Effects of microbiota–testis interactions on the reproductive health of male ruminants: A review
Cheng Pan
School of Life Sciences and Engineering, Southwest University of Science and Technology, Mianyang, China
Search for more papers by this authorYangzong Zhaxi
Institute of Animal Science, Xizang Academy of Agricultural and Animal Husbandry Science, Lhasa, China
Key Laboratory of Animal Genetics and Breeding on Xizang Plateau, Ministry of Agriculture and Rural Affairs, Lhasa, China
Search for more papers by this authorHaiyan Li
School of Life Sciences and Engineering, Southwest University of Science and Technology, Mianyang, China
Search for more papers by this authorFeng Guan
School of Life Sciences, China Jiliang University, Hangzhou, China
Search for more papers by this authorJunru Pan
School of Life Sciences and Engineering, Southwest University of Science and Technology, Mianyang, China
Search for more papers by this authorDa Wa
Institute of Animal Science, Xizang Academy of Agricultural and Animal Husbandry Science, Lhasa, China
Search for more papers by this authorCorresponding Author
Tianzeng Song
Institute of Animal Science, Xizang Academy of Agricultural and Animal Husbandry Science, Lhasa, China
Key Laboratory of Animal Genetics and Breeding on Xizang Plateau, Ministry of Agriculture and Rural Affairs, Lhasa, China
Correspondence
Tianzeng Song, Institute of Animal Science, Xizang Academy of Agricultural and Animal Husbandry Science, Lhasa, Xizang 850009, China.
Email: [email protected]
Wangsheng Zhao, School of Life Sciences and Engineering, Southwest University of Science and Technology, Mianyang, Sichuan 621000, China.
Email: [email protected]
Search for more papers by this authorCorresponding Author
Wangsheng Zhao
School of Life Sciences and Engineering, Southwest University of Science and Technology, Mianyang, China
Correspondence
Tianzeng Song, Institute of Animal Science, Xizang Academy of Agricultural and Animal Husbandry Science, Lhasa, Xizang 850009, China.
Email: [email protected]
Wangsheng Zhao, School of Life Sciences and Engineering, Southwest University of Science and Technology, Mianyang, Sichuan 621000, China.
Email: [email protected]
Search for more papers by this authorCheng Pan
School of Life Sciences and Engineering, Southwest University of Science and Technology, Mianyang, China
Search for more papers by this authorYangzong Zhaxi
Institute of Animal Science, Xizang Academy of Agricultural and Animal Husbandry Science, Lhasa, China
Key Laboratory of Animal Genetics and Breeding on Xizang Plateau, Ministry of Agriculture and Rural Affairs, Lhasa, China
Search for more papers by this authorHaiyan Li
School of Life Sciences and Engineering, Southwest University of Science and Technology, Mianyang, China
Search for more papers by this authorFeng Guan
School of Life Sciences, China Jiliang University, Hangzhou, China
Search for more papers by this authorJunru Pan
School of Life Sciences and Engineering, Southwest University of Science and Technology, Mianyang, China
Search for more papers by this authorDa Wa
Institute of Animal Science, Xizang Academy of Agricultural and Animal Husbandry Science, Lhasa, China
Search for more papers by this authorCorresponding Author
Tianzeng Song
Institute of Animal Science, Xizang Academy of Agricultural and Animal Husbandry Science, Lhasa, China
Key Laboratory of Animal Genetics and Breeding on Xizang Plateau, Ministry of Agriculture and Rural Affairs, Lhasa, China
Correspondence
Tianzeng Song, Institute of Animal Science, Xizang Academy of Agricultural and Animal Husbandry Science, Lhasa, Xizang 850009, China.
Email: [email protected]
Wangsheng Zhao, School of Life Sciences and Engineering, Southwest University of Science and Technology, Mianyang, Sichuan 621000, China.
Email: [email protected]
Search for more papers by this authorCorresponding Author
Wangsheng Zhao
School of Life Sciences and Engineering, Southwest University of Science and Technology, Mianyang, China
Correspondence
Tianzeng Song, Institute of Animal Science, Xizang Academy of Agricultural and Animal Husbandry Science, Lhasa, Xizang 850009, China.
Email: [email protected]
Wangsheng Zhao, School of Life Sciences and Engineering, Southwest University of Science and Technology, Mianyang, Sichuan 621000, China.
Email: [email protected]
Search for more papers by this authorAbstract
Ruminants are one of the world's economically important species, and their reproductive health is critical to the economic development of the livestock industry. In recent years, research on the relationship between microbiota and reproductive health has received much attention. Microbiota disruption affects the developmental health of the testes and epididymis, the male reproductive organs of the host, which in turn is related to sperm quality. Maintaining a stable microbiota protects the host from pathogens and increases breeding performance, which in turn promotes the economic development of animal husbandry. In addition, the effects and mechanisms of microbiota on reproduction were further explored. These findings support new approaches to improving and managing reproductive health in ruminants through the microbiota and facilitate further systematic exploration of microbiota-mediated reproductive impacts.
CONFLICT OF INTEREST STATEMENT
None of the authors have any conflict of interest to declare.
Open Research
DATA AVAILABILITY STATEMENT
All data in this study are available upon request by contact with the corresponding author.
REFERENCES
- Adamczewska, D., Słowikowska-Hilczer, J., & Walczak-Jędrzejowska, R. (2022). The fate of Leydig cells in men with Spermatogenic failure. Life (Basel), 12(4), 570.
- Alfano, M., Pederzoli, F., Locatelli, I., Ippolito, S., Longhi, E., Zerbi, P., Ferrari, M., Brendolan, A., Montorsi, F., Drago, D., Andolfo, A., Nebuloni, M., & Salonia, A. (2019). Impaired testicular signaling of vitamin a and vitamin K contributes to the aberrant composition of the extracellular matrix in idiopathic germ cell aplasia. Fertility and Sterility, 111(4), 687–698.
- Amann, R. P. (1989). Structure and function of the normal testis and epididymis[J]. Journal of the American College of Toxicology, 8(3), 457–471.
10.3109/10915818909014532 Google Scholar
- Ashonibare, V. J., Akorede, B. A., Ashonibare, P. J., Akhigbe, T. M., & Akhigbe, R. E. (2024). Gut microbiota-gonadal axis: The impact of gut microbiota on reproductive functions[J]. Frontiers in Immunology, 15, 1346035.
- Avidor-Reiss, T., Khire, A., Fishman, E. L., & Jo, K. H. (2015). Atypical centrioles during sexual reproduction. Frontiers in Cell and Development Biology, 3, 21.
- Baker, J. M., Al-Nakkash, L., & Herbst-Kralovetz, M. M. (2017). Estrogen-gut microbiome axis: Physiological and clinical implications. Maturitas, 103, 45–53.
- Barbagallo, F., Condorelli, R. A., Mongioì, L. M., Cannarella, R., Aversa, A., Calogero, A. E., & la Vignera, S. (2020). Effects of bisphenols on testicular steroidogenesis[J]. Frontiers in Endocrinology, 11, 523987.
10.3389/fendo.2020.00373 Google Scholar
- Bennison, C., Hemmings, N., Slate, J., & Birkhead, T. (2015). Long sperm fertilize more eggs in a bird. Proceedings of the Biological Sciences, 282(1799), 20141897.
- Bešlo, D., Došlić, G., Agić, D., Rastija, V., Šperanda, M., Gantner, V., & Lučić, B. (2022). Polyphenols in ruminant nutrition and their effects on reproduction. Antioxidants (Basel), 11(5), 970.
- Bhasin, S., Travison, T. G., Pencina, K. M., O'Leary, M., Cunningham, G. R., Lincoff, A. M., Nissen, S. E., Lucia, M. S., Preston, M. A., Khera, M., Khan, N., Snabes, M. C., Li, X., Tangen, C. M., Buhr, K. A., & Thompson, I. M., Jr. (2023). Prostate safety events during testosterone replacement therapy in men with hypogonadism: A randomized clinical trial. JAMA Network Open, 6(12), e2348692.
- Bo, T., Liu, H., Liu, M., Liu, Q., Li, Q., Cong, Y., Luo, Y., Wang, Y., Yu, B., Pu, T., Wang, L., Wang, Z., & Wang, D. (2023). Mechanism of inulin in colic and gut microbiota of captive Asian elephant. Microbiome, 11(1), 148.
- Boe-Hansen, G. B., Fortes, M. R. S., & Satake, N. (2018). Morphological defects, sperm DNA integrity, and protamination of bovine spermatozoa. Andrology, 6(4), 627–633.
- Boguenet, M., Bocca, C., Bouet, P. E., Serri, O., Chupin, S., Tessier, L., Blanchet, O., el Hachem, H., Chao de la Barca, J. M., Reynier, P., & May-Panloup, P. (2020). Metabolomic signature of the seminal plasma in men with severe oligoasthenospermia. Andrology, 8(6), 1859–1866.
- Cai, J., Rimal, B., Jiang, C., Chiang, J. Y. L., & Patterson, A. D. (2022). Bile acid metabolism and signaling, the microbiota, and metabolic disease[J]. Pharmacology & Therapeutics, 237, 108238.
- Chen, P., Li, S., Zheng, L., Wang, Z., He, Y., Liu, K., Li, M., Wang, Y., Shaukat, A., Li, S., Huang, S., & Jian, F. (2024). Effects of radix dichroae extract supplementation on growth performance, oocysts output and gut microbiota in growing lambs with coccidiosis. Veterinary Research Communications, 48(1), 279–290.
- Chen, Q., Deng, T., & Han, D. (2016). Testicular immunoregulation and spermatogenesis. Seminars in Cell & Developmental Biology, 59, 157–165.
- Chen, X., Li, X., Guo, J., Zhang, P., & Zeng, W. (2017). The roles of microRNAs in regulation of mammalian spermatogenesis. Journal of Animal Science and Biotechnology, 8, 35.
- Deng, S. L., Wang, Z. P., Jin, C., Kang, X. L., Batool, A., Zhang, Y., Li, X. Y., Wang, X. X., Chen, S. R., Chang, C. S., Cheng, C. Y., Lian, Z. X., & Liu, Y. X. (2018). Melatonin promotes sheep Leydig cell testosterone secretionin a co-culture with Sertoli cells. Theriogenology, 106, 170–177.
- Ding, N., Zhang, X., Zhang, X. D., Jing, J., Liu, S. S., Mu, Y. P., Peng, L. L., Yan, Y. J., Xiao, G. M., Bi, X. Y., Chen, H., Li, F. H., Yao, B., & Zhao, A. Z. (2020). Impairment of spermatogenesis and sperm motility by the high-fat diet-induced dysbiosis of gut microbes. Gut, 69(9), 1608–1619.
- Elbashir, S., Magdi, Y., Rashed, A., Henkel, R., & Agarwal, A. (2021). Epididymal contribution to male infertility: An overlooked problem[J]. Andrologia, 53(1), e13721.
- Gu, N. H., Zhao, W. L., Wang, G. S., & Sun, F. (2019). Comparative analysis of mammalian sperm ultrastructure reveals relationships between sperm morphology, mitochondrial functions and motility. Reproductive Biology and Endocrinology, 17(1), 66.
- Guo, Q., Cheng, Y., Li, T., Huang, J., Li, J., Zhang, Z., & Qu, Y. (2024). The gut microbiota contributes to the development of LPS-induced Orchitis by disrupting the blood-testosterone barrier in mice[J]. Reproductive Sciences, 1–12.
- Gury-BenAri, M., Thaiss, C. A., Serafini, N., Winter, D. R., Giladi, A., Lara-Astiaso, D., Levy, M., Salame, T. M., Weiner, A., David, E., Shapiro, H., Dori-Bachash, M., Pevsner-Fischer, M., Lorenzo-Vivas, E., Keren-Shaul, H., Paul, F., Harmelin, A., Eberl, G., Itzkovitz, S., … Amit, I. (2016). The Spectrum and regulatory landscape of intestinal innate lymphoid cells are shaped by the microbiome. Cell, 166(5), 1231–1246.
- Huang, W., Cao, Z., Yao, Q., Ji, Q., Zhang, J., & Li, Y. (2020). Mitochondrial damage are involved in aflatoxin B(1)-induced testicular damage and spermatogenesis disorder in mice. The Science of the Total Environment, 701, 135077.
- Hussain, T., Murtaza, G., Kalhoro, D. H., Kalhoro, M. S., Metwally, E., Chughtai, M. I., Mazhar, M. U., & Khan, S. A. (2021). Relationship between gut microbiota and host-metabolism: Emphasis on hormones related to reproductive function. Animal Nutrition, 7(1), 1–10.
- Inhorn, M. C., & Patrizio, P. (2015). Infertility around the globe: New thinking on gender, reproductive technologies and global movements in the 21st century. Human Reproduction Update, 21(4), 411–426.
- Insenser, M., Murri, M., Del Campo, R., Martínez-García, M. Á., Fernández-Durán, E., & Escobar-Morreale, H. F. (2018). Gut microbiota and the polycystic ovary syndrome: Influence of sex, sex hormones, and obesity. The Journal of Clinical Endocrinology and Metabolism, 103(7), 2552–2562.
- Karimi, H., Ranjbar Saraskanroud, M., & Balazadeh Koucheh, F. (2019). Influence of laterality on testis anatomy and histology in Ghezel rams. Veterinary Medicine and Science, 5(2), 151–156.
- Le Blévec, E., Muroňová, J., Ray, P. F., & Arnoult, C. (2020). Paternal epigenetics: Mammalian sperm provide much more than DNA at fertilization. Molecular and Cellular Endocrinology, 518, 110964.
- Lecluze, E., Jégou, B., Rolland, A. D., & Chalmel, F. (2018). New transcriptomic tools to understand testis development and functions. Molecular and Cellular Endocrinology, 468, 47–59.
- Lehti, M. S., & Sironen, A. (2017). Formation and function of sperm tail structures in association with sperm motility defects. Biology of Reproduction, 97(4), 522–536.
- Li, C., Zhang, J., Li, Y., Zhao, X., Liang, H., Li, K., Qu, M., Qiu, Q., & Ouyang, K. (2022). Glutamate supplementation improves growth performance, rumen fermentation, and serum metabolites in heat-stressed Hu sheep. Frontiers in Nutrition, 9, 851386.
- Li, H., Li, N., Lu, Q., Yang, J., Zhao, J., Zhu, Q., Yi, S., Fu, W., Luo, T., Tang, J., Zhang, Y., Yang, G., Liu, Z., Xu, J., Chen, W., & Zhu, J. (2022). Chronic alcohol-induced dysbiosis of the gut microbiota and gut metabolites impairs sperm quality in mice[J]. Frontiers in Microbiology, 13, 1042923.
- Li, T., Wang, H., Ma, K., Wu, Y., Qi, X., Liu, Z., Li, Q., Zhang, Y., & Ma, Y. (2023). Identification and functional characterization of developmental-stage-dependent piRNAs in Tibetan sheep testes. Journal of Animal Science, 101, skad189.
- Li, X., Cheng, W., Shang, H., Wei, H., & Deng, C. (2022). The interplay between androgen and gut microbiota: Is there a microbiota-gut-testis Axis. Reproductive Sciences, 29(6), 1674–1684.
- Li, Z., Shi, J., Lei, Y., Wu, J., Zhang, R., Zhang, X., Jia, L., Wang, Y., Ma, Y., He, P., Ma, Y., Cheng, Q., Zhang, Z., Zhang, K., & Lei, Z. (2022). Castration alters the cecal microbiota and inhibits growth in Holstein cattle. Journal of Animal Science, 100(12), skac367.
- Liang, J., Wu, T., Wang, T., Ma, Y., Li, Y., Zhao, S., Guo, Y., & Liu, B. (2023). Moringa oleifera leaf ethanolic extract benefits cashmere goat semen quality via improving rumen microbiota and metabolome. Frontiers in Veterinary Science, 10, 1049093.
- Lin, L. X., Cao, Q. Q., Zhang, C. D., Xu, T. T., Yue, K., Li, Q., Liu, F., Wang, X., Dong, H. J., Huang, S. C., & Jian, F. C. (2022). Aflatoxin B1 causes oxidative stress and apoptosis in sheep testes associated with disrupting rumen microbiota. Ecotoxicology and Environmental Safety, 232, 113225.
- Lin, Y., Wang, K., Che, L., Fang, Z., Xu, S., Feng, B., Zhuo, Y., Li, J., Wu, C., Zhang, J., Xiong, H., Yu, C., & Wu, D. (2022). The improvement of semen quality by dietary fiber intake is positively related with gut microbiota and SCFA in a boar model[J]. Frontiers in Microbiology, 13, 863315.
- Lindemann, C. B., & Lesich, K. A. (2016). Functional anatomy of the mammalian sperm flagellum. Cytoskeleton (Hoboken), 73(11), 652–669.
- Liu, J. B., Chen, K., Li, Z. F., Wang, Z. Y., & Wang, L. (2022). Glyphosate-induced gut microbiota dysbiosis facilitates male reproductive toxicity in rats. The Science of the Total Environment, 805, 150368.
- Liu, R., Cai, D., Li, X., Liu, B., Chen, J., Jiang, X., Li, H., Li, Z., Teerds, K., Sun, J., Bai, W., & Jin, Y. (2022). Effects of Bisphenol a on reproductive toxicity and gut microbiota dysbiosis in male rats. Ecotoxicology and Environmental Safety, 239, 113623.
- Mahiddine, F. Y., You, I., Park, H., & Kim, M. J. (2023). Management of dog sperm parameters and gut microbiota composition with lactobacillus rhamnosus supplementation. Veterinary Research Communications, 47(3), 1629–1640.
- Marchesi, J. R., Adams, D. H., Fava, F., Hermes, G. D. A., Hirschfield, G. M., Hold, G., Quraishi, M. N., Kinross, J., Smidt, H., Tuohy, K. M., Thomas, L. V., Zoetendal, E. G., & Hart, A. (2016). The gut microbiota and host health: A new clinical frontier. Gut, 65(2), 330–339.
- Mathur, P. P., & D'cruz, S. C. (2011). The effect of environmental contaminants on testicular function[J]. Asian Journal of Andrology, 13(4), 585–591.
- Miller, M. P., Amon, A., & Ünal, E. (2013). Meiosis I: When chromosomes undergo extreme makeover. Current Opinion in Cell Biology, 25(6), 687–696.
- Mocé, M. L., Esteve, I. C., Pérez-Fuentes, S., Gómez, E. A., & Mocé, E. (2022). Microbiota in goat Buck ejaculates differs between breeding and non-breeding seasons. Frontiers in Veterinary Science, 9, 867671.
- Morohoshi, A., Miyata, H., Oyama, Y., Oura, S., Noda, T., & Ikawa, M. (2021). FAM71F1 binds to RAB2A and RAB2B and is essential for acrosome formation and male fertility in mice. Development, 148(21), dev19964.
10.1242/dev.199644 Google Scholar
- Morrison, D. J., & Preston, T. (2016). Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism. Gut Microbes, 7(3), 189–200.
- Negretto, L., Rassi, N., Soares, L. R., Saraiva, A. B. C., Teixeira, M. E. F., Santos, L. D. R., Souza, A. L. L., Jardim, P. C. B. V., Barroso de Souza, W. K. S., & Jardim, T. S. V. (2024). Testosterone deficiency in hypertensive men: Prevalence and associated factors. Arquivos Brasileiros de Cardiologia, 121(3), e20230138.
- Piras, A. R., Menéndez-Blanco, I., Soto-Heras, S., Catalá, M. G., Izquierdo, D., Bogliolo, L., & Paramio, M. T. (2019). Resveratrol supplementation during in vitro maturation improves embryo development of prepubertal goat oocytes selected by brilliant cresyl blue staining. The Journal of Reproduction and Development, 65(2), 113–120.
- Popov, D. V. (2022). Microbiota and reproduction in agricultural mammals. Agricultural Biology, 57(2), 222–236.
- Santacroce, L., Imbimbo, C., Ballini, A., Crocetto, F., Scacco, S., Cantore, S., di Zazzo, E., Colella, M., & Jirillo, E. (2022). Testicular immunity and its connection with the microbiota. Physiological and clinical implications in the light of personalized medicine. Journal of Personalized Medicine, 12(8), 1335.
- Saravanan, G., Praveenkumar, D., Vinothkumar, A., & Achiraman, S. (2022). Evaluation of the fecal microbes in pre-adult, adult and castrated male goats (Capra hircus). Bulletin of Environment, Pharmacology and Life Sciences, 11, 58–63.
- Schroeder, B. O., & Bäckhed, F. (2016). Signals from the gut microbiota to distant organs in physiology and disease. Nature Medicine, 22(10), 1079–1089.
- Scott, H. M., Mason, J. I., & Sharpe, R. M. (2009). Steroidogenesis in the fetal testis and its susceptibility to disruption by exogenous compounds[J]. Endocrine Reviews, 30(7), 883–925.
- Shi, J., Li, Z., Jia, L., Ma, Y., Huang, Y., He, P., Ran, T., Liu, W., Zhang, W., Cheng, Q., Zhang, Z., & Lei, Z. (2024). Castration alters the ileum microbiota of Holstein bulls and promotes beef flavor compounds. BMC Genomics, 25(1), 426.
- Shin, J. H., Park, Y. H., Sim, M., Kim, S. A., Joung, H., & Shin, D. M. (2019). Serum level of sex steroid hormone is associated with diversity and profiles of human gut microbiome. Research in Microbiology, 170(4–5), 192–201.
- Sommer, F., & Bäckhed, F. (2013). The gut microbiota—Masters of host development and physiology. Nature Reviews Microbiology, 11(4), 227–238.
- Šturm, S., Švara, T., Spörndly-Nees, E., Cerkvenik-Flajs, V., Gombač, M., Weber, A. L., & Weber, K. (2021). Seminiferous epithelium cycle staging based on the development of the acrosome in ram testis. Journal of Toxicologic Pathology, 34(4), 331–338.
- Sun, Y., Sun, P., Hu, Y., Shan, L., Geng, Q., Gong, Y., Fan, H., Zhang, T., & Zhou, Y. (2022). Elevated testicular apoptosis is associated with elevated sphingosine driven by gut microbiota in prediabetic sheep. BMC Biology, 20(1), 121.
- Teves, M. E., & Roldan, E. (2022). Sperm bauplan and function and underlying processes of sperm formation and selection. Physiological Reviews, 102(1), 7–60.
- Thaiss, C. A., Zmora, N., Levy, M., & Elinav, E. (2016). The microbiome and innate immunity. Nature, 535(7610), 65–74.
- Valcarce, D. G., Genovés, S., Riesco, M. F., Martorell, P., Herráez, M. P., Ramón, D., & Robles, V. (2017). Probiotic administration improves sperm quality in asthenozoospermic human donors[J]. Beneficial Microbes, 8(2), 193–206.
- Valcarce, D. G., Riesco, M. F., Martínez-Vázquez, J. M., & Robles, V. (2019). Diet supplemented with antioxidant and anti-inflammatory probiotics improves sperm quality after only one spermatogenic cycle in zebrafish model[J]. Nutrients, 11(4), 843.
- Walker, W. H. (2022). Regulation of mammalian spermatogenesis by miRNAs. Seminars in Cell & Developmental Biology, 121, 24–31.
- Wang, M., Ren, C., Wang, P., Cheng, X., Chen, Y., Huang, Y., Chen, J., Sun, Z., Wang, Q., & Zhang, Z. (2023). Microbiome-metabolome reveals the contribution of the gut-testis axis to sperm motility in sheep (Ovis aries). Animals (Basel), 13(6), 996.
- Wang, Y. Y., Lai, T. H., Chen, M. F., Lee, H. L., Kuo, P. L., & Lin, Y. H. (2019). SEPT14 mutations and Teratozoospermia: Genetic effects on sperm head morphology and DNA integrity. Journal of Clinical Medicine, 8(9), 1297.
- Wanjari, U. R., & Gopalakrishnan, A. V. (2024). Blood-testis barrier: A review on regulators in maintaining cell junction integrity between Sertoli cells. Cell and Tissue Research, 396(2), 157–175.
- White, J. C., Highland, M., Kaiser, M., & Clagett-Dame, M. (2000). Vitamin a deficiency results in the dose-dependent acquisition of anterior character and shortening of the caudal hindbrain of the rat embryo. Developmental Biology, 220(2), 263–284.
- Whon, T. W., Kim, H. S., Shin, N. R., Jung, E. S., Tak, E. J., Sung, H., Jung, M. J., Jeong, Y. S., Hyun, D. W., Kim, P. S., Jang, Y. K., Lee, C. H., & Bae, J. W. (2021). Male castration increases adiposity via small intestinal microbial alterations. EMBO Reports, 22(1), e50663.
- Woolley, D. M., Carter, D. A., & Tilly, G. N. (2008). Compliance in the neck structures of the Guinea pig spermatozoon, as indicated by rapid freezing and electron microscopy. Journal of Anatomy, 213(3), 336–341.
- Zeitoun, M., Farahna, M., al-Sobayil, K., & Abdel-Salam, A. (2014). Impact of the aqueous extract of dandelion, probiotic and their synbiotic on male lamb's testicular histopathology relative to semen characteristics. Open Journal of Animal Sciences, 2014, 23–30.
10.4236/ojas.2014.41004 Google Scholar
- Zhang, C., Zhang, W., Zhang, J., Jing, Y., Yang, M., du, L., Gao, F., Gong, H., Chen, L., Li, J., Liu, H., Qin, C., Jia, Y., Qiao, J., Wei, B., Yu, Y., Zhou, H., Liu, Z., Yang, D., & Li, J. (2018). Gut microbiota dysbiosis in male patients with chronic traumatic complete spinal cord injury. Journal of Translational Medicine, 16(1), 353.
- Zhang, K., He, C., Xu, Y., Zhang, C., Li, C., Jing, X., Wang, M., Yang, Y., Suo, L., Kalds, P., Song, J., Wang, X., Brugger, D., Wu, Y., & Chen, Y. (2021). Taxonomic and functional adaption of the gastrointestinal microbiome of goats kept at high altitude (4800 m) under intensive or extensive rearing conditions. FEMS Microbiology Ecology, 97(3), fiab009.
- Zhang, P., Feng, Y., Li, L., Ge, W., Yu, S., Hao, Y., Shen, W., Han, X., Ma, D., Yin, S., Tian, Y., Min, L., Sun, Z., Sun, Q., Zhang, H., & Zhao, Y. (2021). Improvement in sperm quality and spermatogenesis following faecal microbiota transplantation from alginate oligosaccharide dosed mice. Gut, 70(1), 222–225.
- Zhang, T., Sun, P., Geng, Q., Fan, H., Gong, Y., Hu, Y., Shan, L., Sun, Y., Shen, W., & Zhou, Y. (2022). Disrupted spermatogenesis in a metabolic syndrome model: The role of vitamin a metabolism in the gut-testis axis. Gut, 71(1), 78–87.
- Zhao, W., Quansah, E., Yuan, M., Gou, Q., Mengal, K., Li, P., Wu, S., Xu, C., Yi, C., & Cai, X. (2019). Region-specific gene expression in the epididymis of yak[J]. Theriogenology, 139, 132–146.
- Zhao, Y., Zhang, P., Ge, W., Feng, Y., Li, L., Sun, Z., Zhang, H., & Shen, W. (2020). Alginate oligosaccharides improve germ cell development and testicular microenvironment to rescue busulfan disrupted spermatogenesis. Theranostics, 10(7), 3308–3324.
- Zheng, Y., Gao, Q., Li, T., Liu, R., Cheng, Z., Guo, M., Xiao, J., Wu, D., & Zeng, W. (2022). Sertoli cell and spermatogonial development in pigs. Journal of Animal Science and Biotechnology, 13(1), 45.
- Zhou, Y., Wei, Z., Tan, J., Sun, H., Jiang, H., Gao, Y., Zhang, H., & Schroyen, M. (2023). Alginate oligosaccharide extends the service lifespan by improving the sperm metabolome and gut microbiota in an aging Duroc boars model. Frontiers in Cellular and Infection Microbiology, 13, 1308484.
- Zhu, Y., Sun, G., Luosang-Dunzhu, Li, X., Luosang-Zhaxi, Suolang-Zhaxi, Suolang, Ciyang, Cidan-Yangji, Basang-Wangdui, Pan, F., & Peng, Q. (2022). House feeding pattern increased male yak fertility by improving gut microbiota and serum metabolites. Frontiers in Veterinary Science, 9, 989908.
- Zhu, Y., Lu, S., Cidan, Y., Wang, H., Li, K., & Basang, W. (2024). "comparative analysis of intestinal microbiota composition between free-ranged captive yak populations in Nimu County." Frontiers in cellular and infection. Microbiology, 14, 1420389.