Yak and Tibetan sheep thrive under a co-grazing system on the QTP and/or are fed with the same materials; this offers an excellent opportunity to compare the gut microbiota in different host species which share a similar diet. In addition, the grazing systems on the QTP undergo seasonal diets changes in terms of pasture location and forage composition, especially between winter and summer. This presents a good natural “treatment” which helps vary the diets of the yak and Tibetan sheep populations. In the current study, based on a more substantial sample size than the previous study1, we found that diet and environment (represented by seasons winter and summer) superseded host genetics to the family level. That is to say that the gut microbiota of the two animal species showed convergent adaptation to high altitude and harsh environment in QTP, but this convergence had seasonal diets characteristics. These findings may provide a cautionary note for ongoing efforts to link host genetics to gut microbiota composition and function and would provide some food for thought in the breeding of these two livestock groups.
The mammalian gut microbiota is acquired from the environment starting at birth, and its assembly and composition is largely shaped by factors such as age, diet, lifestyle, hygiene, and disease state. Researchers subconsciously believe that host species play a greater role than environmental factors when it comes to shaping gut microbiota, especially when there is a large taxonomical difference between the host species. So far, the vast majority of research have focused on the ruminal ecosystem because the rumen is primary site of feed fermentation15,16,17. It is rare to find studies that directly compare the gut microbiota of different species. However, evidence showed that energetically-important microbial products, including VFA (10–13% of total GIT VFA) are produced in the ruminant distal gut3. Hence, it is important to study the composition of distal gut microbiota of ruminants.
In this study, at the phylum level, the gut microbiota composition in both groups of livestock was dominated by Bacteroidetes and Firmicutes, which was in agreement with previous reports concerning the yak18. At the same time our result consistently with other study in dairy cows that two dominated phyla Bacteroidetes and Firmicutes found in fecal samples in different seasons were abundant19,20. Firmicutes and Bacteroidetes are responsible for digestion of carbohydrates and proteins, Members of Bacteroidetes having extremely stronger ability to degrade crystalline cellulose. The previous report showed that intestinal microbiome plays an important role in digestion and absorption of the food, and maintaining animals’ health21,22. Intestinal tracts of the ruminants are rich in symbiotic bacteria that helps the body digest plant fibers23,24. Glycans are processed by the distal gut microbiota, generating biologically significant short-chain fatty acids (SCFAs, predominantly acetate, butyrate, and propionate), which serve as the principal energy source for colonocytes25. Fibers may be involved in the regulation of food intake and energy balance via the SCFA-mediated modulation of the secretion of gut hormones26. The higher abundance of Firmicutes and Bacteroidetes in yak may be associated with high-energy consumption at high altitude18.
It is worth noting that, at the family level, the dominant genera (Unclassified Ruminococcaceae, Bacteroidaceae, Unclassified BS11, Unclassified Prevotellaceae, Unclassified Christensenellaceae, CF231, Unclassified Mogibacteriaceae and Unclassified Paraprevotellaceae) in the intestines of yak and Tibetan sheep were more greatly influenced by season than genetics (Fig. 5). This has not previously been accurately identified, which may be because there have been few studies into the gut microbial communities of the yak and Tibetan sheep in QTP. So, to improve their husbandry, it is important in the future to study their microbiota profiles using more precise methods such as 16S full-length sequencing or metagenomic sequencing. Ruminococcaceae is a family of autochthonous and benignspecies that primarily inhabit in the caecum and the colon27. It is known that Ruminococcaceae are common in the rumen and hindgut of ruminants, capable of degrading cellulose and starch28. As a member of short chain fatty acid (SCFA) producers, Ruminococcaceae is considered to be the most important fiber and polysaccharides-degrading bacterium in the intestine of herbivores, and produces large amounts of cellulolytic enzymes, including exoglucanases, endoglucanase, glucosidases and hemicellulase29. The microbial community of Yak and Sheep is greatly influenced by alterations in dietary nutrition, Bacteroidaceae have the ability to degrade complex molecules (polysaccharides, proteins) in the intestine18, which can promote the Yak utilizes grasses as its major source of nutrition, due to shortage of grain and other nutrients. Prevotellaceae is responsible for hemicellulose, pectin and high carbohydrate food digestion30. The higher abundance of these microbes may contribute to gaining more energy, and play vital roles in the process of adaption of the hosts to the harsh natural environment15. Bacteroidales BS11 gut group are specialized to active hemicellulose monomeric sugars (e.g., xylose, fucose, mannose and rhamnose) fermentation and short-chain fatty acid (e.g., acetate and butyrate) production that are vital for ruminant energy31. The Bacteroidales BS11 was positively correlated with some metabolites that are involved in amino acid metabolism and biosynthesis, as well as the metabolism of energy sources, such as starch, sucrose, and galactose32.
At the genus level, 5-7N15 was most abundant in winter in both animals, on the contrary, the Provotella was predominate. Here, our results indicated that seasonal diets change superseded variations derived from genetic differences between the host species, even though the yak and Tibetan sheep are very different, both taxonomically and in terms of body size. In summer, the forage grass on the Qinghai-Tibet Plateau is dominated by Agropyron cristatum, Elymus nutans, Festuca ovina, Kobresia humilis, Poa pratensis, Stipa aliena, Kobresia pygmaea, Oxytropis biflora, Saussurea hieracioides, Astragalus arnoldii Hemsl. In winter, the main forage was Brachypodium sylvaticum. Carex crebra, Trisetum spicatum and Bupleurum smithii. Stipa has both high palatability and nutritional value, with a high content of crude protein, crude fat, and nitrogen- free extract, and low levels of crude fiber33. The levels of crude protein, crude fat, and nitrogen-free extracts of Brachypodium sylvaticum. Carex crebra, Trisetum spicatum and Bupleurum smithii were lower than that of Stipa, whereas the content of crude fiber was higher than that of Stipa34. Crude protein is the main nutrient of herbage. Crude fat and nitrogen-free extracts provide heat and energy33.
Lopes et al. reported that some OTUs known to be functionally relevant for fiber degradation and host development were shared across the entire gastrointestinal tract and present within the feces35. Microbial diversity increases in the distal segments of the gastrointestinal tract. Microbial fermentation appears to be reestablished in the large intestine, with the proportion of acetate, propionate and butyrate being similar to the rumen.
Several explanations for this phenomenon are possible. Firstly, both the yak and Tibetan sheep are ruminants. In herbivores, the gut microbiota is dominated by Firmicutes and Bacteroides, the functions of which are related to cellulose digestion36. Therefore, ruminant microbes could possibly be more similar across species than gut microbes from elsewhere.
Secondly, the yaks and Tibetan sheep in our study co-grazed from birth to death. As such, the initial gut microbiota source, responsible for populating the remainder of the gut in the months and years after the initial seeding at birth, would necessarily come from the same environment. It has been established that early life events are critical for gut microbiota development and for shaping the adult microbiota. Lifestyle and diet will further influence the composition and function of the gut microbiota. In our study, the investigated animals shared a very similar lifestyle and obtained their diets from the same source. The results revealed that sheep and yaks presented almost identical gut microbiota compositions in the winter, but by the date of collection of the summer samples they were quite different. The reason for this could be that during summer and summer there is pronounced pastoral grass growth, giving the animals more variety and choice in their diets; it is known, after all, that sheep have different diet preferences to yaks37. However, during the winter, the animals have no option but to eat the same food in order to survive until winter.
Thirdly, there could be a convergent evolution of gut microbiomes in yaks and Tibetan sheep due to the extremely harsh environment in high-altitude regions1,38. When compared with their low-altitude relatives, cattle (Bos taurus) and ordinary sheep (Ovis aries), metagenomic analyses revealed significant enrichment in rumen microbial genes involving volatile fatty acid-yielding pathways in yaks and Tibetan sheep, whereas methanogenesis pathways were enriched in the cattle metagenome. Analyses of RNA transcriptomes revealed significant upregulation in 36 genes associated with volatile fatty acid transport and absorption in the ruminal epithelium of yaks and Tibetan sheep. This suggests that, aside from host genetics, long-term exposure to harsh environments has allowed the gut microbiome to adapt in order to boost health and survival. In other words, although yaks and Tibetan sheep are very different genetically, their gut microbiota could be similar due to the selection pressures of the high altitude at which they live. Meanwhile, from our data based on functional gene composition (Fig. S3), it is also worth noting that there were no groups clearly distinguished from one another, although the PERMANOVA results indicated both a host and season effect, with the interaction between them being statistically significant. Though factors such as environment and diet (represented by seasons) can trump host genetics, we could not ignore the interplay of these factors as gut microbes are a very complex community.
Winter is the harshest period for the survival of yak and Tibetan sheep. To maintain the survival, it’s best to feed the animals with a high protein content. Furthermore, to get more detailed data in different seasons and various dietary habits of yak and sheep, more study should be assessed about intestinal microbiota by collecting feces.
Source: Ecology - nature.com