Gut Feelings Begin in Childhood: the Gut Metagenome Correlates with Early Environment, Caregiving, and Behavior

ABSTRACT Psychosocial environments impact normative behavioral development in children, increasing the risk of problem behaviors and psychiatric disorders across the life span. Converging evidence demonstrates that early normative development is affected by the gut microbiome, which itself can be al...

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Autores principales:	Jessica E. Flannery, Keaton Stagaman, Adam R. Burns, Roxana J. Hickey, Leslie E. Roos, Ryan J. Giuliano, Philip A. Fisher, Thomas J. Sharpton
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	microbiome metagenomics childhood development behavior Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/55255623cf434eec94203c954dbf29b3
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spelling	oai:doaj.org-article:55255623cf434eec94203c954dbf29b32021-11-15T15:56:58ZGut Feelings Begin in Childhood: the Gut Metagenome Correlates with Early Environment, Caregiving, and Behavior10.1128/mBio.02780-192150-7511https://doaj.org/article/55255623cf434eec94203c954dbf29b32020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02780-19https://doaj.org/toc/2150-7511ABSTRACT Psychosocial environments impact normative behavioral development in children, increasing the risk of problem behaviors and psychiatric disorders across the life span. Converging evidence demonstrates that early normative development is affected by the gut microbiome, which itself can be altered by early psychosocial environments. However, much of our understanding of the gut microbiome’s role in early development stems from nonhuman animal models and predominately focuses on the first years of life, during peri- and postnatal microbial colonization. As a first step to identify if these findings translate to humans and the extent to which these relationships are maintained after initial microbial colonization, we conducted a metagenomic investigation among a cross-sectional sample of early school-aged children with a range of adverse experiences and caregiver stressors and relationships. Our results indicate that the taxonomic and functional composition of the gut microbiome correlates with behavior during a critical period of child development. Furthermore, our analysis reveals that both socioeconomic risk exposure and child behaviors associate with the relative abundances of specific taxa (e.g., Bacteroides and Bifidobacterium species) as well as functional modules encoded in their genomes (e.g., monoamine metabolism) that have been linked to cognition and health. While we cannot infer causality within this study, these findings suggest that caregivers may moderate the gut microbiome’s link to environment and behaviors beyond the first few years of life. IMPORTANCE Childhood is a formative period of behavioral and biological development that can be modified, for better or worse, by the psychosocial environment that is in part determined by caregivers. Not only do our own genes and the external environment influence such developmental trajectories, but the community of microbes living in, on, and around our bodies—the microbiome—plays an important role as well. By surveying the gut microbiomes of a cross-sectional cohort of early school-aged children with a range of psychosocial environments and subclinical mental health symptoms, we demonstrated that caregiving behaviors modified the child gut microbiome’s association to socioeconomic risk and behavioral dysregulation.Jessica E. FlanneryKeaton StagamanAdam R. BurnsRoxana J. HickeyLeslie E. RoosRyan J. GiulianoPhilip A. FisherThomas J. SharptonAmerican Society for MicrobiologyarticlemicrobiomemetagenomicschildhooddevelopmentbehaviorMicrobiologyQR1-502ENmBio, Vol 11, Iss 1 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	microbiome metagenomics childhood development behavior Microbiology QR1-502
spellingShingle	microbiome metagenomics childhood development behavior Microbiology QR1-502 Jessica E. Flannery Keaton Stagaman Adam R. Burns Roxana J. Hickey Leslie E. Roos Ryan J. Giuliano Philip A. Fisher Thomas J. Sharpton Gut Feelings Begin in Childhood: the Gut Metagenome Correlates with Early Environment, Caregiving, and Behavior
description	ABSTRACT Psychosocial environments impact normative behavioral development in children, increasing the risk of problem behaviors and psychiatric disorders across the life span. Converging evidence demonstrates that early normative development is affected by the gut microbiome, which itself can be altered by early psychosocial environments. However, much of our understanding of the gut microbiome’s role in early development stems from nonhuman animal models and predominately focuses on the first years of life, during peri- and postnatal microbial colonization. As a first step to identify if these findings translate to humans and the extent to which these relationships are maintained after initial microbial colonization, we conducted a metagenomic investigation among a cross-sectional sample of early school-aged children with a range of adverse experiences and caregiver stressors and relationships. Our results indicate that the taxonomic and functional composition of the gut microbiome correlates with behavior during a critical period of child development. Furthermore, our analysis reveals that both socioeconomic risk exposure and child behaviors associate with the relative abundances of specific taxa (e.g., Bacteroides and Bifidobacterium species) as well as functional modules encoded in their genomes (e.g., monoamine metabolism) that have been linked to cognition and health. While we cannot infer causality within this study, these findings suggest that caregivers may moderate the gut microbiome’s link to environment and behaviors beyond the first few years of life. IMPORTANCE Childhood is a formative period of behavioral and biological development that can be modified, for better or worse, by the psychosocial environment that is in part determined by caregivers. Not only do our own genes and the external environment influence such developmental trajectories, but the community of microbes living in, on, and around our bodies—the microbiome—plays an important role as well. By surveying the gut microbiomes of a cross-sectional cohort of early school-aged children with a range of psychosocial environments and subclinical mental health symptoms, we demonstrated that caregiving behaviors modified the child gut microbiome’s association to socioeconomic risk and behavioral dysregulation.
format	article
author	Jessica E. Flannery Keaton Stagaman Adam R. Burns Roxana J. Hickey Leslie E. Roos Ryan J. Giuliano Philip A. Fisher Thomas J. Sharpton
author_facet	Jessica E. Flannery Keaton Stagaman Adam R. Burns Roxana J. Hickey Leslie E. Roos Ryan J. Giuliano Philip A. Fisher Thomas J. Sharpton
author_sort	Jessica E. Flannery
title	Gut Feelings Begin in Childhood: the Gut Metagenome Correlates with Early Environment, Caregiving, and Behavior
title_short	Gut Feelings Begin in Childhood: the Gut Metagenome Correlates with Early Environment, Caregiving, and Behavior
title_full	Gut Feelings Begin in Childhood: the Gut Metagenome Correlates with Early Environment, Caregiving, and Behavior
title_fullStr	Gut Feelings Begin in Childhood: the Gut Metagenome Correlates with Early Environment, Caregiving, and Behavior
title_full_unstemmed	Gut Feelings Begin in Childhood: the Gut Metagenome Correlates with Early Environment, Caregiving, and Behavior
title_sort	gut feelings begin in childhood: the gut metagenome correlates with early environment, caregiving, and behavior
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/55255623cf434eec94203c954dbf29b3
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Gut Feelings Begin in Childhood: the Gut Metagenome Correlates with Early Environment, Caregiving, and Behavior

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