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BACKGROUND

Heat stress (HS) commonly occurring in summer has gradually become a factor threatening the reproductive performance of male dairy goats by reducing their fecundity. Despite the melatonin is applied to relieve HS, it is still unclear whether melatonin protects against reproductive damage induced by HS in dairy goats and how it works. The purpose of the present study is to evaluate the role of melatonin in alleviating HS-induced spermatogenesis dysfunction in male dairy goats and further explore its mechanism.

RESULTS

HS impaired spermatogenesis, sperm formation in the testes, and sperm maturation in the epididymis of dairy goats, resulting in decreased sperm quality. Melatonin rescued the decrease of sperm quality induced by HS via decreasing inflammatory and oxidative stress levels in testicular tissue and enhancing intercellular barrier function within the testes. Amplicon-based microbiota analysis revealed that despite gut microbiota differences between melatonin-treated dairy goats and NC dairy goats to some extent, melatonin administration tends to return the gut microbiota of male dairy goats under HS to the levels of natural control dairy goats. To explore whether the protective role of melatonin in sperm quality is mediated by regulating gut microbiota, fecal microbiota of HS dairy goats with or without melatonin treatment were transferred to HS mice, respectively. We found HS mice that had received fecal bacteria of HS dairy goats experienced serious testicular injury and dyszoospermia, while this phenomenon was ameliorated in HS mice that had received fecal bacteria of dairy goats treated with melatonin, indicating melatonin alleviates HS-induced spermatogenic damage in a microbiota dependent manner. We further found that the testicular tissue of both HS dairy goats and mice transplanted with HS dairy goat feces produced large amounts of arachidonic acid (AA)-related metabolites, which were closely associated with semen quality. Consistently, supplementation with AA has been shown to elevate the levels of inflammation and oxidative stress in the testicular tissue of mice, disrupting intercellular connections and ultimately leading to spermatogenic disorders.

CONCLUSION

This study has revealed that melatonin can effectively alleviate spermatogenic disorders in dairy goats caused by HS. This beneficial effect was primarily achieved through the modulation of gut microbiota, which subsequently inhibited the excessive synthesis of AA in testicular tissue. These discoveries are of great significance for preventing or improving the decline in male livestock reproductive performance caused by HS, enhancing the reproductive efficiency of elite male breeds, and ultimately improving the production efficiency of animal husbandry. Video Abstract.

BACKGROUND

RESULTS

CONCLUSION

背景

夏季经常发生的热应激（HS）逐渐成为威胁雄性奶山羊繁殖性能的因素，降低了它们的繁殖力。尽管褪黑素被应用于缓解 HS，但褪黑素是否能保护奶山羊免受 HS 引起的生殖损伤以及如何发挥作用仍不清楚。本研究旨在评估褪黑素在缓解雄性奶山羊 HS 引起的生殖功能障碍中的作用，并进一步探讨其机制。

结果

HS 损害了奶山羊的精子发生、睾丸内精子形成和附睾内精子成熟，导致精子质量下降。褪黑素通过降低睾丸组织中的炎症和氧化应激水平以及增强睾丸内细胞间屏障功能，挽救了 HS 引起的精子质量下降。基于扩增子的微生物组分析显示，尽管褪黑素处理的奶山羊和 NC 奶山羊的肠道微生物组在某种程度上存在差异，但褪黑素给药倾向于使 HS 下的雄性奶山羊的肠道微生物组恢复到自然对照奶山羊的水平。为了探讨褪黑素对精子质量的保护作用是否通过调节肠道微生物组介导，分别将 HS 奶山羊的粪便微生物组用或不用褪黑素处理后转移到 HS 小鼠中。我们发现，接受 HS 奶山羊粪便细菌的 HS 小鼠经历了严重的睾丸损伤和精子异常，而接受褪黑素处理的奶山羊粪便细菌的 HS 小鼠中这种现象得到了改善，表明褪黑素以依赖微生物组的方式缓解 HS 引起的生精损伤。我们进一步发现，接受 HS 奶山羊粪便移植的 HS 奶山羊和小鼠的睾丸组织产生了大量与花生四烯酸（AA）相关的代谢物，这与精液质量密切相关。一致地，AA 的补充已被证明会增加睾丸组织中的炎症和氧化应激水平，破坏细胞间连接，最终导致生精障碍。