Bacterial–fungal interactions in the neonatal gut influence asthma outcomes later in life

Bacterial members of the infant gut microbiota and bacterial-derived short-chain fatty acids (SCFAs) have been shown to be protective against childhood asthma, but a role for the fungal microbiota in asthma etiology remains poorly defined. We recently reported an association between overgrowth of th...

Full description

Bibliographic Details
Main Authors: Rozlyn CT Boutin, Charisse Petersen, Sarah E Woodward, Antonio Serapio-Palacios, Tahereh Bozorgmehr, Rachelle Loo, Alina Chalanuchpong, Mihai Cirstea, Bernard Lo, Kelsey E Huus, Weronika Barcik, Meghan B Azad, Allan B Becker, Piush J Mandhane, Theo J Moraes, Malcolm R Sears, Padmaja Subbarao, Kelly M McNagny, Stuart E Turvey, B Brett Finlay
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-04-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/67740
id doaj-3528669980c6489896b4811b6c6f4526
record_format Article
collection DOAJ
language English
format Article
sources DOAJ
author Rozlyn CT Boutin
Charisse Petersen
Sarah E Woodward
Antonio Serapio-Palacios
Tahereh Bozorgmehr
Rachelle Loo
Alina Chalanuchpong
Mihai Cirstea
Bernard Lo
Kelsey E Huus
Weronika Barcik
Meghan B Azad
Allan B Becker
Piush J Mandhane
Theo J Moraes
Malcolm R Sears
Padmaja Subbarao
Kelly M McNagny
Stuart E Turvey
B Brett Finlay
spellingShingle Rozlyn CT Boutin
Charisse Petersen
Sarah E Woodward
Antonio Serapio-Palacios
Tahereh Bozorgmehr
Rachelle Loo
Alina Chalanuchpong
Mihai Cirstea
Bernard Lo
Kelsey E Huus
Weronika Barcik
Meghan B Azad
Allan B Becker
Piush J Mandhane
Theo J Moraes
Malcolm R Sears
Padmaja Subbarao
Kelly M McNagny
Stuart E Turvey
B Brett Finlay
Bacterial–fungal interactions in the neonatal gut influence asthma outcomes later in life
eLife
pichia kudriavzevii
microbiota
asthma
mycobiota
author_facet Rozlyn CT Boutin
Charisse Petersen
Sarah E Woodward
Antonio Serapio-Palacios
Tahereh Bozorgmehr
Rachelle Loo
Alina Chalanuchpong
Mihai Cirstea
Bernard Lo
Kelsey E Huus
Weronika Barcik
Meghan B Azad
Allan B Becker
Piush J Mandhane
Theo J Moraes
Malcolm R Sears
Padmaja Subbarao
Kelly M McNagny
Stuart E Turvey
B Brett Finlay
author_sort Rozlyn CT Boutin
title Bacterial–fungal interactions in the neonatal gut influence asthma outcomes later in life
title_short Bacterial–fungal interactions in the neonatal gut influence asthma outcomes later in life
title_full Bacterial–fungal interactions in the neonatal gut influence asthma outcomes later in life
title_fullStr Bacterial–fungal interactions in the neonatal gut influence asthma outcomes later in life
title_full_unstemmed Bacterial–fungal interactions in the neonatal gut influence asthma outcomes later in life
title_sort bacterial–fungal interactions in the neonatal gut influence asthma outcomes later in life
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2021-04-01
description Bacterial members of the infant gut microbiota and bacterial-derived short-chain fatty acids (SCFAs) have been shown to be protective against childhood asthma, but a role for the fungal microbiota in asthma etiology remains poorly defined. We recently reported an association between overgrowth of the yeast Pichia kudriavzevii in the gut microbiota of Ecuadorian infants and increased asthma risk. In the present study, we replicated these findings in Canadian infants and investigated a causal association between early life gut fungal dysbiosis and later allergic airway disease (AAD). In a mouse model, we demonstrate that overgrowth of P. kudriavzevii within the neonatal gut exacerbates features of type-2 and -17 inflammation during AAD later in life. We further show that P. kudriavzevii growth and adherence to gut epithelial cells are altered by SCFAs. Collectively, our results underscore the potential for leveraging inter-kingdom interactions when designing putative microbiota-based asthma therapeutics.
topic pichia kudriavzevii
microbiota
asthma
mycobiota
url https://elifesciences.org/articles/67740
work_keys_str_mv AT rozlynctboutin bacterialfungalinteractionsintheneonatalgutinfluenceasthmaoutcomeslaterinlife
AT charissepetersen bacterialfungalinteractionsintheneonatalgutinfluenceasthmaoutcomeslaterinlife
AT sarahewoodward bacterialfungalinteractionsintheneonatalgutinfluenceasthmaoutcomeslaterinlife
AT antonioserapiopalacios bacterialfungalinteractionsintheneonatalgutinfluenceasthmaoutcomeslaterinlife
AT taherehbozorgmehr bacterialfungalinteractionsintheneonatalgutinfluenceasthmaoutcomeslaterinlife
AT rachelleloo bacterialfungalinteractionsintheneonatalgutinfluenceasthmaoutcomeslaterinlife
AT alinachalanuchpong bacterialfungalinteractionsintheneonatalgutinfluenceasthmaoutcomeslaterinlife
AT mihaicirstea bacterialfungalinteractionsintheneonatalgutinfluenceasthmaoutcomeslaterinlife
AT bernardlo bacterialfungalinteractionsintheneonatalgutinfluenceasthmaoutcomeslaterinlife
AT kelseyehuus bacterialfungalinteractionsintheneonatalgutinfluenceasthmaoutcomeslaterinlife
AT weronikabarcik bacterialfungalinteractionsintheneonatalgutinfluenceasthmaoutcomeslaterinlife
AT meghanbazad bacterialfungalinteractionsintheneonatalgutinfluenceasthmaoutcomeslaterinlife
AT allanbbecker bacterialfungalinteractionsintheneonatalgutinfluenceasthmaoutcomeslaterinlife
AT piushjmandhane bacterialfungalinteractionsintheneonatalgutinfluenceasthmaoutcomeslaterinlife
AT theojmoraes bacterialfungalinteractionsintheneonatalgutinfluenceasthmaoutcomeslaterinlife
AT malcolmrsears bacterialfungalinteractionsintheneonatalgutinfluenceasthmaoutcomeslaterinlife
AT padmajasubbarao bacterialfungalinteractionsintheneonatalgutinfluenceasthmaoutcomeslaterinlife
AT kellymmcnagny bacterialfungalinteractionsintheneonatalgutinfluenceasthmaoutcomeslaterinlife
AT stuarteturvey bacterialfungalinteractionsintheneonatalgutinfluenceasthmaoutcomeslaterinlife
AT bbrettfinlay bacterialfungalinteractionsintheneonatalgutinfluenceasthmaoutcomeslaterinlife
_version_ 1721457370354155520
spelling doaj-3528669980c6489896b4811b6c6f45262021-05-05T22:59:30ZengeLife Sciences Publications LtdeLife2050-084X2021-04-011010.7554/eLife.67740Bacterial–fungal interactions in the neonatal gut influence asthma outcomes later in lifeRozlyn CT Boutin0https://orcid.org/0000-0003-1598-0104Charisse Petersen1Sarah E Woodward2https://orcid.org/0000-0002-6688-0595Antonio Serapio-Palacios3Tahereh Bozorgmehr4Rachelle Loo5Alina Chalanuchpong6Mihai Cirstea7https://orcid.org/0000-0003-4900-6385Bernard Lo8Kelsey E Huus9Weronika Barcik10Meghan B Azad11Allan B Becker12Piush J Mandhane13Theo J Moraes14Malcolm R Sears15Padmaja Subbarao16Kelly M McNagny17https://orcid.org/0000-0003-4737-3499Stuart E Turvey18B Brett Finlay19https://orcid.org/0000-0001-5303-6128Department of Microbiology and Immunology, University of British Columbia, Vancouver, Canada; Michael Smith Laboratories, University of British Columbia, Vancouver, CanadaMichael Smith Laboratories, University of British Columbia, Vancouver, CanadaDepartment of Microbiology and Immunology, University of British Columbia, Vancouver, Canada; Michael Smith Laboratories, University of British Columbia, Vancouver, CanadaMichael Smith Laboratories, University of British Columbia, Vancouver, CanadaMichael Smith Laboratories, University of British Columbia, Vancouver, CanadaDepartment of Microbiology and Immunology, University of British Columbia, Vancouver, Canada; Michael Smith Laboratories, University of British Columbia, Vancouver, CanadaDepartment of Microbiology and Immunology, University of British Columbia, Vancouver, Canada; Michael Smith Laboratories, University of British Columbia, Vancouver, CanadaDepartment of Microbiology and Immunology, University of British Columbia, Vancouver, Canada; Michael Smith Laboratories, University of British Columbia, Vancouver, CanadaDepartment of Microbiology and Immunology, University of British Columbia, Vancouver, CanadaDepartment of Microbiology and Immunology, University of British Columbia, Vancouver, Canada; Michael Smith Laboratories, University of British Columbia, Vancouver, CanadaMichael Smith Laboratories, University of British Columbia, Vancouver, CanadaChildren’s Hospital Research Institute of Manitoba and Department of Pediatrics and Child Health, University of Manitoba, WinnipegMB, CanadaChildren’s Hospital Research Institute of Manitoba and Department of Pediatrics and Child Health, University of Manitoba, WinnipegMB, CanadaDepartment of Pediatrics, University of Alberta, Edmonton, Canada; School of Public Health, University of Alberta, Edmonton, CanadaThe Hospital for Sick Children, Toronto, CanadaDepartment of Medicine, McMaster University, Hamilton, CanadaThe Hospital for Sick Children, Toronto, Canada; Department of Pediatrics, University of Toronto, Toronto, CanadaDepartment of Biomedical Engineering, University of British Columbia, Vancouver, Canada; Department of Medical Genetics University of British Columbia, Vancouver, CanadaDepartment of Microbiology and Immunology, University of British Columbia, Vancouver, Canada; Department of Pediatrics, University of British Columbia, Vancouver, CanadaDepartment of Microbiology and Immunology, University of British Columbia, Vancouver, Canada; Michael Smith Laboratories, University of British Columbia, Vancouver, Canada; Department of Biochemistry and Molecular Biology, University of British Columbia, Vancouver, CanadaBacterial members of the infant gut microbiota and bacterial-derived short-chain fatty acids (SCFAs) have been shown to be protective against childhood asthma, but a role for the fungal microbiota in asthma etiology remains poorly defined. We recently reported an association between overgrowth of the yeast Pichia kudriavzevii in the gut microbiota of Ecuadorian infants and increased asthma risk. In the present study, we replicated these findings in Canadian infants and investigated a causal association between early life gut fungal dysbiosis and later allergic airway disease (AAD). In a mouse model, we demonstrate that overgrowth of P. kudriavzevii within the neonatal gut exacerbates features of type-2 and -17 inflammation during AAD later in life. We further show that P. kudriavzevii growth and adherence to gut epithelial cells are altered by SCFAs. Collectively, our results underscore the potential for leveraging inter-kingdom interactions when designing putative microbiota-based asthma therapeutics.https://elifesciences.org/articles/67740pichia kudriavzeviimicrobiotaasthmamycobiota