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Exploring the association between microbiota and behaviour in suckling piglets.

ABSTRACT: It is increasingly recognised that the microbes residing in the gastrointestinal tract can influence brain physiology and behaviour, via the microbiota-gut-brain axis. Here, we made a first explorative evaluation at the association between the gut microbiota and behaviour in suckling piglets. 16S microbiota profiling information was obtained from two independent replicate experiments at 2 and 4 weeks of age. Piglets underwent a backtest to assess their personality or coping style at 2 weeks of age, and were subjected to a combined open field and novel object test at 3.5 weeks of age, recording anxiety-related and exploratory behaviour. The number of squeals vocalised during the open field test was associated with microbial groups such as Coprococcus 3 and CAG-873, whereas in the novel object test, explorative behaviour was significantly associated with microbial genera like Atopobium and Prevotella. Overall, this study explores the microbiota-behavioural relation by employing multivariate analysis and exemplifies the importance of individualised analyses when evaluating such relationships.

SUBMITTER: Choudhury R

PROVIDER: S-EPMC9296644 | biostudies-literature | 2022 Jul

REPOSITORIES: biostudies-literature

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Exploring the association between microbiota and behaviour in suckling piglets.

Choudhury R R Middelkoop A A Bolhuis J E JE Kleerebezem M M

Scientific reports 20220719 1

It is increasingly recognised that the microbes residing in the gastrointestinal tract can influence brain physiology and behaviour, via the microbiota-gut-brain axis. Here, we made a first explorative evaluation at the association between the gut microbiota and behaviour in suckling piglets. 16S microbiota profiling information was obtained from two independent replicate experiments at 2 and 4 weeks of age. Piglets underwent a backtest to assess their personality or coping style at 2 weeks of a ...[more]

PMID: 35854042

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Project description:Emerging knowledge shows the importance of early life events in programming the intestinal mucosal immune system and development of the intestinal barrier function. These processes depend heavily on close interactions between gut microbiota and host cells in the intestinal mucosa. In turn, development of the intestinal microbiota is largely dependent on available nutrients and substrates required for the specific microbial community structures to expand. It is currently not known what the specificities are of intestinal microbial community structures in relation to the programming of the intestinal mucosal immune system and development of the intestinal barrier function. The objective of the present study was to investigate the effect of a nutritional intervention on intestinal development of suckling piglets by daily oral administration of fructooligosaccharides (FOS) over a period of 12 days. At the microbiota community level a clear “bifidogenic” effect of the FOS administration was observed in colon digesta at day 14. The former, however, did not translate into significant changes of local gene expression in the colonic mucosa. In the jejunum, significant changes were observed for microbiota composition at day 14, and microbiota diversity at day 25. In addition, significant differentially expressed gene sets in mucosal tissues of jejunum were identified at both days 14 and 25 of age. At the age of 14 days, lower activity of cell cycle-related processes and a higher activity of extracellular matrix processes were observed in jejunal scrapings of piglets supplemented with FOS compared to control piglets. At day 25, lower activity of immune-related processes in jejunal tissue were seen in piglets supplemented with FOS. Histological parameters, villi height and crypt depth, were significantly different at day 25 between the experimental and control group, where piglets supplemented with FOS had higher villi and deeper crypts. We conclude that oral FOS administration during the suckling period of piglets has significant bifidogenic effects on the microbiota in the colon and on gene expression in jejunal mucosa scrapings. We hypothesize that FOS supplementation of suckling piglets results in a higher butyrate production in the colon due to the increase in bifidobacteria and lactobacilli in the hindgut. We further speculate that a higher butyrate production in colonic digesta relates to changes in gene expression in the jejunum by thus far unknown mechanisms.

Project description:Small-scale studies investigating the relationship between pigs' intestinal microbiota and growth performance have generated inconsistent results. We hypothesized that on farms under favorable environmental conditions (e.g., promoting sow nest-building behavior, high colostrum production, low incidence of diseases and minimal use of antimicrobials), the piglet gut microbiota may develop toward a population that promotes growth and reduces pathogenic bacteria. Using 16S rRNA gene amplicon sequencing, we sampled and profiled the fecal microbiota from 170 individual piglets throughout suckling and postweaning periods (in total 670 samples) to track gut microbiota development and its potential association with growth. During the suckling period, the dominant genera were Lactobacillus and Bacteroides, the latter being gradually replaced by Clostridium sensu scricto 1 as piglets aged. The gut microbiota during the nursery stage, not the suckling period, predicted the average daily growth (ADG) of piglets. The relative abundances of SCFA-producing genera, in particular Faecalibacterium, Megasphaera, Mitsuokella, and Subdoligranulum, significantly correlated with high ADG of weaned piglets. In addition, the succession of the gut microbiota in high-ADG piglets occurred faster and stabilized sooner upon weaning, whereas the gut microbiota of low-ADG piglets continued to mature after weaning. Overall, our findings suggest that weaning is the major driver of gut microbiota variation in piglets with different levels of overall growth performance. This calls for further research to verify if promotion of specific gut microbiota, identified here at weaning transition, is beneficial for piglet growth. IMPORTANCE The relationship between pigs' intestinal microbiota and growth performance is of great importance for improving piglets' health and reducing antimicrobial use. We found that gut microbiota variation is significantly associated with growth during weaning and the early nursery period. Importantly, transitions toward a mature gut microbiota enriched with fiber-degrading bacteria mostly complete upon weaning in piglets with better growth. Postponing the weaning age may therefore favor the development of fiber degrading gut bacteria, conferring the necessary capacity to digest and harvest solid postweaning feed. The bacterial taxa associated with piglet growth identified herein hold potential to improve piglet growth and health.

Project description:Emerging knowledge shows the importance of early life events in programming the intestinal mucosal immune system and development of the intestinal barrier function. These processes depend heavily on close interactions between gut microbiota and host cells in the intestinal mucosa. In turn, development of the intestinal microbiota is largely dependent on available nutrients required for the specific microbial community structures to expand. It is currently not known what the specificities are of intestinal microbial community structures in relation to the programming of the intestinal mucosal immune system and development of the intestinal barrier function. The objective of the present study was to investigate the effects of a nutritional intervention on intestinal development of suckling piglets by daily oral administration of fructooligosaccharides (FOS) over a period of 12 d (days 2-14 of age). At the microbiota community level, a clear "bifidogenic" effect of the FOS administration was observed in the colon digesta at day 14. The former, however, did not translate into significant changes of local gene expression in the colonic mucosa. In the jejunum, significant changes were observed for microbiota composition at day 14, and microbiota diversity at day 25. In addition, significant differentially expressed gene sets in mucosal tissues of the jejunum were identified at both days 14 and 25 of age. At the age of 14 d, a lower activity of cell cycle-related processes and a higher activity of extracellular matrix processes were observed in the jejunal mucosa of piglets supplemented with FOS compared with control piglets. At day 25, the lower activity of immune-related processes in jejunal tissue was seen in piglets supplemented with FOS. Villi height and crypt depth in the jejunum were significantly different at day 25 between the experimental and control groups, where piglets supplemented with FOS had greater villi and deeper crypts. We conclude that oral FOS administration during the early suckling period of piglets had significant bifidogenic effects on the microbiota in the colon and on gene expression in the jejunal mucosa by thus far unknown mechanisms.

Dataset Information

Exploring the association between microbiota and behaviour in suckling piglets.

Publications

Exploring the association between microbiota and behaviour in suckling piglets.

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