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Research Article

Environmental biodiversity, human microbiota, and allergy are interrelated

Ilkka Hanski, Leena von Hertzen, Nanna Fyhrquist, Kaisa Koskinen, Kaisa Torppa, Tiina Laatikainen, Piia Karisola, Petri Auvinen, Lars Paulin, Mika J. Mäkelä, Erkki Vartiainen, Timo U. Kosunen, Harri Alenius, and Tari Haahtela
PNAS May 22, 2012 109 (21) 8334-8339; https://doi.org/10.1073/pnas.1205624109
Ilkka Hanski
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  • For correspondence: ilkka.hanski@helsinki.fi tari.haahtela@hus.fi
Leena von Hertzen
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Nanna Fyhrquist
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Kaisa Koskinen
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Kaisa Torppa
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Tiina Laatikainen
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Piia Karisola
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Petri Auvinen
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Lars Paulin
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Mika J. Mäkelä
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Erkki Vartiainen
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Timo U. Kosunen
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Harri Alenius
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Tari Haahtela
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  • For correspondence: ilkka.hanski@helsinki.fi tari.haahtela@hus.fi
  1. Contributed by Ilkka Hanski, April 4, 2012 (sent for review March 14, 2012)

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Abstract

Rapidly declining biodiversity may be a contributing factor to another global megatrend—the rapidly increasing prevalence of allergies and other chronic inflammatory diseases among urban populations worldwide. According to the “biodiversity hypothesis,” reduced contact of people with natural environmental features and biodiversity may adversely affect the human commensal microbiota and its immunomodulatory capacity. Analyzing atopic sensitization (i.e., allergic disposition) in a random sample of adolescents living in a heterogeneous region of 100 × 150 km, we show that environmental biodiversity in the surroundings of the study subjects’ homes influenced the composition of the bacterial classes on their skin. Compared with healthy individuals, atopic individuals had lower environmental biodiversity in the surroundings of their homes and significantly lower generic diversity of gammaproteobacteria on their skin. The functional role of the Gram-negative gammaproteobacteria is supported by in vitro measurements of expression of IL-10, a key anti-inflammatory cytokine in immunologic tolerance, in peripheral blood mononuclear cells. In healthy, but not in atopic, individuals, IL-10 expression was positively correlated with the abundance of the gammaproteobacterial genus Acinetobacter on the skin. These results raise fundamental questions about the consequences of biodiversity loss for both allergic conditions and public health in general.

  • biodiversity benefits
  • hygiene hypothesis
  • microbial deprivation
  • civilization diseases

Footnotes

  • ↵1To whom correspondence may be addressed. E-mail: ilkka.hanski{at}helsinki.fi or tari.haahtela{at}hus.fi.
  • Author contributions: I.H., L.v.H., M.J.M., E.V., T.U.K., and T.H. designed research; N.F., K.K., K.T., P.A., and L.P. performed research; N.F., K.K., and H.A. contributed new reagents/analytic tools; T.L. contributed data on allergies; I.H., K.K., T.L., P.K., P.A., and L.P. analyzed data; and I.H., L.v.H., and T.H. wrote the paper.

  • The authors declare no conflict of interest.

  • Data deposition: The sequences reported in this paper have been deposited in the Sequence Read Archive at the European Bioinformatics Institute (accession no. ERP001059).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1205624109/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Biodiversity, human microbiota, and allergy
Ilkka Hanski, Leena von Hertzen, Nanna Fyhrquist, Kaisa Koskinen, Kaisa Torppa, Tiina Laatikainen, Piia Karisola, Petri Auvinen, Lars Paulin, Mika J. Mäkelä, Erkki Vartiainen, Timo U. Kosunen, Harri Alenius, Tari Haahtela
Proceedings of the National Academy of Sciences May 2012, 109 (21) 8334-8339; DOI: 10.1073/pnas.1205624109

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Biodiversity, human microbiota, and allergy
Ilkka Hanski, Leena von Hertzen, Nanna Fyhrquist, Kaisa Koskinen, Kaisa Torppa, Tiina Laatikainen, Piia Karisola, Petri Auvinen, Lars Paulin, Mika J. Mäkelä, Erkki Vartiainen, Timo U. Kosunen, Harri Alenius, Tari Haahtela
Proceedings of the National Academy of Sciences May 2012, 109 (21) 8334-8339; DOI: 10.1073/pnas.1205624109
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