Associations between biodiversity, pollution, the commensal microbiota of children, and immune response

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Title: Associations between biodiversity, pollution, the commensal microbiota of children, and immune response
Author: Roslund, Marja
Contributor: University of Helsinki, Faculty of Biological and Environmental Sciences, Ecosystems and Environment Research Programme
Doctoral Programme in Interdisciplinary Environmental Sciences
Publisher: Helsingin yliopisto
Date: 2020-10-30
Belongs to series: Dissertationes Schola Doctoralis Scientiae Circumiectalis, Alimentariae, Biologicae. Universitatis Helsinkiensis - URN:ISSN:2342-5431
Thesis level: Doctoral dissertation (article-based)
Abstract: The incidence of immune-mediated diseases has increased rapidly in developed societies. According to the biodiversity hypothesis, the core reason is the evident biodiversity loss in urban areas. This biodiversity loss limits exposure to a diverse microbiota, which is associated with the human commensal microbiota and immune regulation. In addition, urban pollutants, such as polycyclic aromatic hydrocarbons (PAHs), may alter microbial communities and interfere with immune regulation. However, studies linking urban biodiversity loss, PAH pollution, environmental and human commensal microbiota and immune regulation are lacking. This study is one of the first to estimate the connections between environmental exposure, the commensal microbiota, and the immune response of urban children using both intervention trials and comparative studies. The aim of this study was also to develop practices to reduce the risk of non-communicable immune-mediated diseases that are globally recognized as emerging public health problems. These diseases comprise over 80 inflammatory disorders including allergies, type 1 diabetes, asthma and inflammatory bowel disease. The research focused on two aspects: the effect of biodiversity and pollution on the commensal microbiota of children and immune regulation. First, I estimated PAH induced bacterial shifts in polluted urban landscaping materials, and whether environmental exposure to PAHs can affect children’s commensal bacterial communities on the skin and in the gut. Secondly, we set up a human intervention trial in which urban environmental biodiversity was manipulated and examined its effects on environmental and commensal microbiota and immune regulation in children. The PAH pollution studies showed that PAHs may induce shifts in environmental and human commensal bacterial communities that are associated with human health and immune regulation. Bacterial shifts in urban landscaping materials depended on soil material type, indicating that in the future it is possible to design gardening and landscaping materials that are more resilient to bacterial shifts induced by PAH pollution. Soil PAH pollution in day-care center yards was associated with altered Actinobacteria, Bacteroidetes and Proteobacteria communities on children’s skin and in day-care yard soils. However, altered genera differed between skin and soil, excluding Mycobacterium, the abundance of which increased on skin and in soil with increasing surface soil PAH levels. Associations were not found between gut microbiota and PAH levels in day-care yard surface soils or ambient air. However, gaseous chrysene levels in the ambient air were associated with the endocrine signaling pathways predicted from the gut bacterial metagenome with the Kyoto Encyclopedia of Genes and Genomes. The peroxisome proliferator-activated receptor (PPAR) is a crucial signaling pathway in the regulation of inflammation, metabolism, and tumorigenesis. The PPAR signaling pathway together with the adipocytokine signaling pathway can regulate immune cells and affect hormonally-mediated diseases, including obesity, insulin sensitivity, puberty, and fertility. The PPAR and adipocytokine signaling pathways both decreased among children, with higher gaseous chrysene levels in the day-care center’s ambient outdoor air. These findings indicate that PAH concentrations that are below the risk assessment safety limits may alter the human commensal microbiota and interfere with endocrine signaling. The imbalance in human microbiota and the decrease in endocrine signaling pathways might contribute to inflammatory disorders. Therefore, optimal risk assessments should take into account the possibility of the disruption of endocrine signaling pathways and the microbiota–health nexus. The 28-day biodiversity intervention trial included 75 children in three different day-care environments (standard urban, biodiversity intervention, and nature-oriented). During this intervention, the environmental and intervention children’s commensal microbiota was diversified, which in turn promoted their immune regulation and eventually may have beneficial health consequences. Surface soil bacterial communities differed between intervention and standard day-care yards and, in particular, differences were seen within alpha-, beta-, and gammaproteobacterial classes. The relative abundance of bacteria typically found in the forests of Finland increased in intervention day-care yards. These environmental changes in day-care yards remained for 2 years. The diversity of proteobacterial communities in soil and on the skin of the day-care children increased during the 28-day intervention. Importantly, an increase in skin gammaproteobacterial diversity was associated with beneficial effects in immune regulation, promotion of the plasma transforming growth factor-β level and proportion of regulatory T cells, and a decline in pro-inflammatory interleukin 17A (IL-17A) levels. In addition, among intervention children the ratio between anti-inflammatory IL-10 and pro-inflammatory IL-17A increased, indicating that the biodiversity intervention promoted children’s immune regulation. In addition, among intervention children, I observed shifts within gut Ruminococcaceae and Lachnospiraceae communities that have earlier been associated with gut health. Interestingly, the microbiota on the skin and in the gut of intervention day-care children shifted toward those in nature-oriented day cares. I followed the environmental and commensal bacterial shifts on the skin, in the saliva, and in the gut for a 2-year period among children in the intervention group. This long-term study showed that the biodiversity intervention shifted the environmental and commensal bacterial communities at the intervention day cares, and these shifts include important primers for the immune system. In particular, environmental shifts were permanent based on the 2-year period. These results are proving valuable since now that we understand the effect of biodiversity in the living environment, we can shape children’s commensal bacteria and thus affect immune regulation. The challenge will be to design novel pathogen-free nature-based solutions for urban people that include a high diversity and richness of anti-inflammatory health-promoting bacteria. Future research should target this challenge. The results of this thesis support the biodiversity hypothesis: environmental biodiversity is associated with the commensal microbiota of humans and immune regulation. Indeed, both biodiversity loss and pollution in the urban environment may lead to an altered environmental microbiome. This in turn can lead to an imbalanced immune system and consequently increase the prevalence of emerging public health problems, including allergies, asthma, type 1 diabetes, and inflammatory bowel disease. Importantly, this study has demonstrated that modifying the living environment of children with microbiologically diverse natural materials might provide a feasible approach for decreasing the risk of immune-mediated diseases in urban populations.Nykyisin noin viidennes kehittyneiden maiden väestöstä kärsii immuunivälitteisestä häiriöistä, kuten allergioista, allergisesta astmasta ja tyypin 1 diabeteksesta. Biodiversiteettihypoteesin mukaan häiriöiden lisääntymisen taustalla on kaupungistumisen myötä tapahtunut luontokontaktien vähentyminen, mikä voi vaikuttaa haitallisesti immuunisäätelyyn elimistön mikrobiston yksipuolistumisen kautta. Lisäksi altistuminen kaupungin haitta-aineille, kuten liikenteestä peräisin oleville polysyklisille aromaattisille hiilivedyille (PAH), voi häiritä immuunipuolustuksen toimintaa ja kehittymistä. Väitöskirjani on ensimmäisiä tutkimuksia, jossa arvioidaan syy-seuraussuhteita luontoaltistuksen, PAH-pitoisuuksien, kaupunkilaislasten elimistön mikrobiston ja immuunipuolustuksen säätelyn välillä. Väitöskirjani perustuu kahteen näkökulmaan: 1) haitta-aineiden vaikutuksiin sekä 2) biodiversiteetin lisäämisen vaikutuksiin. Haitta-ainetutkimuksissa arvioin, miten kaupunkiympäristössä päiväkodin pihan maahan kertyvät sekä ilman PAH-pitoisuudet vaikuttavat maaperän ja lasten elimistön mikrobistoon. Biodiversiteettitutkimuksissa arvioin, miten lisääntynyt luontoaltistus vaikuttaa lasten elimistön mikrobistoon ja sitä kautta immuunisäätelyyn. Biodiversiteettitutkimuksessa vertailin kolmea erilaista päiväkotiympäristöä: 1) luontopäiväkoteja, 2) kaupunkipäiväkoteja (kontrolliryhmä) ja 3) interventiopäiväkoteja, joiden piha muokattiin vihermateriaaleilla. Haitta-ainetutkimukset osoittivat, että suhteellisen alhaiset PAH-pitoisuudet voivat yksipuolistaa kaupunkimaaperän ja lasten ihon mikrobistoa sekä häiritä hormonitoiminnan säätelyä suolistobakteerien välityksellä. Lisääntynyt luontoaltistus voi sen sijaan monipuolistaa lasten ihon mikrobistoa, mikä oli yhteydessä parempaan immuunitasapainoon. Biodiversiteettitutkimuksessa havaitsin eroja myös terveyteen liittyvässä suolistobakteeriyhteisössä eri päiväkotiryhmien välillä. Kahden vuoden pitkäaikaisseurannan perusteella mikrobistomuutokset piha-alueella olivat suhteellisen pysyviä. Biodiversiteetti-interventio sai aikaan muutoksia bakteeriryhmissä, jotka ovat aiempien tutkimusten perusteella osoittautuneet tärkeiksi immuunijärjestelmän kehittymiselle lapsuudessa. Tämän väitöskirjan tulokset puoltavat biodiversiteettihypoteesiä: altistuminen monimuotoiselle luonnolle edistää immuunitasapainoa elimistön mikrobiston kautta. Myös kaupungissa esiintyvät haitta-aineet voivat muuntaa elinympäristön ja elimistön mikrobistoa. Biodiversiteettikato ja altistuminen haitta-aineille voivat lopulta johtaa immuunijärjestelmän epätasapainoon ja lisätä kansanterveyttä uhkaavia tulehdussairauksia. Tämä väitöskirja antaa myös näyttöä siitä, että luontoyhteyden parantaminen päiväkodeissa voi olla yksi merkittävä tapa vähentää immuunivälitteisten sairauksien riskiä kaupungistuneissa yhteiskunnissa.
Subject: ympäristöekologia
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