Seasonal dynamics of rumen anaerobic fungi in grazing yak (Bos grunniens) and cattle (Bos taurus) driven by seasonal variation of forage nutrition

Background: Anaerobic fungi (AF), an early diverging lineage of the zoosporic fungi Neocallimastigomycota, inhabit in the gut of herbivores where they play an essential role in feed conversion in light of their potent fiber degrading enzymes and invasive growth. Previous studies showed that yak houses a unique rumen microbiome with strong fiber-degrading potential which has evolved during long-term natural selection and evolution. However, the interspecific differences and associated driving forces to maintain host-microbe interactions leading to seasonal dynamics of rumen AF communities between yak and cattle grazing throughout the year under the same natural habitat on the Qinghai-Tibet Plateau (QTP) are not clear.Result: Following the natural grazing system on the QTP, the monthly mean temperatures, forage nutrients, rumen microbial and host blood metabolism changed along grazing seasons. Under such conditions, the rumen microbial metabolism of yak was significantly higher than that of cattle. Grazing season, forage quality and host genetic background had important effects on the seasonal dynamics of rumen AF communities, where the abundance and diversity of rumen AF in cold season were significantly higher than that in warm season. We identified 12 rumen anaerobic fungi genera, among which Caecomyces, Cyllamyces and Orpinomyces were predominant in the rumen of both yak and cattle. LEfSe and random forest analysis showed that Feramyces and Tahromyces were important seasonal indicators in yak rumen. Feramyces was associated with a wide substrate utilization pattern, indicating that yak has evolved a unique rumen microecosystem with strong fiber-degrading ability to adapt to the extreme natural environments. We further found that environmental selection and dispersal limitation were the dominant factors affecting ruminal AF assemblies in yak and cattle during cold season, while the assemblies were significantly affected by the environmental selection during warm season. Based on the Mantel test and the structural equation model revealed that forage physico-chemical properties including dry matter, neutral detergent fiber and hemicellulose contentment were the key factors driving the seasonal variations of rumen AF communities, confirming forage lignocellulose to be important in determining seasonal rumen AF communities.Conclusion: This study realized that forage nutritional quality and host genetic background are important factors affecting the seasonal dynamics and interspecific differences of rumen AF communities in yak and cattle, but forage lignocellulose is the key driving factor for the seasonal dynamics of rumen AF communities. Our findings provided new insights into seasonal changes and diet-microbiota linkages during the adaptation of yak and cattle to high altitudes.