Associations of Stool Metal Exposures with Childhood Gut Microbiome Multiomics Profiles in a Prospective Birth Cohort Study

Feng Gao; Yike Shen; Haotian Wu; Hannah E. Laue; Fion K. Lau; Virginie Gillet; Yunjia Lai; Martha J. Shrubsole; Diddier Prada; Wei Zhang; Zhonghua Liu; Jean Philippe Bellenger; Larissa Takser; Andrea A. Baccarelli

doi:10.1021/acs.est.4c09642

Associations of Stool Metal Exposures with Childhood Gut Microbiome Multiomics Profiles in a Prospective Birth Cohort Study

Feng Gao, Yike Shen^*, Haotian Wu, Hannah E. Laue, Fion K. Lau, Virginie Gillet, Yunjia Lai, Martha J. Shrubsole, Diddier Prada, Wei Zhang, Zhonghua Liu, Jean Philippe Bellenger, Larissa Takser, Andrea A. Baccarelli

^*Corresponding author for this work

Preventive Medicine

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

Abstract

Metal exposures are closely related to childhood developmental health. However, their effects on the childhood gut microbiome, which also impacts health, are largely unexplored using microbiome multiomics including the metagenome and metatranscriptome. This study examined the associations of fecal profiles of metal/element exposures with gut microbiome species and active functional pathways in 8- to 12-year-old children (N = 116) participating in the GESTation and Environment (GESTE) cohort study. We analyzed 19 stool metal and element concentrations (B, Na, Mg, Al, K, Ca, V, Cr, Mn, Fe, Co, Ni, Cu, Zn, As, Mo, Cd, Ba, and Pb). Covariate-adjusted linear regression models identified several significant microbiome associations with continuous stool metal/element concentrations. For instance, Zn was positively associated with Turicibacter sanguinis (coef = 1.354, q-value = 0.039) and negatively associated with Eubacterium eligens (coef = −0.794, q-value = 0.044). Higher concentrations of Cd were associated with lower Eubacterium eligens (coef = −0.774, q-value = 0.045). Additionally, a total of 490 significant functional pathways such as biosynthesis and degradation/utilization/assimilation were identified, corresponding to different functions, including amino acid synthesis and carbohydrate degradation. Our results suggest links among metal exposures, pediatric gut microbiome multiomics, and potential health implications. Future work will further explore their relation to childhood health.

Original language	English (US)
Pages (from-to)	22053-22063
Number of pages	11
Journal	Environmental Science and Technology
Volume	58
Issue number	50
DOIs	https://doi.org/10.1021/acs.est.4c09642
State	Published - Dec 17 2024

Funding

The study was supported by Grants R01ES027845 and P30ES009089 from the National Institute of Environmental Health Sciences; Grant MOP-84551 from the Canadian Institutes of Health Research; and Canadian Research Chair Grant CRC-950-230570 from the Natural Sciences and Engineering Research Council of Canada. We acknowledge The University of Texas System Rising STARs award to support Y.S.\u2019s research. H.E.L.\u2019s time was supported by K99ES034086 from the NIEHS. We appreciate the participation of all GESTation and Environment Cohort Study families and the support of the cohort study staff. We appreciate Abigail Rauso, Tessa R. Bloomquist, and Peter Meyn for performing stool DNA and RNA extraction and shotgun metagenome and metatranscriptome sequencing as well as Fe\u0301lix Hardy for measuring metal concentrations in stool. Figure 1 and the graphic abstract were created with bioRender.com. The study was supported by Grants R01ES027845 and P30ES009089 from the National Institute of Environmental Health Sciences; Grant MOP-84551 from the Canadian Institutes of Health Research; and Canadian Research Chair Grant CRC-950-230570 from the Natural Sciences and Engineering Research Council of Canada. We acknowledge The University of Texas System Rising STARs award to support Y.S.\u2019s research. H.E.L.\u2019s time was supported by K99ES034086 from the NIEHS. We appreciate the participation of all GESTation and Environment Cohort Study families and the support of the cohort study staff. We appreciate Abigail Rauso, Tessa R. Bloomquist, and Peter Meyn for performing stool DNA and RNA extraction and shotgun metagenome and metatranscriptome sequencing as well as Fe\u0301lix Hardy for measuring metal concentrations in stool. and the graphic abstract were created with bioRender.com .

Keywords

metagenome
metal exposures
metatranscriptome
multiomics
pediatric gut microbiome

ASJC Scopus subject areas

General Chemistry
Environmental Chemistry

Access to Document

10.1021/acs.est.4c09642

Cite this

Gao, F., Shen, Y., Wu, H., Laue, H. E., Lau, F. K., Gillet, V., Lai, Y., Shrubsole, M. J., Prada, D., Zhang, W., Liu, Z., Bellenger, J. P., Takser, L., & Baccarelli, A. A. (2024). Associations of Stool Metal Exposures with Childhood Gut Microbiome Multiomics Profiles in a Prospective Birth Cohort Study. Environmental Science and Technology, 58(50), 22053-22063. https://doi.org/10.1021/acs.est.4c09642

@article{9874114c821b42f383a16ec5685883a8,

title = "Associations of Stool Metal Exposures with Childhood Gut Microbiome Multiomics Profiles in a Prospective Birth Cohort Study",

abstract = "Metal exposures are closely related to childhood developmental health. However, their effects on the childhood gut microbiome, which also impacts health, are largely unexplored using microbiome multiomics including the metagenome and metatranscriptome. This study examined the associations of fecal profiles of metal/element exposures with gut microbiome species and active functional pathways in 8- to 12-year-old children (N = 116) participating in the GESTation and Environment (GESTE) cohort study. We analyzed 19 stool metal and element concentrations (B, Na, Mg, Al, K, Ca, V, Cr, Mn, Fe, Co, Ni, Cu, Zn, As, Mo, Cd, Ba, and Pb). Covariate-adjusted linear regression models identified several significant microbiome associations with continuous stool metal/element concentrations. For instance, Zn was positively associated with Turicibacter sanguinis (coef = 1.354, q-value = 0.039) and negatively associated with Eubacterium eligens (coef = −0.794, q-value = 0.044). Higher concentrations of Cd were associated with lower Eubacterium eligens (coef = −0.774, q-value = 0.045). Additionally, a total of 490 significant functional pathways such as biosynthesis and degradation/utilization/assimilation were identified, corresponding to different functions, including amino acid synthesis and carbohydrate degradation. Our results suggest links among metal exposures, pediatric gut microbiome multiomics, and potential health implications. Future work will further explore their relation to childhood health.",

keywords = "metagenome, metal exposures, metatranscriptome, multiomics, pediatric gut microbiome",

author = "Feng Gao and Yike Shen and Haotian Wu and Laue, {Hannah E.} and Lau, {Fion K.} and Virginie Gillet and Yunjia Lai and Shrubsole, {Martha J.} and Diddier Prada and Wei Zhang and Zhonghua Liu and Bellenger, {Jean Philippe} and Larissa Takser and Baccarelli, {Andrea A.}",

note = "Publisher Copyright: {\textcopyright} 2024 American Chemical Society.",

year = "2024",

month = dec,

day = "17",

doi = "10.1021/acs.est.4c09642",

language = "English (US)",

volume = "58",

pages = "22053--22063",

journal = "Environmental Science and Technology",

issn = "0013-936X",

publisher = "American Chemical Society",

number = "50",

}

Gao, F, Shen, Y, Wu, H, Laue, HE, Lau, FK, Gillet, V, Lai, Y, Shrubsole, MJ, Prada, D, Zhang, W, Liu, Z, Bellenger, JP, Takser, L & Baccarelli, AA 2024, 'Associations of Stool Metal Exposures with Childhood Gut Microbiome Multiomics Profiles in a Prospective Birth Cohort Study', Environmental Science and Technology, vol. 58, no. 50, pp. 22053-22063. https://doi.org/10.1021/acs.est.4c09642

TY - JOUR

T1 - Associations of Stool Metal Exposures with Childhood Gut Microbiome Multiomics Profiles in a Prospective Birth Cohort Study

AU - Gao, Feng

AU - Shen, Yike

AU - Wu, Haotian

AU - Laue, Hannah E.

AU - Lau, Fion K.

AU - Gillet, Virginie

AU - Lai, Yunjia

AU - Shrubsole, Martha J.

AU - Prada, Diddier

AU - Zhang, Wei

AU - Liu, Zhonghua

AU - Bellenger, Jean Philippe

AU - Takser, Larissa

AU - Baccarelli, Andrea A.

PY - 2024/12/17

Y1 - 2024/12/17

N2 - Metal exposures are closely related to childhood developmental health. However, their effects on the childhood gut microbiome, which also impacts health, are largely unexplored using microbiome multiomics including the metagenome and metatranscriptome. This study examined the associations of fecal profiles of metal/element exposures with gut microbiome species and active functional pathways in 8- to 12-year-old children (N = 116) participating in the GESTation and Environment (GESTE) cohort study. We analyzed 19 stool metal and element concentrations (B, Na, Mg, Al, K, Ca, V, Cr, Mn, Fe, Co, Ni, Cu, Zn, As, Mo, Cd, Ba, and Pb). Covariate-adjusted linear regression models identified several significant microbiome associations with continuous stool metal/element concentrations. For instance, Zn was positively associated with Turicibacter sanguinis (coef = 1.354, q-value = 0.039) and negatively associated with Eubacterium eligens (coef = −0.794, q-value = 0.044). Higher concentrations of Cd were associated with lower Eubacterium eligens (coef = −0.774, q-value = 0.045). Additionally, a total of 490 significant functional pathways such as biosynthesis and degradation/utilization/assimilation were identified, corresponding to different functions, including amino acid synthesis and carbohydrate degradation. Our results suggest links among metal exposures, pediatric gut microbiome multiomics, and potential health implications. Future work will further explore their relation to childhood health.

AB - Metal exposures are closely related to childhood developmental health. However, their effects on the childhood gut microbiome, which also impacts health, are largely unexplored using microbiome multiomics including the metagenome and metatranscriptome. This study examined the associations of fecal profiles of metal/element exposures with gut microbiome species and active functional pathways in 8- to 12-year-old children (N = 116) participating in the GESTation and Environment (GESTE) cohort study. We analyzed 19 stool metal and element concentrations (B, Na, Mg, Al, K, Ca, V, Cr, Mn, Fe, Co, Ni, Cu, Zn, As, Mo, Cd, Ba, and Pb). Covariate-adjusted linear regression models identified several significant microbiome associations with continuous stool metal/element concentrations. For instance, Zn was positively associated with Turicibacter sanguinis (coef = 1.354, q-value = 0.039) and negatively associated with Eubacterium eligens (coef = −0.794, q-value = 0.044). Higher concentrations of Cd were associated with lower Eubacterium eligens (coef = −0.774, q-value = 0.045). Additionally, a total of 490 significant functional pathways such as biosynthesis and degradation/utilization/assimilation were identified, corresponding to different functions, including amino acid synthesis and carbohydrate degradation. Our results suggest links among metal exposures, pediatric gut microbiome multiomics, and potential health implications. Future work will further explore their relation to childhood health.

KW - metagenome

KW - metal exposures

KW - metatranscriptome

KW - multiomics

KW - pediatric gut microbiome

UR - http://www.scopus.com/inward/record.url?scp=85211027866&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85211027866&partnerID=8YFLogxK

U2 - 10.1021/acs.est.4c09642

DO - 10.1021/acs.est.4c09642

M3 - Article

C2 - 39630952

AN - SCOPUS:85211027866

SN - 0013-936X

VL - 58

SP - 22053

EP - 22063

JO - Environmental Science and Technology

JF - Environmental Science and Technology

IS - 50

ER -

Associations of Stool Metal Exposures with Childhood Gut Microbiome Multiomics Profiles in a Prospective Birth Cohort Study

Abstract

Funding

Keywords

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Cite this