Intestinal microbiota could transfer host Gut characteristics from pigs to mice

Gut microbiota has been recognized as a strong determinant factor of host physiology, especially its critical role in host gut development [19]. The causal relationship between gut microbiota and host phenotypes has been widely studied via fecal microbiota transplantation. It has been shown that inflammatory bowel disease could be cured by transplanting fecal microbota from healthy human [28]. Previous studies indicated that the gut of individuals and animals with different genotype or phenotype may harbor distinct microbiota [16, 17, 37]. However, there is not enough evidence to indicate the relationship between gut microbiota and gut phenotype features. Here, we demonstrated that different pig breeds exhibit a distinct gut microbial profile. Moreover, we found that transfering porcine microbiota to mice recipients can replicate the gut characteristics of the pig donors.

16S rRNA gene sequencing in donor pigs and recipient mice showed that the fecal microbiota composition at the phylum and genus levels were widely different in TP, YP and RP, and so were the same phenomena in TFM, YFM and RFM. More specifically, lower Firmicutes and higher Bacteroidetes levels were observed in YP and YFM, whereas higher levels of bacteria from Elusimicrobia, Fibrobacteres and Spirochaetes were observed in TP, and a higher level of Spirochaetes was observed in TFM. Studies comparing the gut microbiota between obese and lean animals showed that lower Firmicutes and higher Bacteroidetes levels were associated with lean phenotype [18, 38]. As is known to us, YP is an imported breed and is characterized by high body lean mass, which is consistent with our study. Spirochaetes is capable of degrading polymers, such as xylan, pectin and arabinogalactan, and is found to be positively correlated with the apparent hemicellulose digestibility of pigs [39–41]. Elusimicrobia is the intracellular symbiont of termite gut flagellates, Fibrobacteres is an important phylum of cellulose-degrading bacteria, and both of them are capable of degrading fiber [42, 43]. TP were recognized to be more adaptable to poor dietary conditions than foreign pig breeds [30], and this may be attributed to higher spirochaetes, Fibrobacteres and Elusimicrobia proportion in gut microbiota. In addition, for the genus level, a higher proportion of Prevotella and a lower proportion of Ruminococcus were found in healthy weight adolescents compared with obese humans [44, 45], which is similar to our study, a higher proportion of Prevotella and lower proportion of Ruminococcus were found in YP and YFM. Roseburia and Blautia are major bacteria that produce butyrate and acetic acid respectively [46, 47]. In our study, TP and TFM exhibited increased abundance of Roseburia and Blautia compared with YP and YFM, which is beneficial to gut health. Moreover, Lactobacillus and Parabacteroides are found to cure enteritis [48, 49]. In the present study, TP and TFM had higher proportion of Lactobacillus and Parabacteroides, and this may be attributed to better gut characteristics in TP.

Previous studies indicated that gut communities in the same phenotype individuals were similar to each other [37, 50]. We also found that TP, YP and RP fecal microbiota could be divided into three separate clusters based on PCA through 16S rRNA gene sequencing. Previous studies have shown that human and rat microbiota can be transferred to GF mice with striking preservation of structure and diversity [51, 52], which was consistent with our study, recipient mice exhibited a high similarity in bacterial community structure with their corresponding pig donors. From the above, gut composition differs between TP, YP and RP, and the mice recipients share high similarity in the gut microbiota with their pig donors.

Long-term reproductive and environmental isolation may lead to specific profiles of organ development, digestive ability and nutrient deposition existing in different pig breeds during their adaptation and evolution [53, 54]. In the present study, the relative weight of total intestine in Chinese indigenous pig breeds (TP and RP) and their mice recipients (TFM and RFM) was significantly higher than that in YP and YFM, which was in agreement with the previous finding that indicated the lean-type pigs had a lower proportional weight of intestine than indigenous genotypes [55]. But many findings elucidated that pigs with leaner carcasses exhibited higher weights for small intestine and large intestine [54, 56]. An experiment with growth stages has shown that the development changes of relative viscera weight between lean pigs and fatter pigs was dissimilar in different growth stage [57, 58]. Thus, further research is clearly warranted. In this study, the intestine length did not differ between RP and YP, and the results were in accordance with previous findings [57], which indicated that the length of small intestine did not differ between foreign pig breeds and native pig breeds. However, the intestine length was higher in TP and TFM compared with YP and YFM in the current experiment. The differences of gut microbial ecology were observed between pig breeds, and changes in microbiota composition would affect the endogenous intestinotrophic proglucagon-derived peptide (GLP-2) production [38, 59]. It is well-known that IGF-1, EGF, GLP-2, and its receptor (GLP-2R) are important regulators of intestine length [60, 61], and ANG4 is a paneth cell granule protein shaping intestinal angiogenesis [62]. In this study, TP and TFM had highest GLP-2 mRNA expression among the three pig breeds and their mice recipients, and TFM had higher ANG4 mRNA expression compared with YFM, which are associated with higher intestine length in TP and TFM.

Previous reports confirmed that pig breeds produce variation in the structure of the small intestine [57]. In the present study, variations in small intestinal morphology were also observed among pig breeds and their mice recipients. Higher villus height of duodenum and jejunum was observed in TP and TFM compared with YP and RP, YFM and RFM, respectively. This is in accordance with data previously reported, villus surface was larger for Iberian pigs than Landrace?×?Large White pigs at 15 kg of BW [63]. As we know, the CDX2 and AKP are involved in intestinal cell proliferation and differentiation, which could contribute to the structure of the intestine [64, 65]. In our study, we found that TP displayed higher CDX2 mRNA expression in the ileum and AKP activity in the jejunum compared with YP, and TFM exhibited higher CDX2 mRNA expression in the ileum compared with YFM. These results are generally consistent with that of Rubio et al. (2010) who reported differences in AKP activity were found among pig breeds [63]. The abovementioned positive regulators must have a potent nutritional effect on the intestine growth and development, and these factors are differently expressed in the digestive tract among pig breeds and their mice recipients to account for differences in phenotype.

Small intestinal nutrient digestion and absorption was also affected by pig breeds. It has been observed that pig genotype (Iberian v. Landrace?×?Large White) exhibited different nitrogen retention and apparent total tract digestibility of nitrogen, energy and organic matter [57]. In a study of changes in small intestinal nutrient transport in Meishan pigs and Yorkshire pigs showed that different glucose, arginine, glutamine and threonine transportation in the small intestine were observed in the two pig breeds [53]. The ratio of bacteroidetes and firmicutes bacterial groups in the gut was increased in lean-type pigs which exhibited greater ability to absorb nutrients [66]. Consistent with previous work [63], which observed that Landrace?×?Large White pigs had higher activities of lactase, sucrase and maltase than Iberian pigs in the small intestine, our current study showed YP and YFM had elevated jejunal sucrase and maltase activities, which may have resulted from its higher ratio of bacteroidetes and firmicutes bacterial groups. Meanwhile, TP had higher jejunal amylase, and trypsin than YP or RP, which is generally consistent with the previous study of two pig breeds, total activities of lipase, trypsin and amylase at 49 d of age were 2.0, 1.5 and 5.0 fold higher, respectively, in Alentejano piglets than Large White piglets [67]. In our study, TP and TFM had higher jejunal ?-GT and relative SGLT1 mRNA expression, suggesting the differences of absorptive enzymes and transport carriers possibly affect nutrient digestion and absorption in different pig breeds. In addition, YP and YFM had highest MDA concentration in the jejunum among the three pig genotypes and their mice recipients in this study, and there is currently no available information on the difference in intestinal antioxidant capacity among pig breeds, and thus no comparisons could be made with other studies. Nevertheless, there have been some studies regarding meat antioxidant capacity among pig breeds, which exhibited differences of catalase and SOD in muscle among Pietrain, Landrace, Large-White, lberian, and lberian-Duroc [68]. Taken together, the digestion and absorption function in the three pig genotypes are distinct, which is accompanied by different digestive and absorptive enzymes activities, transport carriers abundance and antioxidant capacity in the intestine.

Pig breeds also differ for their intestinal barrier. Previous study has shown that Yorkshire pigs responded to LPS by increasing resistance (decreasing conductance), whereas resistance in Meishan intestine did not change with LPS, which indicated that intestinal barrier function in traditional pig breed was better than Yorkshire pigs [53]. Innate defenses, such as epithelial production of a-defensins and mucins, help prevent bacteria from crossing the mucosal barrier [69]. ZO-1 is a junctional adaptor protein that interacts with multiple other junctional components, including the transmembrane proteins of the claudin, occludin and JAM families, which is important for intestinal integrity and barrier function [70]. Furthermore, the direct host-commensal interaction is dictated by the presence of the intestinal mucus layer, and the expression and activation of mucin and ZO-1 are induced by exposing to a developing gut microbial community or their structural components, as well as the presence of products of bacterial metabolism [1]. In our study, the relative ZO-1 mRNA expression of the ileum in TP and TFM was higher than that in YP and YFM, and RP and RFM had the highest relative MUC2 mRNA expression in the duodenum, suggesting native pig breeds (TP and RP) had better gut barrier function than foreign pig breeds (YP), which verified their stronger adaptability and disease resistance. As mentioned above, the differences in intestine characteristics including intestinal development and gut barrier among pig breeds could transmit to their recipients by fecal microbiota transplantation, and the intestinal microorganisms are essential for intestine development of mammals.

Our study showed that the microbiota affected gut characteristics through their impacts on epithelial renewal rate, morphology, nutrient digestion and absorption, and the intestinal barrier. Thus, while bacteria in the gut are highly variable, the influence of the microbiota in the intestine has far-reaching effects on host physiology. Short chain fatty acids (SCFA) were generated by bacterial fermentation of dietary polysaccharides, and it significantly affects energy metabolism, intestine morphology and immune function of the host via activation of its receptor GPR41 and GPR43 [71, 72]. Moreover, gut microbiota play a key role in determining bile acid (BA) profiles and subsequent effects on host gene expression [73]. BA was reported to differentially activate BA receptors, which function as systemic signaling molecules to regulate host metabolism [74]. Gut microbiota affect pig characteristics and transfer these phenotypes to recipient mice via aforementioned mechanisms in the current study. This study provides new approaches to intervene in animal production and health.