Long-term biodiversity intervention shapes health-associated commensal microbiota among urban day-care children.


Journal

Environment international
ISSN: 1873-6750
Titre abrégé: Environ Int
Pays: Netherlands
ID NLM: 7807270

Informations de publication

Date de publication:
12 2021
Historique:
received: 04 06 2021
revised: 17 07 2021
accepted: 30 07 2021
pubmed: 18 8 2021
medline: 21 10 2021
entrez: 17 8 2021
Statut: ppublish

Résumé

In modern urban environments children have a high incidence of inflammatory disorders, including allergies, asthma, and type1 diabetes. The underlying cause of these disorders, according to the biodiversity hypothesis, is an imbalance in immune regulation caused by a weak interaction with environmental microbes. In this 2-year study, we analyzed bacterial community shifts in the soil surface in day-care centers and commensal bacteria inhabiting the mouth, skin, and gut of children. We compared two different day-care environments: standard urban day-care centers and intervention day-care centers. Yards in the latter were amended with biodiverse forest floor vegetation and sod at the beginning of the study. Intervention caused a long-standing increase in the relative abundance of nonpathogenic environmental mycobacteria in the surface soils. Treatment-specific shifts became evident in the community composition of Gammaproteobacteria, Negativicutes, and Bacilli, which jointly accounted for almost 40 and 50% of the taxa on the intervention day-care children's skin and in saliva, respectively. In the year-one skin swabs, richness of Alpha-, Beta-, and Gammaproteobacteria was higher, and the relative abundance of potentially pathogenic bacteria, including Haemophilus parainfluenzae, Streptococcus sp., and Veillonella sp., was lower among children in intervention day-care centers compared with children in standard day-care centers. In the gut, the relative abundance of Clostridium sensu stricto decreased, particularly among the intervention children. This study shows that a 2-year biodiversity intervention shapes human commensal microbiota, including taxa that have been associated with immune regulation. Results indicate that intervention enriched commensal microbiota and suppressed the potentially pathogenic bacteria on the skin. We recommend future studies that expand intervention strategies to immune response and eventually the incidence of immune-mediated diseases.

Sections du résumé

BACKGROUND
In modern urban environments children have a high incidence of inflammatory disorders, including allergies, asthma, and type1 diabetes. The underlying cause of these disorders, according to the biodiversity hypothesis, is an imbalance in immune regulation caused by a weak interaction with environmental microbes. In this 2-year study, we analyzed bacterial community shifts in the soil surface in day-care centers and commensal bacteria inhabiting the mouth, skin, and gut of children. We compared two different day-care environments: standard urban day-care centers and intervention day-care centers. Yards in the latter were amended with biodiverse forest floor vegetation and sod at the beginning of the study.
RESULTS
Intervention caused a long-standing increase in the relative abundance of nonpathogenic environmental mycobacteria in the surface soils. Treatment-specific shifts became evident in the community composition of Gammaproteobacteria, Negativicutes, and Bacilli, which jointly accounted for almost 40 and 50% of the taxa on the intervention day-care children's skin and in saliva, respectively. In the year-one skin swabs, richness of Alpha-, Beta-, and Gammaproteobacteria was higher, and the relative abundance of potentially pathogenic bacteria, including Haemophilus parainfluenzae, Streptococcus sp., and Veillonella sp., was lower among children in intervention day-care centers compared with children in standard day-care centers. In the gut, the relative abundance of Clostridium sensu stricto decreased, particularly among the intervention children.
CONCLUSIONS
This study shows that a 2-year biodiversity intervention shapes human commensal microbiota, including taxa that have been associated with immune regulation. Results indicate that intervention enriched commensal microbiota and suppressed the potentially pathogenic bacteria on the skin. We recommend future studies that expand intervention strategies to immune response and eventually the incidence of immune-mediated diseases.

Identifiants

pubmed: 34403882
pii: S0160-4120(21)00436-0
doi: 10.1016/j.envint.2021.106811
pii:
doi:

Substances chimiques

Soil 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

106811

Investigateurs

Damiano Cerrone (D)
Mira Grönroos (M)
Nan Hui (N)
Iida Mäkelä (I)
Noora Nurminen (N)
Sami Oikarinen (S)
Anirudra Parajuli (A)
Riikka Puhakka (R)
Marja I Roslund (MI)
Mika Saarenpää (M)
Laura Soininen (L)
Yan Sun (Y)
Heli K Vari (HK)
Olli H Laitinen (OH)
Juho Rajaniemi (J)
Heikki Hyöty (H)
Aki Sinkkonen (A)

Informations de copyright

Copyright © 2021. Published by Elsevier Ltd.

Auteurs

Marja I Roslund (MI)

Ecosystems and Environment Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, Niemenkatu 73, FI-15140 Lahti, Finland.

Riikka Puhakka (R)

Ecosystems and Environment Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, Niemenkatu 73, FI-15140 Lahti, Finland.

Noora Nurminen (N)

Faculty of Medicine and Health Technology, Tampere University, Arvo Ylpön katu 34, FI-33520 Tampere, Finland.

Sami Oikarinen (S)

Faculty of Medicine and Health Technology, Tampere University, Arvo Ylpön katu 34, FI-33520 Tampere, Finland.

Nathan Siter (N)

Faculty of Built Environment, Tampere University, Korkeakoulunkatu 5, FI-33720 Tampere, Finland.

Mira Grönroos (M)

Ecosystems and Environment Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, Niemenkatu 73, FI-15140 Lahti, Finland.

Ondřej Cinek (O)

Department of Pediatrics, Second Faculty of Medicine, Charles University, V Úvalu 84, Praha 5, 150 06 Prague, Czech Republic.

Lenka Kramná (L)

Department of Pediatrics, Second Faculty of Medicine, Charles University, V Úvalu 84, Praha 5, 150 06 Prague, Czech Republic.

Ari Jumpponen (A)

Division of Biology, Kansas State University, Manhattan KS66506, KS, United States of America.

Olli H Laitinen (OH)

Faculty of Medicine and Health Technology, Tampere University, Arvo Ylpön katu 34, FI-33520 Tampere, Finland.

Juho Rajaniemi (J)

Faculty of Built Environment, Tampere University, Korkeakoulunkatu 5, FI-33720 Tampere, Finland.

Heikki Hyöty (H)

Faculty of Medicine and Health Technology, Tampere University, Arvo Ylpön katu 34, FI-33520 Tampere, Finland.

Aki Sinkkonen (A)

Natural Resources Institute Finland, Turku, Finland. Electronic address: aki.sinkkonen@luke.fi.

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