Microbiota control of maternal behavior regulates early postnatal growth of offspring

Lee, Yujung Michelle; Mu, Andre; Wallace, Martina; Gengatharan, Jivani M.; Fürst, Annalee; Bode, Lars; Metallo, Christian M.; Ayres, Janelle S.

doi:10.1126/sciadv.abe6563

Cited by 17 publications

(15 citation statements)

References 61 publications

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“…It is well accepted that neurodevelopment is susceptible to changes in early life, and the impacts of maternal care on neurodevelopment have been highly investigated 53 – 55 . More recently, it has been shown that the fetal and infant microbiome is also dynamic and shares similar susceptibilities to early life changes dependent on infant-mother interactions 5 , 56 – 58 . Maternal diet can also influence offspring microbiome diversity, as the ratio of Firmicutes to Bacteroidetes in HFD-fed mothers is shared by their non-HFD-fed offspring 59 , 60 .…”

Section: Introductionmentioning

confidence: 99%

Effects of paternal high-fat diet and maternal rearing environment on the gut microbiota and behavior

Korgan

Foxx

Hashmi

et al. 2022

Sci Rep

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Exposing a male rat to an obesogenic high-fat diet (HFD) influences attractiveness to potential female mates, the subsequent interaction of female mates with infant offspring, and the development of stress-related behavioral and neural responses in offspring. To examine the stomach and fecal microbiome’s potential roles, fecal samples from 44 offspring and stomach samples from offspring and their fathers were collected and bacterial community composition was studied by 16 small subunit ribosomal RNA (16S rRNA) gene sequencing. Paternal diet (control, high-fat), maternal housing conditions (standard or semi-naturalistic housing), and maternal care (quality of nursing and other maternal behaviors) affected the within-subjects alpha-diversity of the offspring stomach and fecal microbiomes. We provide evidence from beta-diversity analyses that paternal diet and maternal behavior induced community-wide shifts to the adult offspring gut microbiome. Additionally, we show that paternal HFD significantly altered the adult offspring Firmicutes to Bacteroidetes ratio, an indicator of obesogenic potential in the gut microbiome. Additional machine-learning analyses indicated that microbial species driving these differences converged on Bifidobacterium pseudolongum. These results suggest that differences in early-life care induced by paternal diet and maternal care significantly influence the microbiota composition of offspring through the microbiota-gut-brain axis, having implications for adult stress reactivity.

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Section: Introductionmentioning

confidence: 99%

Effects of paternal high-fat diet and maternal rearing environment on the gut microbiota and behavior

Korgan

Foxx

Hashmi

et al. 2022

Sci Rep

View full text Add to dashboard Cite

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“…Changes in community structure could result in functional changes, and then affect host health. For instance, adiposity and insulin insensitivity were increased in germ-free mice receiving the intestinal microbiota from women in late pregnancy compared to those in mice inoculated with the gut microbiota of women in early pregnancy ( Koren et al, 2012 ), thus affecting innate immune function and fetal development and health ( Gomez de Agüero et al, 2016 ; Lee et al, 2021 ) by regulating the incipient microbial biomass and communities of offspring ( Perez-Muñoz et al, 2017 ; Bi et al, 2021 ). Furthermore, gut microbiota changes may directly influence maternal metabolic alterations related to pregnancy ( Koren et al, 2012 ).…”

Section: Introductionmentioning

confidence: 99%

Metabolic Alternations During Gestation in Dezhou Donkeys and the Link to the Gut Microbiota

Liu

et al. 2022

Front. Microbiol.

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The maternal intestinal microbial community changes dramatically during pregnancy and plays an important role in animal growth, metabolism, immunity and reproduction. However, our understanding of microbiota compositional dynamics during the whole pregnancy period in donkey is incomplete. This study was carried out to evaluate gut microbiota alterations as well as the correlation with serum biochemical indices, comparing pregnant donkeys to non-pregnant donkeys. A total of 18 pregnant (including EP, early-stage pregnancy; MP, middle-stage pregnancy and LP, late-stage pregnancy) and six non-pregnant (C as a control) donkey blood samples and rectum contents were collected. The results showed that pregnant donkeys had higher microbial richness than non-pregnant donkeys and that the lowest microbial diversity occurred at the EP period. Moreover, the relative abundances of the families Clostridiaceae and Streptococcaceae were significantly higher in the EP group (p < 0.05) than that in the C and MP groups, while the relative abundances of the families Lachnospiraceae and Rikenellaceae were significantly lower in the EP group (p < 0.05) than that in the C group. The predicted microbial gene functions related to the inflammatory response and apoptosis, such as Staphylococcus aureus infection, the RIG-1-like receptor signaling pathway and apoptosis, were mainly enriched in EP. Furthermore, pregnant donkeys had higher glucose levels than non-pregnant donkeys, especially at EP period. EP donkeys had lower triglyceride, total protein and albumin levels but higher malondialdehyde, interleukin 1β, interleukin 6 and tumor necrosis factor-α levels than those in the C and MP groups. Additionally, there were strong correlations between inflammatory cytokine levels and the relative abundances of genera belonging to the Clostridiaceae and Streptococcaceae families. This is the first comparative study performed in donkeys that indicates that pregnancy status (especially in the early pregnancy period) alters the gut microbiota composition, which was correlated with serum biochemical parameters. These results could provide useful information for improving the reproductive management in Dezhou donkeys.

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“…The early postnatal period of life is a vital stage for growth and development. The intestinal microbiota has emerged as a critical regulator of growth and development in the early postnatal period of life ( Lee et al, 2021 ). The intestinal microbiota is deemed to coincide with the development of our body systems ( Cowan et al, 2020 ; Wilkins and Reimer, 2021 ).…”

Section: Introductionmentioning

confidence: 99%

The Influence of Cesarean Section on the Composition and Development of Gut Microbiota During the First 3 Months of Life

Gao

Tao

et al. 2021

Front. Microbiol.

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The intestinal microbiota has emerged as a critical regulator of growth and development in the early postnatal period of life. Cesarean section (CS) delivery is one of the strongest disrupting factors of the normal colonization process and has been reported as a risk factor for disorders in later life. In this study, we dynamically and longitudinally evaluated the impact of CS on the initial colonization pattern and development of gut microbiota by 16 healthy Chinese infants with fecal samples collected at 9 time points (day 5, day 8, day 11, week 2, week 4, week 6, week 7, month 2, and month 3) during the first 3 months of life. The V3–V4 regions of 16S rRNA gene were analyzed by Illumina sequencing. In comparison with vaginally delivered (VD) infants, infants born by CS showed decreased relative abundance of Bacteroides and Parabacteroides and enrichment of Clostridium_sensu_stricto_1, Enterococcus, Klebsiella, Clostridioides, and Veillonella. Most interestingly, Firmicutes/Bacteroidetes ratio was found to be significantly higher in the CS group than in the VD group from day 5 until month 3. Besides, the results of microbial functions showed that the VD group harbored significantly higher levels of functional genes in vitamin B6 metabolism at day 5, day 8, week 2, week 4, week 6, week 7, month 2, and month 3 and taurine and hypotaurine metabolism at day 5, while the phosphotransferase system and starch and sucrose metabolism involved functional genes were plentiful in the CS group at day 11, week 2, week 4, week 6, week 7, and month 2 and at week 2, week 7, and month 2, respectively. Our results establish a new evidence that CS affected the composition and development of gut microbiota in the first 3 months and provide a novel insight into strategies for CS-related disorders in later life.

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Microbiota control of maternal behavior regulates early postnatal growth of offspring

Cited by 17 publications

References 61 publications

Effects of paternal high-fat diet and maternal rearing environment on the gut microbiota and behavior

Effects of paternal high-fat diet and maternal rearing environment on the gut microbiota and behavior

Metabolic Alternations During Gestation in Dezhou Donkeys and the Link to the Gut Microbiota

The Influence of Cesarean Section on the Composition and Development of Gut Microbiota During the First 3 Months of Life

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