Social and psychological adversity are associated with distinct mother and infant gut microbiome variations

Barbara B. Warner; Bruce A. Rosa; I. Malick Ndao; Phillip I. Tarr; J. Philip Miller; Sarah K. England; Joan L. Luby; Cynthia E. Rogers; Carla Hall-Moore; Renay E. Bryant; Jacqueline D. Wang; Laura A. Linneman; Tara A. Smyser; Christopher D. Smyser; Deanna M. Barch; Gregory E. Miller; Edith Chen; John Martin; Makedonka Mitreva

doi:10.1038/s41467-023-41421-4

Social and psychological adversity are associated with distinct mother and infant gut microbiome variations

Barbara B. Warner^*, Bruce A. Rosa, I. Malick Ndao, Phillip I. Tarr, J. Philip Miller, Sarah K. England, Joan L. Luby, Cynthia E. Rogers, Carla Hall-Moore, Renay E. Bryant, Jacqueline D. Wang, Laura A. Linneman, Tara A. Smyser, Christopher D. Smyser, Deanna M. Barch, Gregory E. Miller, Edith Chen, John Martin, Makedonka Mitreva^*

^*Corresponding author for this work

Psychology

Research output: Contribution to journal › Article › peer-review

2 Scopus citations

Abstract

Health disparities are driven by underlying social disadvantage and psychosocial stressors. However, how social disadvantage and psychosocial stressors lead to adverse health outcomes is unclear, particularly when exposure begins prenatally. Variations in the gut microbiome and circulating proinflammatory cytokines offer potential mechanistic pathways. Here, we interrogate the gut microbiome of mother-child dyads to compare high-versus-low prenatal social disadvantage, psychosocial stressors and maternal circulating cytokine cohorts (prospective case-control study design using gut microbiomes from 121 dyads profiled with 16 S rRNA sequencing and 89 dyads with shotgun metagenomic sequencing). Gut microbiome characteristics significantly predictive of social disadvantage and psychosocial stressors in the mothers and children indicate that different discriminatory taxa and related pathways are involved, including many species of Bifidobacterium and related pathways across several comparisons. The lowest inter-individual gut microbiome similarity was observed among high-social disadvantage/high-psychosocial stressors mothers, suggesting distinct environmental exposures driving a diverging gut microbiome assembly compared to low-social disadvantage/low-psychosocial stressors controls (P = 3.5 × 10⁻⁵ for social disadvantage, P = 2.7 × 10⁻¹⁵ for psychosocial stressors). Children’s gut metagenome profiles at 4 months also significantly predicted high/low maternal prenatal IL-6 (P = 0.029), with many bacterial species overlapping those identified by social disadvantage and psychosocial stressors. These differences, based on maternal social and psychological status during a critical developmental window early in life, offer potentially modifiable targets to mitigate health inequities.

Original language	English (US)
Article number	5824
Journal	Nature communications
Volume	14
Issue number	1
DOIs	https://doi.org/10.1038/s41467-023-41421-4
State	Published - Dec 2023

Funding

This work was supported in part by NIMH grant RO1 MH113883, (BBW, BAR, IMN, PPT, PJM, SKE, JLL, CER, TAS, CDS, DMB, GEM, EC, JM, MM) March of Dimes (SKE), Children’s Discovery Institute II MD-II-2015-489 (BBW, IMN), Biobank Core P30DK052574 (PIT), REDCap database with Clinical and Translational Science Award (CTSA) Grant [UL1 TR000448] and Siteman Comprehensive Cancer Center and NCI Cancer Center Support Grant P30 CA091842. We are thankful to the families involved in the study, the MARCH of Dime Premature Research Center at Washington University and to members of the Washington University in St. Louis’ GTAC@MGI for technical support related to library construction and sequencing. This work was supported in part by NIMH grant RO1 MH113883, (BBW, BAR, IMN, PPT, PJM, SKE, JLL, CER, TAS, CDS, DMB, GEM, EC, JM, MM) March of Dimes (SKE), Children’s Discovery Institute II MD-II-2015-489 (BBW, IMN), Biobank Core P30DK052574 (PIT), REDCap database with Clinical and Translational Science Award (CTSA) Grant [UL1 TR000448] and Siteman Comprehensive Cancer Center and NCI Cancer Center Support Grant P30 CA091842. We are thankful to the families involved in the study, the MARCH of Dime Premature Research Center at Washington University and to members of the Washington University in St. Louis’ GTAC@MGI for technical support related to library construction and sequencing.

ASJC Scopus subject areas

General Chemistry
General Biochemistry, Genetics and Molecular Biology
General Physics and Astronomy

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Warner, B. B., Rosa, B. A., Ndao, I. M., Tarr, P. I., Miller, J. P., England, S. K., Luby, J. L., Rogers, C. E., Hall-Moore, C., Bryant, R. E., Wang, J. D., Linneman, L. A., Smyser, T. A., Smyser, C. D., Barch, D. M., Miller, G. E., Chen, E., Martin, J., & Mitreva, M. (2023). Social and psychological adversity are associated with distinct mother and infant gut microbiome variations. Nature communications, 14(1), Article 5824. https://doi.org/10.1038/s41467-023-41421-4

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title = "Social and psychological adversity are associated with distinct mother and infant gut microbiome variations",

abstract = "Health disparities are driven by underlying social disadvantage and psychosocial stressors. However, how social disadvantage and psychosocial stressors lead to adverse health outcomes is unclear, particularly when exposure begins prenatally. Variations in the gut microbiome and circulating proinflammatory cytokines offer potential mechanistic pathways. Here, we interrogate the gut microbiome of mother-child dyads to compare high-versus-low prenatal social disadvantage, psychosocial stressors and maternal circulating cytokine cohorts (prospective case-control study design using gut microbiomes from 121 dyads profiled with 16 S rRNA sequencing and 89 dyads with shotgun metagenomic sequencing). Gut microbiome characteristics significantly predictive of social disadvantage and psychosocial stressors in the mothers and children indicate that different discriminatory taxa and related pathways are involved, including many species of Bifidobacterium and related pathways across several comparisons. The lowest inter-individual gut microbiome similarity was observed among high-social disadvantage/high-psychosocial stressors mothers, suggesting distinct environmental exposures driving a diverging gut microbiome assembly compared to low-social disadvantage/low-psychosocial stressors controls (P = 3.5 × 10−5 for social disadvantage, P = 2.7 × 10−15 for psychosocial stressors). Children{\textquoteright}s gut metagenome profiles at 4 months also significantly predicted high/low maternal prenatal IL-6 (P = 0.029), with many bacterial species overlapping those identified by social disadvantage and psychosocial stressors. These differences, based on maternal social and psychological status during a critical developmental window early in life, offer potentially modifiable targets to mitigate health inequities.",

author = "Warner, {Barbara B.} and Rosa, {Bruce A.} and Ndao, {I. Malick} and Tarr, {Phillip I.} and Miller, {J. Philip} and England, {Sarah K.} and Luby, {Joan L.} and Rogers, {Cynthia E.} and Carla Hall-Moore and Bryant, {Renay E.} and Wang, {Jacqueline D.} and Linneman, {Laura A.} and Smyser, {Tara A.} and Smyser, {Christopher D.} and Barch, {Deanna M.} and Miller, {Gregory E.} and Edith Chen and John Martin and Makedonka Mitreva",

note = "Publisher Copyright: {\textcopyright} 2023, Springer Nature Limited.",

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Warner, BB, Rosa, BA, Ndao, IM, Tarr, PI, Miller, JP, England, SK, Luby, JL, Rogers, CE, Hall-Moore, C, Bryant, RE, Wang, JD, Linneman, LA, Smyser, TA, Smyser, CD, Barch, DM, Miller, GE , Chen, E, Martin, J & Mitreva, M 2023, 'Social and psychological adversity are associated with distinct mother and infant gut microbiome variations', Nature communications, vol. 14, no. 1, 5824. https://doi.org/10.1038/s41467-023-41421-4

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T1 - Social and psychological adversity are associated with distinct mother and infant gut microbiome variations

AU - Warner, Barbara B.

AU - Rosa, Bruce A.

AU - Ndao, I. Malick

AU - Tarr, Phillip I.

AU - Miller, J. Philip

AU - England, Sarah K.

AU - Luby, Joan L.

AU - Rogers, Cynthia E.

AU - Hall-Moore, Carla

AU - Bryant, Renay E.

AU - Wang, Jacqueline D.

AU - Linneman, Laura A.

AU - Smyser, Tara A.

AU - Smyser, Christopher D.

AU - Barch, Deanna M.

AU - Miller, Gregory E.

AU - Chen, Edith

AU - Martin, John

AU - Mitreva, Makedonka

PY - 2023/12

Y1 - 2023/12

N2 - Health disparities are driven by underlying social disadvantage and psychosocial stressors. However, how social disadvantage and psychosocial stressors lead to adverse health outcomes is unclear, particularly when exposure begins prenatally. Variations in the gut microbiome and circulating proinflammatory cytokines offer potential mechanistic pathways. Here, we interrogate the gut microbiome of mother-child dyads to compare high-versus-low prenatal social disadvantage, psychosocial stressors and maternal circulating cytokine cohorts (prospective case-control study design using gut microbiomes from 121 dyads profiled with 16 S rRNA sequencing and 89 dyads with shotgun metagenomic sequencing). Gut microbiome characteristics significantly predictive of social disadvantage and psychosocial stressors in the mothers and children indicate that different discriminatory taxa and related pathways are involved, including many species of Bifidobacterium and related pathways across several comparisons. The lowest inter-individual gut microbiome similarity was observed among high-social disadvantage/high-psychosocial stressors mothers, suggesting distinct environmental exposures driving a diverging gut microbiome assembly compared to low-social disadvantage/low-psychosocial stressors controls (P = 3.5 × 10−5 for social disadvantage, P = 2.7 × 10−15 for psychosocial stressors). Children’s gut metagenome profiles at 4 months also significantly predicted high/low maternal prenatal IL-6 (P = 0.029), with many bacterial species overlapping those identified by social disadvantage and psychosocial stressors. These differences, based on maternal social and psychological status during a critical developmental window early in life, offer potentially modifiable targets to mitigate health inequities.

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Social and psychological adversity are associated with distinct mother and infant gut microbiome variations

Abstract

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