Age, introduction of solid feed and weaning are more important determinants of gut bacterial succession in piglets than breed and nursing mother as revealed by a reciprocal cross‐fostering model

Bian, Gaorui; Ma, Shouqing; Zhu, Zhigang; Su, Yong; Zoetendal, Erwin G.; Mackie, Roderick I.; Liu, Junhua; Mu, Chunlong; Huang, Ruihua; Smidt, Hauke; Zhu, Weiyun

doi:10.1111/1462-2920.13272

Cited by 183 publications

(225 citation statements)

References 51 publications

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“…As reported previously [28][29][30], age and diet were the main factors influencing the development of the fecal bacterial microbiota, with the greatest shift in the phyla Proteobacteria and Firmicutes during the suckling phase. Aside from maturational changes leading to a more diversified fecal microbiota composition from day 0 to 28 of life, introduction of solid feed on day 10 of life likely further promoted an earlier diversification of the fecal microbiota in pigs of the present study compared to other studies in which suckling piglets had no access to creep feed [28,30].…”

Section: Discussionsupporting

confidence: 72%

“…Likewise, Clostridiaceae are typical early colonizers of the neonatal GI tract and function as precursor for anaerobic bacteria like Bacteroides [31]. We did not find a clear predominance of Bacteroidales which have been associated with milk-glycan utilization during the suckling period as reported by others [28][29][30]. Instead, Christensenellaceae increased in feces until day 28 of life in the present study, indicating their potential role in fermentation of milk sugar, which would be supported by results for stool of lactose-intolerant humans where Christensenellaceae increased after the ingestion of galacto-oligosaccharides or dairy-based diets [32].…”

Section: Discussionsupporting

confidence: 56%

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Early Parenteral Administration of Ceftiofur has Gender-Specific Short- and Long-Term Effects on the Fecal Microbiota and Growth in Pigs from the Suckling to Growing Phase

Ruczizka

Metzler‐Zebeli

Unterweger

et al. 2019

Animals

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Simple Summary: Antibiotics are commonly used in prevention and therapy of bacterial diseases in pig production. Although the main target of antibiotics are the pathogenic bacteria, they often disrupt the commensal gut microbiota as a whole, leading to intestinal disturbances. These detrimental effects have been well established for oral administration of antibiotics, whereas knowledge about potential disturbing effects of single parenteral antibiotic treatments on the gut microbiota development is limited. In this research, the impact of a single antibiotic injection on the first day of life on the maturation of the fecal microbiome and host growth performance was evaluated from the suckling to the growing phase. Results showed that a single antibiotic injection early in life influenced the bacterial community development in the short-and long-term and that this disturbance in the bacterial community was sex-specific. Present results further demonstrated that changes in the bacterial ecosystem of the gut may impair the growth performance of the growing pig. Thus, the results of the present study emphasize the importance of a proper and strict use of antibiotics in swine herds.Abstract: Using ceftiofur during the first days of life is a common preventative strategy against several bacterial diseases in pig production. This study aimed to evaluate short-and long-term effects of early use of ceftiofur on the fecal microbiota development in suckling and growing pigs. Sixty-four piglets from eight litters were assigned to the antibiotic (AB; n = 32) or control group (control; n = 32). Twelve hours postpartum (day 0) AB piglets received an intramuscular injection of ceftiofur (5.0 mg/kg body weight) or a placebo. DNA was extracted from fecal samples collected on days 0, 12, 28, and 97 for deep-sequencing of the 16S rRNA gene. The AB administration disturbed the maturational changes in the fecal microbiome, whereby effects were sex-specific. Sex-related differences in AB metabolism in females and males may have caused these diverging AB-effects on the fecal microbiota. Especially the loss of bacterial diversity and of certain taxa in female AB pigs may have contributed to the decreased body weight of these females on day 97 of life. Taken together, this study showed that an AB injection with ceftiofur 12 h postpartum markedly affected the successional changes in the fecal microbiota composition in male and female pigs, with long-term consequences for host performance.

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Section: Discussionsupporting

confidence: 72%

Section: Discussionsupporting

confidence: 56%

Early Parenteral Administration of Ceftiofur has Gender-Specific Short- and Long-Term Effects on the Fecal Microbiota and Growth in Pigs from the Suckling to Growing Phase

Ruczizka

Metzler‐Zebeli

Unterweger

et al. 2019

Animals

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“…Not only were these mice siblings but also weaned by different mothers. The effects of weaning are similar to Bian et al wherein the abundance of an unclassified strain of Clostridiaceae was affected by the nursing mother [63]. Our results reiterate the impact of the mother on the microbiome, but also show this dynamic transfers even when explanted from the source.…”

Section: Discussionsupporting

confidence: 89%

A new technique for use in the study of the microbiome: An evaluation of a three-dimensional cell culture technique in maintaining the gastrointestinal microbiome of four Balb/c female mice and implications for future studies

Castaneda

Brady²,

Speshock

2019

Preprint

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Fluctuations in oxygen, pH, nutrients, or other factors such as food or pharmaceuticals, may perturb the microbiota of the gastrointestinal (GI) tract. This environmental variation is a cause for concern given dysbiosis of the microbiome is correlated with disease states; thereby, model organisms are utilized to study microbial communities during, after, or before shifts in microbes since intact ex vivo microbiomes have historically been challenging to utilize. The objective of this study is to culture an explant microbiome of 4 Balb/c, laboratory bred mice to develop an ex vivo tool for future microbiome studies. We cultured homogenates of the distal colon of 4 mice in three dimensional, 24 well plate culture dishes. These dishes were incubated for 24 hours in two different oxygen concentration levels, 0% and 20%. The pH of the plate was tested before and after incubation. To analyze the integrity of the microbiome, we utilized 16S sequencing. Further, we utilized 16S metagenomics to characterize fecal samples and colon samples to speculate whether future studies may utilize feces in constructing an explant microbiome to spare animal lives. We found that pH and familial relationship had a profound impact on community structure while oxygen did not have a significant influence. The feces and the colon were similar in community profiles, which lends credence to utilizing feces in future studies. In addition, our efforts successfully cultured archaea, which included difficult to culture strains such as Miscellaneous Crenarchaeota group (MCG) and Methanobacteria. Ultimately, further attempts to culture and preserve an animal’s microbiome needs to control for and maintain stable pH.

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“…The upregulation of acetate and propionate production 264 by the microbiota at weaning reflects the metabolic adaptation of the gut bacteria to solid feed derived 265 substrates since these SCFAs are produced mainly through plant carbohydrate fermentation(Louis and 266 Flint, 2017). Besides this substrate effects, the increase SCFA production in piglets from maternity 1 267 after weaning might also be linked to the increase in the relative abundance of the Christensenellaceae, 268Christensenellaceae R-7 group and Ruminococcaceae UCG-002, also observed in previous studies 269(Frese et al, 2015;Bian et al, 2016;Chen et al, 2017). The ability of these bacterial groups to break 270 down complex plant polysaccharides suggests that the shift from maternal milk to a plant based diet 271 favored their growth (La Reau and Suen, 2018).…”

supporting

confidence: 55%

Functional maturation of the gut microbiota at weaning is influenced by maternal environment in piglets

Beaumont

Cauquil

Bertide

et al. 2020

Preprint

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13 14 Running title: Metabolic activity of piglet gut microbiota 15 2 ORIGINALITY -SIGNIFICANCE STATEMENT 16Bacterial metabolites are key molecular intermediates between the gut microbiota and host cells. Our 17 study in piglets reveals that the metabolic activity of the gut microbiota shifts at weaning, a key 18 developmental period for intestinal and immune health. We also show that this functional maturation 19 of the gut microbiota is strongly influenced by maternal environment. Thus, targeting early life 20 environmental factors is a promising strategy to program health trough the production of beneficial 21 bacterial metabolites at the suckling-to-weaning transition. 22 from the second maternity farm probably because they already had high relative concentration of short 34 chain fatty acids and higher relative abundance of Christensenellaceae R-7 group and 35Ruminococcaceae UCG-002 during the suckling period. In conclusion, the functional maturation of 36 the microbiota at weaning is highly dependent on the maternal environment in piglets. 37 38 KEY WORDS 39Early life, Milk, Solid food, Metabolites 40 observed only in piglets from one of the two maternity farms studied. In piglets from maternity 1, 126 there was a reduction of the relative abundance of Proteobacteria, Enterobacteriaceae and Escherichia-127Shigella after weaning while the relative abundances of Christensenellaceae, Christensenellaceae R-7 128 group and Ruminococcaceae UCG-002 increased. In piglets from maternity 2, the relative abundance 129 of Peptostreptococcaceae increased after weaning. After weaning (at day 23), the relative abundances 130 of Spirochaetes and Ruminococcaceae UCG-002 were higher in piglets from maternity 2 when 131 compared to piglets from maternity 1 while the opposite was observed for Atopobiaceae. Altogether, 132these results show that both maternal environment and weaning shape the microbiota composition in 133 piglets. 134 135 ACKNOWLEDGMENTS 369

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Age, introduction of solid feed and weaning are more important determinants of gut bacterial succession in piglets than breed and nursing mother as revealed by a reciprocal cross‐fostering model

Cited by 183 publications

References 51 publications

Early Parenteral Administration of Ceftiofur has Gender-Specific Short- and Long-Term Effects on the Fecal Microbiota and Growth in Pigs from the Suckling to Growing Phase

Early Parenteral Administration of Ceftiofur has Gender-Specific Short- and Long-Term Effects on the Fecal Microbiota and Growth in Pigs from the Suckling to Growing Phase

A new technique for use in the study of the microbiome: An evaluation of a three-dimensional cell culture technique in maintaining the gastrointestinal microbiome of four Balb/c female mice and implications for future studies

Functional maturation of the gut microbiota at weaning is influenced by maternal environment in piglets

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