Bacterial, fungal, and interkingdom microbiome features of exclusively breastfeeding dyads are associated with infant age, antibiotic exposure, and birth mode

Tim Heisel; Abigail J. Johnson; Sara J Gonia; Abrielle Dillon; Emily Skalla; Jacob Haapala; Katherine M Jacobs; Emily M Nagel; Stephanie Pierce; David Fields; Ellen Demerath; Dan Knights; Cheryl A Gale

doi:10.3389/fmicb.2022.1050574

Bacterial, fungal, and interkingdom microbiome features of exclusively breastfeeding dyads are associated with infant age, antibiotic exposure, and birth mode

Tim Heisel, Abigail J. Johnson, Sara J Gonia, Abrielle Dillon, Emily Skalla, Jacob Haapala, Katherine M Jacobs, Emily M Nagel, Stephanie Pierce, David Fields, Ellen Demerath, Dan Knights, Cheryl A Gale

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

Abstract

The composition and function of early life gut bacterial communities (microbiomes) have been proposed to modulate health for the long term. In addition to bacteria, fungi (mycobiomes) also colonize the early life gut and have been implicated in health disorders such as asthma and obesity. Despite the potential importance of mycobiomes in health, there has been a lack of study regarding fungi and their interkingdom interactions with bacteria during infancy. The goal of this study was to obtain a more complete understanding of microbial communities thought to be relevant for the early life programming of health. Breastmilk and infant feces were obtained from a unique cohort of healthy, exclusively breastfeeding dyads recruited as part of the Mothers and Infants Linked for Healthy Growth (MILk) study with microbial taxa characterized using amplicon-based sequencing approaches. Bacterial and fungal communities in breastmilk were both distinct from those of infant feces, consistent with niche-specific microbial community development. Nevertheless, overlap was observed among sample types (breastmilk, 1-month feces, 6-month feces) with respect to the taxa that were the most prevalent and abundant. Self-reported antibacterial antibiotic exposure was associated with micro- as well as mycobiome variation, which depended upon the subject receiving antibiotics (mother or infant), timing of exposure (prenatal, peri- or postpartum), and sample type. In addition, birth mode was associated with bacterial and fungal community variation in infant feces, but not breastmilk. Correlations between bacterial and fungal taxa abundances were identified in all sample types. For infant feces, congruency between bacterial and fungal communities was higher for older infants, consistent with the idea of co-maturation of bacterial and fungal gut communities. Interkingdom connectedness also tended to be higher in older infants. Additionally, higher interkingdom connectedness was associated with Cesarean section birth and with antibiotic exposure for microbial communities of both breastmilk and infant feces. Overall, these results implicate infant age, birth mode, and antibiotic exposure in bacterial, fungal and interkingdom relationship variation in early-life-relevant microbiomes, expanding the current literature beyond bacteria.

Original language	English (US)
Article number	1050574
Journal	Frontiers in Microbiology
Volume	13
DOIs	https://doi.org/10.3389/fmicb.2022.1050574
State	Published - Nov 17 2022

Bibliographical note

Funding Information:
The authors acknowledge and thank all the women and health care providers who contributed to the MILk study. The authors also acknowledge University of Minnesota Genomics Center staff (Daryl Gohl and Jon Badalamenti) and Gabriel Al-Ghalith for providing technical advice with respect to sequencing approaches and microbiome analyses, respectively. We also acknowledge the valuable assistance of Neely Miller and Kristin Sandness and the resources of the Center for Neurobehavioral Development, Rebecca Hollister from the Center for Pediatric Obesity at the University of Minnesota, the Clinical and Translational Research Services support team at the Clinical and Translational Science Institute at the University of Minnesota (supported by grant number UL1TR002494 from the National Institutes of Health’s National Center for Advancing Translational Sciences), and Elisabeth Seburg and the data collection and information technology team at the HealthPartners Institute. The authors also acknowledge use of the following resources: Diet*Calc Analysis Program, Version 1.5.0. National Cancer Institute, Epidemiology and Genomics Research Program, October 2012. Diet History Questionnaire, Version 2.0. National Institutes of Health, Epidemiology and Genomics Research Program, National Cancer Institute, 2010. DHQ Nutrient Database. dhq2.database.092914.csv. National Cancer Institute, Epidemiology and Genomics Research Program.

Funding Information:
The authors acknowledge and thank all the women and health care providers who contributed to the MILk study. The authors also acknowledge University of Minnesota Genomics Center staff (Daryl Gohl and Jon Badalamenti) and Gabriel Al-Ghalith for providing technical advice with respect to sequencing approaches and microbiome analyses, respectively. We also acknowledge the valuable assistance of Neely Miller and Kristin Sandness and the resources of the Center for Neurobehavioral Development, Rebecca Hollister from the Center for Pediatric Obesity at the University of Minnesota, the Clinical and Translational Research Services support team at the Clinical and Translational Science Institute at the University of Minnesota (supported by grant number UL1TR002494 from the National Institutes of Health’s National Center for Advancing Translational Sciences), and Elisabeth Seburg and the data collection and information technology team at the HealthPartners Institute. The authors also acknowledge use of the following resources: Diet*Calc Analysis Program, Version 1.5.0. National Cancer Institute, Epidemiology and Genomics Research Program, October 2012. Diet History Questionnaire, Version 2.0. National Institutes of Health, Epidemiology and Genomics Research Program, National Cancer Institute, 2010. DHQ Nutrient Database. dhq2.database.092914.csv. National Cancer Institute, Epidemiology and Genomics Research Program.

Funding Information:
The MILk Study which provided the cohort and milk samples for this study was supported by NIH/NICHD grant (R01HD080444) to ED and DF; microbiome and mycobiome analyses of cohort biospecimens was supported by a University of Minnesota Masonic Children’s Hospital Research Fund Award to CG, ED, and DK, a University of Minnesota Office of Academic and Clinical Affairs Faculty Research Development Grant to CG, ED, KJ, and DK and NIH grants (R21AI139730, R21HD099473) to CG and DK. EN was supported by NIH/NIDDK fellowship grant (T32DK083250) and K99/R00 K99HD108276.

Publisher Copyright:
Copyright © 2022 Heisel, Johnson, Gonia, Dillon, Skalla, Haapala, Jacobs, Nagel, Pierce, Fields, Demerath, Knights and Gale.

Keywords

bacteria
breastmilk
fungi
infant gut
interkingdom interactions
microbial community variation
microbiome
mycobiome

PubMed: MeSH publication types

Journal Article

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.3389/fmicb.2022.1050574

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Heisel, T., Johnson, A. J., Gonia, S. J., Dillon, A., Skalla, E., Haapala, J., Jacobs, K. M., Nagel, E. M., Pierce, S., Fields, D., Demerath, E., Knights, D., & Gale, C. A. (2022). Bacterial, fungal, and interkingdom microbiome features of exclusively breastfeeding dyads are associated with infant age, antibiotic exposure, and birth mode. Frontiers in Microbiology, 13, [1050574]. https://doi.org/10.3389/fmicb.2022.1050574

Heisel, T , Johnson, AJ , Gonia, SJ, Dillon, A, Skalla, E, Haapala, J, Jacobs, KM, Nagel, EM, Pierce, S, Fields, D, Demerath, E , Knights, D & Gale, CA 2022, 'Bacterial, fungal, and interkingdom microbiome features of exclusively breastfeeding dyads are associated with infant age, antibiotic exposure, and birth mode', Frontiers in Microbiology, vol. 13, 1050574. https://doi.org/10.3389/fmicb.2022.1050574

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title = "Bacterial, fungal, and interkingdom microbiome features of exclusively breastfeeding dyads are associated with infant age, antibiotic exposure, and birth mode",

abstract = "The composition and function of early life gut bacterial communities (microbiomes) have been proposed to modulate health for the long term. In addition to bacteria, fungi (mycobiomes) also colonize the early life gut and have been implicated in health disorders such as asthma and obesity. Despite the potential importance of mycobiomes in health, there has been a lack of study regarding fungi and their interkingdom interactions with bacteria during infancy. The goal of this study was to obtain a more complete understanding of microbial communities thought to be relevant for the early life programming of health. Breastmilk and infant feces were obtained from a unique cohort of healthy, exclusively breastfeeding dyads recruited as part of the Mothers and Infants Linked for Healthy Growth (MILk) study with microbial taxa characterized using amplicon-based sequencing approaches. Bacterial and fungal communities in breastmilk were both distinct from those of infant feces, consistent with niche-specific microbial community development. Nevertheless, overlap was observed among sample types (breastmilk, 1-month feces, 6-month feces) with respect to the taxa that were the most prevalent and abundant. Self-reported antibacterial antibiotic exposure was associated with micro- as well as mycobiome variation, which depended upon the subject receiving antibiotics (mother or infant), timing of exposure (prenatal, peri- or postpartum), and sample type. In addition, birth mode was associated with bacterial and fungal community variation in infant feces, but not breastmilk. Correlations between bacterial and fungal taxa abundances were identified in all sample types. For infant feces, congruency between bacterial and fungal communities was higher for older infants, consistent with the idea of co-maturation of bacterial and fungal gut communities. Interkingdom connectedness also tended to be higher in older infants. Additionally, higher interkingdom connectedness was associated with Cesarean section birth and with antibiotic exposure for microbial communities of both breastmilk and infant feces. Overall, these results implicate infant age, birth mode, and antibiotic exposure in bacterial, fungal and interkingdom relationship variation in early-life-relevant microbiomes, expanding the current literature beyond bacteria.",

keywords = "bacteria, breastmilk, fungi, infant gut, interkingdom interactions, microbial community variation, microbiome, mycobiome",

author = "Tim Heisel and Johnson, {Abigail J.} and Gonia, {Sara J} and Abrielle Dillon and Emily Skalla and Jacob Haapala and Jacobs, {Katherine M} and Nagel, {Emily M} and Stephanie Pierce and David Fields and Ellen Demerath and Dan Knights and Gale, {Cheryl A}",

note = "Funding Information: The authors acknowledge and thank all the women and health care providers who contributed to the MILk study. The authors also acknowledge University of Minnesota Genomics Center staff (Daryl Gohl and Jon Badalamenti) and Gabriel Al-Ghalith for providing technical advice with respect to sequencing approaches and microbiome analyses, respectively. We also acknowledge the valuable assistance of Neely Miller and Kristin Sandness and the resources of the Center for Neurobehavioral Development, Rebecca Hollister from the Center for Pediatric Obesity at the University of Minnesota, the Clinical and Translational Research Services support team at the Clinical and Translational Science Institute at the University of Minnesota (supported by grant number UL1TR002494 from the National Institutes of Health{\textquoteright}s National Center for Advancing Translational Sciences), and Elisabeth Seburg and the data collection and information technology team at the HealthPartners Institute. The authors also acknowledge use of the following resources: Diet*Calc Analysis Program, Version 1.5.0. National Cancer Institute, Epidemiology and Genomics Research Program, October 2012. Diet History Questionnaire, Version 2.0. National Institutes of Health, Epidemiology and Genomics Research Program, National Cancer Institute, 2010. DHQ Nutrient Database. dhq2.database.092914.csv. National Cancer Institute, Epidemiology and Genomics Research Program. Funding Information: The authors acknowledge and thank all the women and health care providers who contributed to the MILk study. The authors also acknowledge University of Minnesota Genomics Center staff (Daryl Gohl and Jon Badalamenti) and Gabriel Al-Ghalith for providing technical advice with respect to sequencing approaches and microbiome analyses, respectively. We also acknowledge the valuable assistance of Neely Miller and Kristin Sandness and the resources of the Center for Neurobehavioral Development, Rebecca Hollister from the Center for Pediatric Obesity at the University of Minnesota, the Clinical and Translational Research Services support team at the Clinical and Translational Science Institute at the University of Minnesota (supported by grant number UL1TR002494 from the National Institutes of Health{\textquoteright}s National Center for Advancing Translational Sciences), and Elisabeth Seburg and the data collection and information technology team at the HealthPartners Institute. The authors also acknowledge use of the following resources: Diet*Calc Analysis Program, Version 1.5.0. National Cancer Institute, Epidemiology and Genomics Research Program, October 2012. Diet History Questionnaire, Version 2.0. National Institutes of Health, Epidemiology and Genomics Research Program, National Cancer Institute, 2010. DHQ Nutrient Database. dhq2.database.092914.csv. National Cancer Institute, Epidemiology and Genomics Research Program. Funding Information: The MILk Study which provided the cohort and milk samples for this study was supported by NIH/NICHD grant (R01HD080444) to ED and DF; microbiome and mycobiome analyses of cohort biospecimens was supported by a University of Minnesota Masonic Children{\textquoteright}s Hospital Research Fund Award to CG, ED, and DK, a University of Minnesota Office of Academic and Clinical Affairs Faculty Research Development Grant to CG, ED, KJ, and DK and NIH grants (R21AI139730, R21HD099473) to CG and DK. EN was supported by NIH/NIDDK fellowship grant (T32DK083250) and K99/R00 K99HD108276. Publisher Copyright: Copyright {\textcopyright} 2022 Heisel, Johnson, Gonia, Dillon, Skalla, Haapala, Jacobs, Nagel, Pierce, Fields, Demerath, Knights and Gale.",

year = "2022",

month = nov,

day = "17",

doi = "10.3389/fmicb.2022.1050574",

language = "English (US)",

volume = "13",

journal = "Frontiers in Microbiology",

issn = "1664-302X",

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TY - JOUR

T1 - Bacterial, fungal, and interkingdom microbiome features of exclusively breastfeeding dyads are associated with infant age, antibiotic exposure, and birth mode

AU - Heisel, Tim

AU - Johnson, Abigail J.

AU - Gonia, Sara J

AU - Dillon, Abrielle

AU - Skalla, Emily

AU - Haapala, Jacob

AU - Jacobs, Katherine M

AU - Nagel, Emily M

AU - Pierce, Stephanie

AU - Fields, David

AU - Demerath, Ellen

AU - Knights, Dan

AU - Gale, Cheryl A

N1 - Funding Information: The authors acknowledge and thank all the women and health care providers who contributed to the MILk study. The authors also acknowledge University of Minnesota Genomics Center staff (Daryl Gohl and Jon Badalamenti) and Gabriel Al-Ghalith for providing technical advice with respect to sequencing approaches and microbiome analyses, respectively. We also acknowledge the valuable assistance of Neely Miller and Kristin Sandness and the resources of the Center for Neurobehavioral Development, Rebecca Hollister from the Center for Pediatric Obesity at the University of Minnesota, the Clinical and Translational Research Services support team at the Clinical and Translational Science Institute at the University of Minnesota (supported by grant number UL1TR002494 from the National Institutes of Health’s National Center for Advancing Translational Sciences), and Elisabeth Seburg and the data collection and information technology team at the HealthPartners Institute. The authors also acknowledge use of the following resources: Diet*Calc Analysis Program, Version 1.5.0. National Cancer Institute, Epidemiology and Genomics Research Program, October 2012. Diet History Questionnaire, Version 2.0. National Institutes of Health, Epidemiology and Genomics Research Program, National Cancer Institute, 2010. DHQ Nutrient Database. dhq2.database.092914.csv. National Cancer Institute, Epidemiology and Genomics Research Program. Funding Information: The authors acknowledge and thank all the women and health care providers who contributed to the MILk study. The authors also acknowledge University of Minnesota Genomics Center staff (Daryl Gohl and Jon Badalamenti) and Gabriel Al-Ghalith for providing technical advice with respect to sequencing approaches and microbiome analyses, respectively. We also acknowledge the valuable assistance of Neely Miller and Kristin Sandness and the resources of the Center for Neurobehavioral Development, Rebecca Hollister from the Center for Pediatric Obesity at the University of Minnesota, the Clinical and Translational Research Services support team at the Clinical and Translational Science Institute at the University of Minnesota (supported by grant number UL1TR002494 from the National Institutes of Health’s National Center for Advancing Translational Sciences), and Elisabeth Seburg and the data collection and information technology team at the HealthPartners Institute. The authors also acknowledge use of the following resources: Diet*Calc Analysis Program, Version 1.5.0. National Cancer Institute, Epidemiology and Genomics Research Program, October 2012. Diet History Questionnaire, Version 2.0. National Institutes of Health, Epidemiology and Genomics Research Program, National Cancer Institute, 2010. DHQ Nutrient Database. dhq2.database.092914.csv. National Cancer Institute, Epidemiology and Genomics Research Program. Funding Information: The MILk Study which provided the cohort and milk samples for this study was supported by NIH/NICHD grant (R01HD080444) to ED and DF; microbiome and mycobiome analyses of cohort biospecimens was supported by a University of Minnesota Masonic Children’s Hospital Research Fund Award to CG, ED, and DK, a University of Minnesota Office of Academic and Clinical Affairs Faculty Research Development Grant to CG, ED, KJ, and DK and NIH grants (R21AI139730, R21HD099473) to CG and DK. EN was supported by NIH/NIDDK fellowship grant (T32DK083250) and K99/R00 K99HD108276. Publisher Copyright: Copyright © 2022 Heisel, Johnson, Gonia, Dillon, Skalla, Haapala, Jacobs, Nagel, Pierce, Fields, Demerath, Knights and Gale.

PY - 2022/11/17

Y1 - 2022/11/17

N2 - The composition and function of early life gut bacterial communities (microbiomes) have been proposed to modulate health for the long term. In addition to bacteria, fungi (mycobiomes) also colonize the early life gut and have been implicated in health disorders such as asthma and obesity. Despite the potential importance of mycobiomes in health, there has been a lack of study regarding fungi and their interkingdom interactions with bacteria during infancy. The goal of this study was to obtain a more complete understanding of microbial communities thought to be relevant for the early life programming of health. Breastmilk and infant feces were obtained from a unique cohort of healthy, exclusively breastfeeding dyads recruited as part of the Mothers and Infants Linked for Healthy Growth (MILk) study with microbial taxa characterized using amplicon-based sequencing approaches. Bacterial and fungal communities in breastmilk were both distinct from those of infant feces, consistent with niche-specific microbial community development. Nevertheless, overlap was observed among sample types (breastmilk, 1-month feces, 6-month feces) with respect to the taxa that were the most prevalent and abundant. Self-reported antibacterial antibiotic exposure was associated with micro- as well as mycobiome variation, which depended upon the subject receiving antibiotics (mother or infant), timing of exposure (prenatal, peri- or postpartum), and sample type. In addition, birth mode was associated with bacterial and fungal community variation in infant feces, but not breastmilk. Correlations between bacterial and fungal taxa abundances were identified in all sample types. For infant feces, congruency between bacterial and fungal communities was higher for older infants, consistent with the idea of co-maturation of bacterial and fungal gut communities. Interkingdom connectedness also tended to be higher in older infants. Additionally, higher interkingdom connectedness was associated with Cesarean section birth and with antibiotic exposure for microbial communities of both breastmilk and infant feces. Overall, these results implicate infant age, birth mode, and antibiotic exposure in bacterial, fungal and interkingdom relationship variation in early-life-relevant microbiomes, expanding the current literature beyond bacteria.

AB - The composition and function of early life gut bacterial communities (microbiomes) have been proposed to modulate health for the long term. In addition to bacteria, fungi (mycobiomes) also colonize the early life gut and have been implicated in health disorders such as asthma and obesity. Despite the potential importance of mycobiomes in health, there has been a lack of study regarding fungi and their interkingdom interactions with bacteria during infancy. The goal of this study was to obtain a more complete understanding of microbial communities thought to be relevant for the early life programming of health. Breastmilk and infant feces were obtained from a unique cohort of healthy, exclusively breastfeeding dyads recruited as part of the Mothers and Infants Linked for Healthy Growth (MILk) study with microbial taxa characterized using amplicon-based sequencing approaches. Bacterial and fungal communities in breastmilk were both distinct from those of infant feces, consistent with niche-specific microbial community development. Nevertheless, overlap was observed among sample types (breastmilk, 1-month feces, 6-month feces) with respect to the taxa that were the most prevalent and abundant. Self-reported antibacterial antibiotic exposure was associated with micro- as well as mycobiome variation, which depended upon the subject receiving antibiotics (mother or infant), timing of exposure (prenatal, peri- or postpartum), and sample type. In addition, birth mode was associated with bacterial and fungal community variation in infant feces, but not breastmilk. Correlations between bacterial and fungal taxa abundances were identified in all sample types. For infant feces, congruency between bacterial and fungal communities was higher for older infants, consistent with the idea of co-maturation of bacterial and fungal gut communities. Interkingdom connectedness also tended to be higher in older infants. Additionally, higher interkingdom connectedness was associated with Cesarean section birth and with antibiotic exposure for microbial communities of both breastmilk and infant feces. Overall, these results implicate infant age, birth mode, and antibiotic exposure in bacterial, fungal and interkingdom relationship variation in early-life-relevant microbiomes, expanding the current literature beyond bacteria.

KW - bacteria

KW - breastmilk

KW - fungi

KW - infant gut

KW - interkingdom interactions

KW - microbial community variation

KW - microbiome

KW - mycobiome

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Bacterial, fungal, and interkingdom microbiome features of exclusively breastfeeding dyads are associated with infant age, antibiotic exposure, and birth mode

Abstract

Bibliographical note

Keywords

PubMed: MeSH publication types

UN SDGs

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