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Multigenerational adversity impacts on human gut microbiome composition and socioemotional functioning in early childhood

Multigenerational adversity impacts on human gut microbiome composition and socioemotional functioning in early childhood
Multigenerational adversity impacts on human gut microbiome composition and socioemotional functioning in early childhood

Adversity exposures in the prenatal and postnatal period are associated with an increased risk for psychopathology, which can be perpetuated across generations. Nonhuman animal research highlights the gut microbiome as a putative biological mechanism underlying such generational risks. In a sample of 450 mother–child dyads living in Singapore, we examined associations between three distinct adversity exposures experienced across two generations—maternal childhood maltreatment, maternal prenatal anxiety, and second-generation children’s exposure to stressful life events—and the gut microbiome composition of second-generation children at 2 y of age. We found distinct differences in gut microbiome profiles linked to each adversity exposure, as well as some nonaffected microbiome features (e.g., beta diversity). Remarkably, some of the microbial taxa associated with concurrent and prospective child socioemotional functioning shared overlapping putative functions with those affected by adversity, suggesting that the intergenerational transmission of adversity may have a lasting impact on children’s mental health via alterations to gut microbiome functions. Our findings open up a new avenue of research into the underlying mechanisms of intergenerational transmission of mental health risks and the potential of the gut microbiome as a target for intervention.

0027-8424
Querdasi, Francesca R.
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Enders, Craig
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Karnani, Neerja
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Broekman, Birit
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Chong, Yap-Seng
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Gluckman, Peter D.
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Daniel, Lourdes Mary
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Yap, Fabian
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Eriksson, Johan G.
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Cai, Shirong
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Chong, Mary Foong-Fong
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Toh, Jia Ying
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Godfrey, Keith
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Meaney, Michael J.
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Callaghan, Bridget L.
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Querdasi, Francesca R.
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Enders, Craig
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Karnani, Neerja
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Broekman, Birit
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Chong, Yap-Seng
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Gluckman, Peter D.
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Daniel, Lourdes Mary
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Yap, Fabian
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Eriksson, Johan G.
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Cai, Shirong
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Chong, Mary Foong-Fong
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Toh, Jia Ying
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Godfrey, Keith
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Meaney, Michael J.
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Callaghan, Bridget L.
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Querdasi, Francesca R., Enders, Craig, Karnani, Neerja, Broekman, Birit, Chong, Yap-Seng, Gluckman, Peter D., Daniel, Lourdes Mary, Yap, Fabian, Eriksson, Johan G., Cai, Shirong, Chong, Mary Foong-Fong, Toh, Jia Ying, Godfrey, Keith, Meaney, Michael J. and Callaghan, Bridget L. (2023) Multigenerational adversity impacts on human gut microbiome composition and socioemotional functioning in early childhood. Proceedings of the National Academy of Sciences, 120 (30), [e2213768120]. (doi:10.1073/pnas.2213768120).

Record type: Article

Abstract

Adversity exposures in the prenatal and postnatal period are associated with an increased risk for psychopathology, which can be perpetuated across generations. Nonhuman animal research highlights the gut microbiome as a putative biological mechanism underlying such generational risks. In a sample of 450 mother–child dyads living in Singapore, we examined associations between three distinct adversity exposures experienced across two generations—maternal childhood maltreatment, maternal prenatal anxiety, and second-generation children’s exposure to stressful life events—and the gut microbiome composition of second-generation children at 2 y of age. We found distinct differences in gut microbiome profiles linked to each adversity exposure, as well as some nonaffected microbiome features (e.g., beta diversity). Remarkably, some of the microbial taxa associated with concurrent and prospective child socioemotional functioning shared overlapping putative functions with those affected by adversity, suggesting that the intergenerational transmission of adversity may have a lasting impact on children’s mental health via alterations to gut microbiome functions. Our findings open up a new avenue of research into the underlying mechanisms of intergenerational transmission of mental health risks and the potential of the gut microbiome as a target for intervention.

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Accepted/In Press date: 25 May 2023
Published date: 18 July 2023
Additional Information: Funding Information: ACKNOWLEDGMENTS. Funding was provided by the Singapore National Research Foundation under its Translational and Clinical Research Flagship Programme and administered by the Singapore Ministry of Health’s National Medical Research Council, Singapore–NMRC/TCR/004-NUS/2008; NMRC/TCR/012-NUHS/2014.Additional funding was provided by the Singapore Institute for Clinical Sciences,Agency for Science Technology and Research,the JPB Foundation (US) Toxic Stress Network (M.J.M.),and the UCLA Psychology Summer Research Fellowship (F.R.Q.). We thank the Growing Up in Singapore Towards healthy Outcomes (GUSTO) study team, and Ang Li Ting in particular, for providing support with data access and processing. We also thank the participants for their invaluable contributions to the GUSTO study. Publisher Copyright: Copyright © 2023 the Author(s).

Identifiers

Local EPrints ID: 478604
URI: http://eprints.soton.ac.uk/id/eprint/478604
ISSN: 0027-8424
PURE UUID: f6eedff7-dcbe-42f5-9362-0f95859e4091
ORCID for Keith Godfrey: ORCID iD orcid.org/0000-0002-4643-0618

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Date deposited: 05 Jul 2023 17:26
Last modified: 18 Mar 2024 02:38

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Contributors

Author: Francesca R. Querdasi
Author: Craig Enders
Author: Neerja Karnani
Author: Birit Broekman
Author: Yap-Seng Chong
Author: Peter D. Gluckman
Author: Lourdes Mary Daniel
Author: Fabian Yap
Author: Johan G. Eriksson
Author: Shirong Cai
Author: Mary Foong-Fong Chong
Author: Jia Ying Toh
Author: Keith Godfrey ORCID iD
Author: Michael J. Meaney
Author: Bridget L. Callaghan

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