[en] [en] INTRODUCTION: Alginate oligosaccharide (AOS), as a natural non-toxic plant extract, has been paid more attention in recent years due to its strong antioxidant, anti-inflammatory, and even anti-cancer properties. However, the mechanism by which AOS affects animal reproductive performance is still unclear.
METHODS: The purpose of this study is to use multi-omics technology to analyze the effects of AOS in extending the service lifespan of aging boars.
RESULTS: The results showed that AOS can significantly improve the sperm motility (p < 0.05) and sperm validity rate (p < 0.001) of aging boars and significantly reduce the abnormal sperm rate (p < 0.01) by increasing the protein levels such as CatSper 8 and protein kinase A (PKA) for semen quality. At the same time, AOS significantly improved the testosterone content in the blood of boars (p < 0.01). AOS significantly improved fatty acids such as adrenic acid (p < 0.05) and antioxidants such as succinic acid (p < 0.05) in sperm metabolites, significantly reducing harmful substances such as dibutyl phthalate (p < 0.05), which has a negative effect on spermatogenesis. AOS can improve the composition of intestinal microbes, mainly increasing beneficial bacteria Enterobacter (p = 0.1262) and reducing harmful bacteria such as Streptococcus (p < 0.05), Prevotellaceae_UCG-001 (p < 0.05), and Prevotellaceae_NK3B31_group (p < 0.05). Meanwhile, short-chain fatty acids in feces such as acetic acid (p < 0.05) and butyric acid (p < 0.05) were significantly increased. Spearman correlation analysis showed that there was a close correlation among microorganisms, sperm metabolites, and sperm parameters.
DISCUSSION: Therefore, the data indicated that AOS improved the semen quality of older boars by improving the intestinal microbiota and sperm metabolome. AOS can be used as a feed additive to solve the problem of high elimination rate in large-scale boar studs.
Disciplines :
Animal production & animal husbandry Microbiology
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, China
Wei, Zeou; State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, China
Tan, Jiajian; YangXiang Joint Stock Company, Animal Nutrition Institute, Guigang, China
Sun, Haiqing; YangXiang Joint Stock Company, Animal Nutrition Institute, Guigang, China
Jiang, Haidi; YangXiang Joint Stock Company, Animal Nutrition Institute, Guigang, China
Gao, Yang; College of Life Science, Baicheng Normal University, Baicheng, Jilin, China
Zhang, Hongfu; State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, China
Schroyen, Martine ; Université de Liège - ULiège > Département GxABT > Animal Sciences (AS)
Language :
English
Title :
Alginate oligosaccharide extends the service lifespan by improving the sperm metabolome and gut microbiota in an aging Duroc boars model.
The author(s) declare financial support was received for the research, authorship, and/or publication of this article. 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). Acknowledgments
Akerfelt M. Morimoto R. I. Sistonen L. (2010). Heat shock factors: integrators of cell stress, development and lifespan. Nat. Rev. Mol. Cell Biol. 11, 545–555. doi: 10.1038/nrm2938
Aly H. A. Hassan M. H. El-Beshbishy H. A. Alahdal A. M. Osman A. M. (2016). Dibutyl phthalate induces oxidative stress and impairs spermatogenesis in adult rats. Toxicol. Ind. Health 32, 1467–1477. doi: 10.1177/0748233714566877
Baro Graf C. Ritagliati C. Stival C. Luque G. M. Gentile I. Buffone M. G. et al. (2020). Everything you ever wanted to know about pka regulation and its involvement in mammalian sperm capacitation. Mol. Cell Endocrinol. 518, 110992. doi: 10.1016/j.mce.2020.110992
Berger T. Mahone J. P. Svoboda G. S. Metz K. W. Clegg E. D. (1980). Sexual maturation of boars and growth of swine exposed to extended photoperiod during decreasing natural photoperiod. J. Anim. Sci. 51, 672–678. doi: 10.2527/jas1980.513672x
Cao X. W. Lin K. Li C. Y. Yuan C. W. (2011). [A review of who laboratory manual for the examination and processing of human semen (5th edition)]. Zhonghua Nan Ke Xue 17, 1059–1063.
Carlson A. E. Burnett L. A. Del Camino D. Quill T. A. Hille B. Chong J. A. et al. (2009). Pharmacological targeting of native catsper channels reveals A required role in maintenance of sperm hyperactivation. PloS One 4, E6844. doi: 10.1371/journal.pone.0006844
Cassady J. P. Young L. D. Leymaster K. A. (2002). Heterosis and recombination effects on pig reproductive traits. J. Anim. Sci. 80, 2303–2315. doi: 10.2527/2002.8092303x
Czubacka E. Czerczak S. Kupczewska-Dobecka M. M. (2021). The overview of current evidence on the reproductive toxicity of dibutyl phthalate. Int. J. Occup. Med. Environ. Health 34, 15–37. doi: 10.13075/ijomeh.1896.01658
D’Allaire S. Leman A. D. (1990). Boar culling in swine breeding herds in minnesota. Can. Vet. J. 31, 581–583.
D’Allaire S. Leman A. D. Drolet R. (1992). Optimizing longevity in sows and boars. Vet. Clin. North Am. Food Anim. Pract. 8, 545–557. doi: 10.1016/S0749-0720(15)30703-9
De Gregorio V. Telesco M. Corrado B. Rosiello V. Urciuolo F. Netti P. A. et al. (2020). Intestine-liver axis on-chip reveals the intestinal protective role on hepatic damage by emulating ethanol first-pass metabolism. Front. Bioeng Biotechnol. 8, 163. doi: 10.3389/fbioe.2020.00163
Du Y. Du Z. Zheng H. Wang D. Li S. Yan Y. et al. (2013). Gaba exists as A negative regulator of cell proliferation in spermatogonial stem cells. [Corrected]. Cell Mol. Biol. Lett. 18, 149–162. doi: 10.2478/s11658-013-0081-4
Farahani L. Tharakan T. Yap T. Ramsay J. W. Jayasena C. N. Minhas S. (2021). The semen microbiome and its impact on sperm function and male fertility: a systematic review and meta-analysis. Andrology 9, 115–144. doi: 10.1111/andr.12886
Feng W. Hu Y. An N. Feng Z. Liu J. Mou J. et al. (2020). Alginate oligosaccharide alleviates monocrotaline-induced pulmonary hypertension via anti-oxidant and anti-inflammation pathways in rats. Int. Heart J. 61, 160–168. doi: 10.1536/ihj.19-096
Feng W. Liu J. Wang S. Hu Y. Pan H. Hu T. et al. (2021). Alginate oligosaccharide alleviates D-galactose-induced cardiac ageing via regulating myocardial mitochondria function and integrity in mice. J. Cell Mol. Med. 25, 7157–7168. doi: 10.1111/jcmm.16746
Frenkel G. Peterson R. N. Freund M. (1975). Oxidative and glycolytic metabolism of semen components by washed Guinea pig spermatozoa. Fertil Steril 26, 144–147. doi: 10.1016/S0015-0282(16)40934-9
Ge R. S. Li X. Wang Y. (2021). Leydig cell and spermatogenesis. Adv. Exp. Med. Biol. 1288, 111–129. doi: 10.1007/978-3-030-77779-1_6
Golan R. Soffer Y. Katz S. Weissenberg R. Wasserzug O. Lewin L. M. (1983). Carnitine and short-chain acylcarnitines in the lumen of the human male reproductive tract. Int. J. Androl 6, 349–357. doi: 10.1111/j.1365-2605.1983.tb00549.x
Guo L. Wu Y. Wang C. Wei H. Tan J. Sun H. et al. (2020). Gut microbiological disorders reduce semen utilization rate in duroc boars. Front. Microbiol. 11, 581926. doi: 10.3389/fmicb.2020.581926
Han Y. Zhang L. Yu X. Wang S. Xu C. Yin H. et al. (2019). Alginate oligosaccharide attenuates Α2,6-sialylation modification to inhibit prostate cancer cell growth via the hippo/yap pathway. Cell Death Dis. 10, 374. doi: 10.1038/s41419-019-1560-y
Han H. Zhou Y. Xiong B. Zhong R. Jiang Y. Sun H. et al. (2022). Alginate oligosaccharides increase boar semen quality by affecting gut microbiota and metabolites in blood and sperm. Front. Microbiol. 13, 982152. doi: 10.3389/fmicb.2022.982152
Hao Y. Feng Y. Yan X. Chen L. Zhong R. Tang 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. doi: 10.1186/s10020-022-00473-w
He J. Zhang P. Shen L. Niu L. Tan Y. Chen L. et al. (2020). Short-chain fatty acids and their association with signalling pathways in inflammation, glucose and lipid metabolism. Int. J. Mol. Sci. 21(17):6356. doi: 10.3390/ijms21176356
Hoffman J. M. Valencak T. G. (2020). A short life on the farm: aging and longevity in agricultural, large-bodied mammals. Geroscience 42, 909–922. doi: 10.1007/s11357-020-00190-4
Hu J. Lin S. Zheng B. Cheung P. C. K. (2018). Short-chain fatty acids in control of energy metabolism. Crit. Rev. Food Sci. Nutr. 58, 1243–1249. doi: 10.1080/10408398.2016.1245650
Huang S. Cao S. Zhou T. Kong L. Liang G. (2018). 4-tert-octylphenol injures motility and viability of human sperm by affecting camp-pka/pkc-tyrosine phosphorylation signals. Environ. Toxicol. Pharmacol. 62, 234–243. doi: 10.1016/j.etap.2018.07.010
Huang P. Jiang A. Wang X. Zhou Y. Tang W. Ren C. et al. (2021). Nmn maintains intestinal homeostasis by regulating the gut microbiota. Front. Nutr. 8, 714604. doi: 10.3389/fnut.2021.714604
Khordad E. Nikravesh M. R. Jalali M. Fazel A. Sankian M. Alipour F. (2022). Evaluation of sperm chromatin/dna integrity, morphology, and catsper expression on diabetic C57bl/6 mice. Cell Mol. Biol. (Noisy-Le-Grand) 68, 8–18. doi: 10.14715/cmb/2022.68.2.2
Knox R. Levis D. Safranski T. Singleton W. (2008). An update on north american boar stud practices. Theriogenology 70, 1202–1208. doi: 10.1016/j.theriogenology.2008.06.036
Koketsu Y. Sasaki Y. (2009). Boar culling and mortality in commercial swine breeding herds. Theriogenology 71, 1186–1191. doi: 10.1016/j.theriogenology.2008.12.018
Lai K. P. Lee J. C. Wan H. T. Li J. W. Wong A. Y. Chan T. F. et al. (2017). Effects of in utero pfos exposure on transcriptome, lipidome, and function of mouse testis. Environ. Sci. Technol. 51, 8782–8794. doi: 10.1021/acs.est.7b02102
Li F. Tang Y. Wei L. Yang M. Lu Z. Shi F. et al. (2022). Alginate oligosaccharide modulates immune response, fat metabolism, and the gut bacterial community in grass carp (Ctenopharyngodon idellus). Fish Shellfish Immunol. 130, 103–113. doi: 10.1016/j.fsi.2022.08.067
Liu P. Wang Y. Yang G. Zhang Q. Meng L. Xin Y. et al. (2021). The role of short-chain fatty acids in intestinal barrier function, inflammation, oxidative stress, and colonic carcinogenesis. Pharmacol. Res. 165, 105420. doi: 10.1016/j.phrs.2021.105420
Longobardi V. Kosior M. A. Pagano N. Fatone G. Staropoli A. Vassetti A. et al. (2020). Changes in bull semen metabolome in relation to cryopreservation and fertility. Anim. (Basel) 10(6):1065. doi: 10.3390/ani10061065
Lu S. Na K. Wei J. Tao T. Zhang L. Fang Y. et al. (2023). Alginate oligosaccharide structures differentially affect dss-induced colitis in mice by modulating gut microbiota. Carbohydr Polym 312, 120806. doi: 10.1016/j.carbpol.2023.120806
Nikolopoulou M. Soucek D. A. Vary J. C. (1985). Changes in the lipid content of boar sperm plasma membranes during epididymal maturation. Biochim. Biophys. Acta 815, 486–498. doi: 10.1016/0005-2736(85)90377-3
Plaengkaeo S. Duangjinda M. Stalder K. J. (2021). Longevity and lifetime reproductive trait genetic parameter estimates from thai landrace and large white pig populations. Trop. Anim. Health Prod 53, 319. doi: 10.1007/s11250-021-02579-5
Poulsen B. G. Nielsen B. Ostersen T. Christensen O. F. (2020). Genetic associations between stayability and longevity in commercial crossbred sows, and stayability in multiplier sows. J. Anim. Sci. 98(6):skaa183. doi: 10.1093/jas/skaa183
Prieto-Martínez N. Bussalleu E. Garcia-Bonavila E. Bonet S. Yeste M. (2014). Effects of enterobacter cloacae on boar sperm quality during liquid storage at 17°C. Anim. Reprod. Sci. 148, 72–82. doi: 10.1016/j.anireprosci.2014.05.008
Saigusa M. Nishizawa M. Shimizu Y. Saeki H. (2015). In vitro and in vivo anti-inflammatory activity of digested peptides derived from salmon myofibrillar protein conjugated with A small quantity of alginate oligosaccharide. Biosci. Biotechnol. Biochem. 79, 1518–1527. doi: 10.1080/09168451.2015.1031075
Sancho S. Pinart E. Briz M. Garcia-Gil N. Badia E. Bassols J. et al. (2004). Semen quality of postpubertal boars during increasing and decreasing natural photoperiods. Theriogenology 62, 1271–1282. doi: 10.1016/j.theriogenology.2004.01.003
Sheng W. Xu W. Ding J. Lu B. Liu L. He Q. et al. (2023). Guijiajiao (Colla carapacis et plastri, ccp) prevents male infertility via gut microbiota modulation. Chin. J. Nat. Med. 21, 403–410. doi: 10.1016/S1875-5364(23)60471-6
Smith L. B. Walker W. H. (2014). The regulation of spermatogenesis by androgens. Semin. Cell Dev. Biol. 30, 2–13. doi: 10.1016/j.semcdb.2014.02.012
Spinaci M. Perteghella S. Chlapanidas T. Galeati G. Vigo D. Tamanini C. et al. (2016). Storage of sexed boar spermatozoa: limits and perspectives. Theriogenology 85, 65–73. doi: 10.1016/j.theriogenology.2015.05.018
Takiishi T. Fenero C. I. M. Câmara N. O. S. (2017). Intestinal barrier and gut microbiota: shaping our immune responses throughout life. Tissue Barriers 5, E1373208. doi: 10.1080/21688370.2017.1373208
Uloko M. Rahman F. Puri L. I. Rubin R. S. (2022). The clinical management of testosterone replacement therapy in postmenopausal women with hypoactive sexual desire disorder: a review. Int. J. Impot Res. 34, 635–641. doi: 10.1038/s41443-022-00613-0
van Anders S. M. (2012). Testosterone and sexual desire in healthy women and men. Arch. Sex Behav. 41, 1471–1484. doi: 10.1007/s10508-012-9946-2
Walker W. H. (2021). Androgen actions in the testis and the regulation of spermatogenesis. Adv. Exp. Med. Biol. 1288, 175–203. doi: 10.1007/978-3-030-77779-1_9
Wan F. Zhong R. Wang M. Zhou Y. Chen Y. Yi B. et al. (2021). Caffeic acid supplement alleviates colonic inflammation and oxidative stress potentially through improved gut microbiota community in mice. Front. Microbiol. 12, 784211. doi: 10.3389/fmicb.2021.784211
Wu Y. Ran L. Yang Y. Gao X. Peng M. Liu S. et al. (2023). Deferasirox alleviates dss-induced ulcerative colitis in mice by inhibiting ferroptosis and improving intestinal microbiota. Life Sci. 314, 121312. doi: 10.1016/j.lfs.2022.121312
Yan X. Feng Y. Hao Y. Zhong R. Jiang Y. Tang X. et al. (2022). Gut-testis axis: microbiota prime metabolome to increase sperm quality in young type 2 diabetes. Microbiol. Spectr. 10, E0142322. doi: 10.1128/spectrum.01423-22
Yan Q. Huang H. Lu S. Ou B. Feng J. Shan W. et al. (2020). Pacap ameliorates fertility in obese male mice via pka/creb pathway-dependent sirt1 activation and P53 deacetylation. J. Cell Physiol. 235, 7465–7483. doi: 10.1002/jcp.29651
Yang B. Joe G. H. Li W. Shimizu Y. Saeki H. (2022). Comparison of maillard-type glycated collagen with alginate oligosaccharide and glucose: its characterization, antioxidant activity, and cytoprotective activity on H(2)O(2)-induced cell oxidative damage. Foods 11(15):2374. doi: 10.3390/foods11152374
Yeste M. Bonet S. Rodríguez-Gil J. E. Rivera Del Álamo M. M. (2018). Evaluation of sperm motility with casa-mot: which factors may influence our measurements? Reprod. Fertil Dev. 30, 789–798. doi: 10.1071/RD17475
Zhang P. Feng Y. Li L. Ge W. Yu S. Hao Y. et al. (2021b). Improvement in sperm quality and spermatogenesis following faecal microbiota transplantation from alginate oligosaccharide dosed mice. Gut 70, 222–225. doi: 10.1136/gutjnl-2020-320992
Zhang Y. Guo C. Li Y. Han X. Luo X. Chen L. et al. (2022a). Alginate oligosaccharides ameliorate dss-induced colitis through modulation of AMPK/NF-Κb pathway and intestinal microbiota. Nutrients 14(14):2864. doi: 10.3390/nu14142864
Zhang Y. Qin S. Song Y. Yuan J. Hu S. Chen M. et al. (2022b). Alginate oligosaccharide alleviated cisplatin-induced kidney oxidative stress via lactobacillus genus-FAHFAs-Nrf2 axis in mice. Front. Immunol. 13, 857242. doi: 10.3389/fimmu.2022.857242
Zhang C. Xiong B. Chen L. Ge W. Yin S. Feng Y. et al. (2021a). Rescue of male fertility following faecal microbiota transplantation from alginate oligosaccharide-dosed mice. Gut 70, 2213–2215. doi: 10.1136/gutjnl-2020-323593
Zhao J. Han Y. Wang Z. Zhang R. Wang G. Mao Y. (2020a). Alginate oligosaccharide protects endothelial cells against oxidative stress injury via integrin-Α/Fak/Pi3k signaling. Biotechnol. Lett. 42, 2749–2758. doi: 10.1007/s10529-020-03010-z
Zhao Y. Li X. N. Zhang H. Cui J. G. Wang J. X. Chen M. S. et al. (2022). Phthalate-induced testosterone/androgen receptor pathway disorder on spermatogenesis and antagonism of lycopene. J. Hazard Mater 439, 129689. doi: 10.1016/j.jhazmat.2022.129689
Zhao T. X. Wei Y. X. Wang J. K. Han L. D. Sun M. Wu Y. H. et al. (2020b). The gut-microbiota-testis axis mediated by the activation of the Nrf2 antioxidant pathway is related to prepuberal steroidogenesis disorders induced by di-(2-ethylhexyl) phthalate. Environ. Sci. pollut. Res. Int. 27, 35261–35271. doi: 10.1007/s11356-020-09854-2
Zhao Y. Zhang P. Ge W. Feng Y. Li L. Sun Z. et al. (2020c). Alginate oligosaccharides improve germ cell development and testicular microenvironment to rescue busulfan disrupted spermatogenesis. Theranostics 10, 3308–3324. doi: 10.7150/thno.43189
Zhou Y. Chen L. Han H. Xiong B. Zhong R. Jiang Y. et al. (2022). Taxifolin increased semen quality of duroc boars by improving gut microbes and blood metabolites. Front. Microbiol. 13, 1020628. doi: 10.3389/fmicb.2022.1020628
Zhou B. Yuan Y. Zhang S. Guo C. Li X. Li G. et al. (2020). Intestinal flora and disease mutually shape the regional immune system in the intestinal tract. Front. Immunol. 11, 575. doi: 10.3389/fimmu.2020.00575
