021) Rescue effect of sodium acetate in diabetes mellitus-associated testicular dysfunction is accompanied by PCSK9 modulation. Biochimie 184:52–62. https://doi.org/10.1016/j.biochi.2021.02.004
Ouyang J, Zhou H, Li Q et al (2022) Tryptophan alleviates acute heat stress-induced impairment of antioxidant status and mitochondrial function in broilers. Front Vet Sci 9:863156. https://doi.org/10.3389/fvets.2022.863156
Pradhan BS, Bhattacharya I, Sarkar R et al (2020) Pubertal down-regulation of Tetraspanin 8 in testicular Sertoli cells is crucial for male fertility. Mol Hum Reprod 26:760–772. https://doi.org/10.1093/molehr/gaaa055
Prieto-Martínez N, Bussalleu E, Garcia-Bonavila E et al (2014) Effects of Enterobacter cloacae on boar sperm quality during liquid storage at 17°C. Anim Reprod Sci 148:72–82. https://doi.org/10.1016/j.anireprosci.2014.05.008
Pritchard MF, Jack AA, Powell LC et al (2017) Alginate oligosaccharides modify hyphal infiltration of Candida albicans in an in vitro model of invasive human candidosis. J Appl Microbiol 123:625–636. https://doi.org/10.1111/jam.13516
Rahban R, Rehfeld A, Schiffer C et al (2021) The antidepressant Sertraline inhibits CatSper Ca2+ channels in human sperm. Hum Reprod 36:2638–2648. https://doi.org/10.1093/humrep/deab190
Ramírez-Acosta S, Selma-Royo M, Collado MC et al (2022) Selenium supplementation influences mice testicular selenoproteins driven by gut microbiota. Sci Rep 12:4218. https://doi.org/10.1038/s41598-022-08121-3
Saghir SAM, Al Hroob AM, Majrashi KA et al (2023) Effects of alginates on the growth, haematological, immunity, antioxidant and pro-inflammatory responses of rabbits under high temperature. Res Vet Sci 155:36–43. https://doi.org/10.1016/j.rvsc.2023.01.002
Sangeeta K, Yenugu S (2022) Ablation of the sperm-associated antigen 11A (SPAG11A) protein by active immunization promotes epididymal oncogenesis in the rat. Cell Tissue Res 389:115–128. https://doi.org/10.1007/s00441-022-03623-y
Sepúlveda L, Bussalleu E, Yeste M et al (2014) Effects of different concentrations of Pseudomonas aeruginosa on boar sperm quality. Anim Reprod Sci 150:96–106. https://doi.org/10.1016/j.anireprosci.2014.09.001
Sepúlveda L, Bussalleu E, Yeste M et al (2016) Effect of Pseudomonas aeruginosa on sperm capacitation and protein phosphorylation of boar spermatozoa. Theriogenology 85:1421–1431. https://doi.org/10.1016/j.theriogenology.2015.12.025
Serviento AM, Labussière E, Castex M et al (2020) Effect of heat stress and feeding management on growth performance and physiological responses of finishing pigs. J Anim Sci 98(12):skaa387. https://doi.org/10.1093/jas/skaa387
Smith LB, Walker WH (2014) The regulation of spermatogenesis by androgens. Semin Cell Dev Biol 30:2–13. https://doi.org/10.1016/j.semcdb.2014.02.012
Stombaugh DP, Roller WL, Adams T et al (1973) Temperature regulation in neonatal piglets during mild cold and severe heat stress. Am J Physiol 225:1192–1198. https://doi.org/10.1152/ajplegacy.1973.225.5.1192
Su LJ, Zhang JH, Gomez H et al (2019) Reactive oxygen species-induced lipid peroxidation in apoptosis, autophagy, and ferroptosis. Oxid Med Cell Longev 2019:5080843. https://doi.org/10.1155/2019/5080843
Sui H, Wang S, Liu G et al (2022) Effects of heat stress on motion characteristics and metabolomic profiles of boar spermatozoa. Genes (Basel) 13(9):1647. https://doi.org/10.3390/genes13091647
Thirumalaikumar VP, Gorka M, Schulz K et al (2021) Selective autophagy regulates heat stress memory in Arabidopsis by NBR1-mediated targeting of HSP90.1 and ROF1. Autophagy 17:2184–2199. https://doi.org/10.1080/15548627.2020.1820778
Thundathil JC, Rajamanickam GD, Kastelic JP et al (2012) The effects of increased testicular temperature on testis-specific isoform of Na+/K+ -ATPase in sperm and its role in spermatogenesis and sperm function. Reprod Domest Anim 47(Suppl 4):170–177. https://doi.org/10.1111/j.1439-0531.2012.02072.x
Usuda H, Okamoto T, Wada K (2021) Leaky gut: effect of dietary fiber and fats on microbiome and intestinal barrier. Int J Mol Sci 22(14):7613. https://doi.org/10.3390/ijms22147613
Valcarce DG, Genovés S, Riesco MF et al (2017) Probiotic administration improves sperm quality in asthenozoospermic human donors. Benef Microbes 8:193–206. https://doi.org/10.3920/bm2016.0122
Valko M, Leibfritz D, Moncol J et al (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39:44–84. https://doi.org/10.1016/j.biocel.2006.07.001
van Anders SM (2012) Testosterone and sexual desire in healthy women and men. Arch Sex Behav 41:1471–1484. https://doi.org/10.1007/s10508-012-9946-2
Wan J, Zhang J, Chen D et al (2018a) Alginate oligosaccharide enhances intestinal integrity of weaned pigs through altering intestinal inflammatory responses and antioxidant status. RSC Adv 8:13482–13492. https://doi.org/10.1039/c8ra01943f
Wan J, Zhang J, Chen D et al (2018b) Alginate oligosaccharide alleviates enterotoxigenic Escherichia coli-induced intestinal mucosal disruption in weaned pigs. Food Funct 9:6401–6413. https://doi.org/10.1039/c8fo01551a
Wan F, Zhong R, Wang M et al (2021a) Caffeic acid supplement alleviates colonic inflammation and oxidative stress potentially through improved gut microbiota community in mice. Front Microbiol 12:784211. https://doi.org/10.3389/fmicb.2021.784211
Wan J, Zhang J, Xu Q et al (2021b) Alginate oligosaccharide protects against enterotoxigenic Escherichia coli-induced porcine intestinal barrier injury. Carbohydr Polym 270:118316. https://doi.org/10.1016/j.carbpol.2021.118316
Wang M, Chen L, Zhang Z (2021) Potential applications of alginate oligosaccharides for biomedicine - A mini review. Carbohydr Polym 271:118408. https://doi.org/10.1016/j.carbpol.2021.118408
Wegner K, Lambertz C, Das G et al (2016) Effects of temperature and temperature-humidity index on the reproductive performance of sows during summer months under a temperate climate. Anim Sci J 87:1334–1339. https://doi.org/10.1111/asj.12569
Yan X, Feng Y, Hao Y et al (2022) Gut-Testis axis: microbiota prime metabolome to increase sperm quality in young type 2 diabetes. Microbiol Spectr 10:e0142322. https://doi.org/10.1128/spectrum.01423-22
Yelumalai S, Giribabu N, Karim K et al (2019) In vivo administration of quercetin ameliorates sperm oxidative stress, inflammation, preserves sperm morphology and functions in streptozotocin-nicotinamide induced adult male diabetic rats. Arch Med Sci 15:240–249. https://doi.org/10.5114/aoms.2018.81038
Zhang Y, Li W, Chen TT et al (2020) Chemical fingerprint analysis and ultra-performance liquid chromatography quadrupole time-of-flight mass spectrometry-based metabolomics study of the protective effect of Buxue Yimu Granule in medical-induced incomplete abortion rats. Front Pharmacol 11:578217. https://doi.org/10.3389/fphar.2020.578217
Zhang P, Feng Y, Li L et al (2021) Improvement in sperm quality and spermatogenesis following faecal microbiota transplantation from alginate oligosaccharide dosed mice. Gut 70:222–225. https://doi.org/10.1136/gutjnl-2020-320992
Zhou Y, Chen L, Han H et al (2022) Taxifolin increased semen quality of Duroc boars by improving gut microbes and blood metabolites. Front Microbiol 13:1020628. https://doi.org/10.3389/fmicb.2022.1020628
Zuleta-González MC, Zapata-Salazar ME, Guerrero-Hurtado LS et al (2019) Klebsiella pneumoniae and Streptococcus agalactiae: passengers in the sperm travel. Arch Esp Urol 72:939–947
