Differential Effects of Breed and Nursing on Early-Life Colonic Microbiota and Immune Status as Revealed in a Cross-Fostering Piglet Model

Abstract

Nursing mother and breed can differently regulate early-life microbiota succession in pigs. However, it remains unclear whether they affect gastrointestinal microbiota and immune status, which are critical for early-life gut health. Here, an interspecific cross-fostering piglet model was employed by fostering neonatal Yorkshire and Meishan piglets to the same or another breed of sows. Jejunal and colonic microbiotas and mucosal immune parameters were analyzed at postnatal days 14 (preweaning) and 49 (postweaning). Nursing mother affected 10 genera in the colon and 3 minor genera in the jejunum. At day 14, Meishan sow-nursed piglets had lower Streptococcus suis and higher Cloacibacillus counts in the colonic digesta and larger amounts of interleukin 10 and Foxp3-positive cells in the colonic mucosa than did Yorkshire sow-nursed piglets. At day 49, nursing mother had no significant effects on cytokine expression. Breed effects were observed; Meishan piglets had lower relative abundances of Prevotella and lower gene expression of tumor necrosis factor alpha (TNF-α) than those of Yorkshire piglets at days 14 and 49. Collectively, nursing mother mainly affected preweaning colonic microbiota and immune status, while breed effects persisted after weaning. Piglets nursed by Meishan sows had different microbiota compositions and inflammatory cytokine profiles in the colon compared with those of piglets nursed by Yorkshire sows. These results highlight the different role of nursing mother and breed in affecting early gut microenvironment. IMPORTANCE Early-life gut microbiota and immune status are pivotal for postnatal growth. By using an interspecific cross-fostering piglet model, we find that change in nursing mother transiently reshapes preweaning colon microbiota and immune status, while breed shows persistent effects both pre- and postweaning. Piglets nursed by Meishan sows had lower Streptococcus suis counts and higher anti-inflammatory cytokine expression. These results highlight the significance of nursing mother in regulating early-life gut health.

Lactic Acid Bacteria: Variability Due to Different Pork Breeds, Breeding Systems and Fermented Sausage Production Technology

“…This is a gap that deserves to be investigated, because they could have direct and undirect effects on the microbial ecology of meat products. In fact, several studies showed the relevant presence of species belonging to the genus Lactobacillus in both gut and reproductive tract microbiota of pigs [36][37][38] and demonstrated that breed affects colonic microbiota and immune status since postnatal period (14-49 days) [36,39]. A possible link between the gut microbiota and feed efficiency in pigs was demonstrated by Tan et al [38], who discovered that, in Landrace pigs, the high-feed conversion rate pigs had a greater abundance of Lactobacillus and Streptococcus than the low-feed conversion rate pigs, having an evident repercussion on pork meat quality [40].…”

Early Inoculation of Microbial Suspension in Suckling Piglets Affects the Transmission of Maternal Microbiota and the Associated Antibiotic Resistance Genes

“…The age at which the piglets are susceptible to their surrounding microbial communities is still unknown, but the pre-weaning period seems to be the most well-adapted: (a) co-housed piglets suddenly develop very similar communities at around 2–3 weeks of age [ 14 ]; (b) feeding yeast to piglets before weaning impacts the average daily weight gain of the piglets, whereas feeding yeast after weaning does not [ 43 ]; (c) feeding a complex community to piglets between 10 and 18 days of age changed the microbial community in a way that increased robustness when the piglets are submitted to an early weaning at 21 days [ 40 ]; and (d) cross-fostering an obese typical Chinese piglet breed and a lean Western breed demonstrated the impact of the nursing mother on the piglets’ microbiota and interleukin 10 [ 44 ]. In other species, the microbial environment in early life is also more important than the microbial imprint at birth, as revealed by the cross-adoption of 1-day-old rabbits [ 13 ].…”

Baicalin-Copper Complex Modulates Gut Microbiota, Inflammatory Responses, and Hormone Secretion in DON-Challenged Piglets

“…Rarefaction curves, and rank abundance curves were drawn using software R (Version 2.15.3) [ 60 ]. For beta-diversity analysis, principal coordinate analysis (PCoA) [ 61 ], principal component analysis (PCA) [ 62 ], nonmetric multidimensional scaling (NMDS) [ 63 ], and unweighted pair group method with arithmetic mean (UPGMA) were performed using QIIME (Version 1.9.1) and R (Version 2.15.3) [ 64 , 65 ]. The bacterial differences between groups were assessed using LEfSe analysis (LDA score = 3.5).…”