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

Author:

Querdasi Francesca R.1ORCID,Enders Craig1,Karnani Neerja2,Broekman Birit2ORCID,Yap Seng Chong23,Gluckman Peter D.24ORCID,Mary Daniel Lourdes56,Yap Fabian789,Eriksson Johan G.231011,Cai Shirong2,Chong Mary Foong-Fong12ORCID,Toh Jia Ying2ORCID,Godfrey Keith1314ORCID,Meaney Michael J.21516,Callaghan Bridget L.1

Affiliation:

1. Department of Psychology, University of California Los Angeles, Los Angeles, CA 90095

2. Singapore Institute for Clinical Sciences, Agency for Science, Technology, and Research, Singapore 138632, Singapore

3. Department of Obstetrics and Gynaecology, Yong Loo School of Medicine, National University of Singapore, Singapore 117597, Singapore

4. Liggins Institute, University of Auckland, Auckland 1023, New Zealand

5. Duke-National University of Singapore Medical School, Singapore 169857, Singapore

6. Department of Child Development, KK Women’s and Children’s Hospital, Singapore 229899, Singapore

7. Department of Paediatrics, KK Women’s and Children’s Hopsital, Singapore 229899, Singapore

8. Department of Pediatrics, Lee Kong Chian School of Medicine, Nanyang Technological University, Singapore 636921, Singapore

9. Department of Maternal Fetal Medicine, KK Women’s and Children’s Hospital, Singapore 229899, Singapore

10. Department of General Practice and Primary Health, University of Helsinki and Helsinki University Hospital, 00100 Helsinki, Finland

11. Program of Public Health Research, Folkhälsan Research Center, 00250 Helsinki, Finland

12. Saw Swee Hock School of Public Health, National University of Singapore, Singapore 117561, Singapore

13. Department of Epidemiology, University of Southampton, Southampton SO16 6YD, United Kingdom

14. Department of Human Development, University of Southampton, Southampton SO16 6YD, United Kingdom

15. Department of Psychiatry, McGill University, Montreal, Quebec H3A 0G4, Canada

16. Brain–Body Initiative, Agency for Science, Technology, and Research, Singapore 138632, Singapore

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.

Funder

Singapore National Research Foundation

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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