Heat stress during late gestation disrupts maternal microbial transmission with altered offspring’s gut microbial colonization and serum metabolites in a pig model

Jian-xin, HE; Zheng, Weijiang; Tao, Chengyuan; Guo, Huijuan; Xue, Yongqiang; Zhao, Ruqian; Yao, Wen

doi:10.1016/j.envpol.2020.115111

Cited by 34 publications

(35 citation statements)

References 81 publications

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“…For example, it caused the increase of Proteobacteria and the decrease of Bacteroides in pig feces (Xiong et al, 2020) and induced significant changes in the variety of duodenum, jejunum, ileum flora in Shaoxing duck (Tian et al, 2020) and cow fecal microbiota (Chen et al, 2018). Neonatal microbial colonization was affected via affecting maternal microbial transmission in late gestational HE in a pig model (He et al, 2020). Besides, significant changes were seen in energy metabolism in HE (including phosphorus, alkaline phosphatase, total protein, et al) stress response indices, hormones and immune factors were disorder in pigs (Xiong et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

Integrative Analysis of Vaginal Microorganisms and Serum Metabolomics in Rats With Estrous Cycle Disorder Induced by Long-Term Heat Exposure Based on 16S rDNA Gene Sequencing and LC/MS-Based Metabolomics

Fan

Chen

et al. 2021

Front. Cell. Infect. Microbiol.

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Long term heat exposure (HE) leads to estrous cycle disorder (ECD) in female rats and damages reproductive function. However, the regulation mechanism of vaginal microorganisms and serum metabolomics remains unclear. This study aimed to explore the effects of microbes on the vaginal secretions of rats with ECD and describe the serum metabolomics characteristics and their relationship with vaginal microorganisms. The alterations in the serum levels of neurotransmitters were used to verify the possible regulatory pathways. The relative abundance, composition, and colony interaction network of microorganisms in the vaginal secretions of rats with ECD changed significantly. The metabolomics analysis identified 22 potential biomarkers in the serum including lipid metabolism, amino acid metabolism, and mammalian target of rapamycin and gonadotropin-releasing hormone (GnRH) signaling pathways. Further, 52 pairs of vaginal microbiota–serum metabolites correlations (21 positive and 31 negative) were determined. The abundance of Gardnerella correlated positively with the metabolite L-arginine concentration and negatively with the oleic acid concentration. Further, a negative correlation was found between the abundance of Pseudomonas and the L-arginine concentration and between the metabolite benzoic acid concentration and the abundance of Adlercreutzia. These four bacteria–metabolite pairs had a direct or indirect relationship with the estrous cycle and reproduction. The glutamine, glutamate, and dopamine levels were significantly uncontrolled. The former two were closely related to GnRH signaling pathways involved in the development and regulation of HE-induced ECD in rats. Serum neurotransmitters partly reflected the regulatory effect of vaginal microorganisms on the host of HE-induced ECD, and glutamatergic neurotransmitters might be closely related to the alteration in vaginal microorganisms. These findings might help comprehend the mechanism of HE-induced ECD and propose a new intervention based on vaginal microorganisms.

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Section: Introductionmentioning

confidence: 99%

Integrative Analysis of Vaginal Microorganisms and Serum Metabolomics in Rats With Estrous Cycle Disorder Induced by Long-Term Heat Exposure Based on 16S rDNA Gene Sequencing and LC/MS-Based Metabolomics

Fan

Chen

et al. 2021

Front. Cell. Infect. Microbiol.

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“…The differences were significant in all the above tests at P < 0.05. Additionally, the potential microbial drivers for the significant differential serum metabolites and mitochondrial functional genes were identified as described previously (He et al, 2020). Yang, J., Yin, P., Zhou, M., Ou, C.-Q., Guo, Y., Gasparrini, A., et al (2015) Cardiovascular mortality risk attributable to ambient temperature in China.…”

Section: Discussionmentioning

confidence: 99%

“…Currently, the HS impacts on the physiological and metabolic profiles of the gestational animal model have been illustrated sufficiently (Gonzalez‐Rivas et al ., 2019). We have pointed out that late gestational HS induces maternal gut microbial dysbiosis which is transferred to her offspring in a pig model (He et al ., 2020). Emerging evidence indicates a robust association between the gut microbiota, especially its metabolites, and liver dysfunction (Compare et al ., 2012).…”

Section: Discussionmentioning

confidence: 99%

High ambient temperature exposure during late gestation disrupts glycolipid metabolism and hepatic mitochondrial function tightly related to gut microbial dysbiosis in pregnant mice

Jian-xin

Liu

Zheng

et al. 2021

Microbial Biotechnology

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As global warming intensifies, emerging evidence has demonstrated high ambient temperature during pregnancy negatively affects maternal physiology with compromised pregnant outcomes; however, little is known about the roles of gut microbiota and its underlying mechanisms in this process. Here, for the first time, we explored the potential mechanisms of gut microbiota involved in the disrupted glycolipid metabolism via hepatic mitochondrial function. Our results indicate heat stress (HS) reduces fat and protein contents and serum levels of insulin and triglyceride (TG), while increases that of non-esterified fatty acid (NEFA), b-hydroxybutyric acid (B-HBA), creatinine and blood urea nitrogen (BUN) (P < 0.05). Additionally, HS downregulates both mitochondrial genes (mtDNA) and nuclear encoding mitochondrial functional genes with increasing serum levels of malondialdehyde (MDA) and 8hydroxydeoxyguanosine (8-OHdG) (P < 0.05). Regarding microbial response, HS boosts serum levels of lipopolysaccharide (LPS) (P < 0.05) and alters b-diversity (ANOSIM, P < 0.01), increasing the proportions of Escherichia-Shigella, Acinetobacter and Klebsiella (q < 0.05), while reducing that of Ruminiclostridium, Blautia, Lachnospiraceae_ NK4A136_group, Clostridium VadinBB60 and Muribaculaceae (q < 0.05). PICRUSt analysis predicts that HS upregulates 11 KEGG pathways, mainly including bile secretion and bacterial invasion of epithelial cells. The collective results suggest that microbial dysbiosis due to late gestational HS has strong associations with damaged hepatic mitochondrial function and disrupted metabolic profiles.

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“…Considering the sow-piglet vertical transmission of the microbiota, distressing the sows by altering their microbiota can directly affect that of the litter. In fact, heat stress (HS) in late gestation affected the beta diversity of the intestinal and vaginal microbiota of the sows and, thus, that of the colon of the offspring [66]. The microbial communities in HT sows shifted toward a type less oriented to the digestion capacity of plant oligosaccharides [66].…”

Section: Environmental Stressors and Managementmentioning

confidence: 99%

“…In fact, heat stress (HS) in late gestation affected the beta diversity of the intestinal and vaginal microbiota of the sows and, thus, that of the colon of the offspring [66]. The microbial communities in HT sows shifted toward a type less oriented to the digestion capacity of plant oligosaccharides [66]. These sows transmitted to the offspring more bacteria of Escherichia-Shigella genus from the mixed intestine vagina path and of Fusobacterium from the sole vagina.…”

Section: Environmental Stressors and Managementmentioning

confidence: 99%

Timely Control of Gastrointestinal Eubiosis: A Strategic Pillar of Pig Health

et al. 2021

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The pig gastrointestinal tract (GIT) is an open ecosystem in which microorganisms and their host are mutually involved and continually adapt to different factors and problems which may or may not be host dependent or due to the production system. The aim of the present review is to highlight the factors affecting the GIT microbial balance in young pigs, focusing on the pre- and post-weaning phases, to define a road map for improving pig health and the production efficiency of the food chain. Birth and weaning body weight, physiological maturation, colostrum and milk (composition and intake), genetic background, environmental stressors and management practices, antibiotic use and diet composition are considered. Overall, there is a lack of knowledge regarding the effect that some factors, including weaning age, the use of creep feed, the composition of the colostrum and milk and the use of antibiotics, may have on the gut microbiome of piglets. Furthermore, the information on the gut microbiome of piglets is mainly based on the taxonomy description, while there is a lack of knowledge regarding the functional modification of the microbiota, essential for the exploitation of microbiota potential for modulating pig physiology.

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Heat stress during late gestation disrupts maternal microbial transmission with altered offspring’s gut microbial colonization and serum metabolites in a pig model

Cited by 34 publications

References 81 publications

Integrative Analysis of Vaginal Microorganisms and Serum Metabolomics in Rats With Estrous Cycle Disorder Induced by Long-Term Heat Exposure Based on 16S rDNA Gene Sequencing and LC/MS-Based Metabolomics

Integrative Analysis of Vaginal Microorganisms and Serum Metabolomics in Rats With Estrous Cycle Disorder Induced by Long-Term Heat Exposure Based on 16S rDNA Gene Sequencing and LC/MS-Based Metabolomics

High ambient temperature exposure during late gestation disrupts glycolipid metabolism and hepatic mitochondrial function tightly related to gut microbial dysbiosis in pregnant mice

Timely Control of Gastrointestinal Eubiosis: A Strategic Pillar of Pig Health

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