Looking in: Air Pollutants and the Human Microbiome

Introduction

Although the impact of air pollution on human health is a growing concern, there is limited discourse regarding the precise interactions between various pollutants and the microbial organisms present in our bodies. Nonetheless, research showcases exposure to various air pollutants such as particulate matter (PM), ozone, nitrogen dioxide, sulfur dioxide, and volatile organic compounds (VOCs) affect the human microbiome and consequently manifest in the form of various health concerns. The human microbiome is a catalog of all the genes present in the microbial cells harbored by humans [1]. Specifically, interactions with noxious chemicals may lead to the dysbiosis of human microbiota, especially those present in the respiratory tract, the gut, and the female reproductive system, [2]. Dysbiosis can be characterized by (1) Loss of beneficial bacteria, (2) Overgrowth of potentially pathogenic bacteria, and (3) Loss of overall bacterial [3].

 

Figure 1. Different types of interaction between environmental chemicals and gastrointestinal microbiota (GI) (Claus et al, 2016)

 

Gut Microbiota

Previous research has illustrated that exposure to air pollution is associated with increased risk of metabolic conditions such as obesity and type-2 diabetes, possibly owing to changes in gut microbial composition [4]. Accordingly, Faloudi et al (2020) utilized whole-genome sequencing to further discern whether the composition of the gut microbiome was truly altered. As illustrated in Figure 2, their research showcased how exposure to higher levels of ozone was indeed associated with a decreased gut microbial diversity [5]. Similar investigations in infants yielded similar results; infants exposed to highest levels of PM2.5 had 60% less of a beneficial bacterium (Phascolarctobacterium) which is associated with decreases in inflammation [6]. These findings suggest that exposure to noxious chemicals can lead to adverse health outcomes, even over a short period of time, thereby reemphasising the importance of regulating these chemicals in our atmosphere. Moreover, researchers have proposed that interactions with gut microbiota may be enhancing the toxicity of air pollutants in the first place [7]. In other words, gut microbiota and air pollutants exhibit a bi-directional relationship, whereby pollutants may affect the composition of the gut microbiome, and the gut microbiota may also increase or decrease the toxicity of air pollutants.

 

Figure 2. Increased exposure to ozone is associated with a lower bacterial Shannon diversity index (C) and evenness (D) at the species level (Fouladi et al, 2020)

 

Respiratory Microbiome

Dysbiosis of the respiratory microbiome can increase the risk of lower and upper respiratory tract infections, inflammation, asthma, and chronic lung diseases [8]. The introduction of particular air pollutants, such as PM 2.5, into the respiratory tract is particularly concerning since this may kickstart a cascade effect. The PM 2.5 first penetrates into the lung cells and compromises epithelial integrity, following which additional harmful microbes and toxic metabolites are able to enter into the epithelial layer, and finally the immune system is activated, which enables dysbiosis of the lung microbiota [8]. Figure 2 showcases how this cascade also occurs within the gut, whereby the dysbiosis of gut microbiota allows infiltration of harmful metabolites into the gut. In extreme cases, these pollutants may induce the production of reactive oxygen species (ROS) which cause the death of respiratory microbiota [9] .

 

Figure 3. Potential pathway of air pollution related microbiota dysbiosis which may ultimately lead to (6) decrease in gut microbiota-dependent metabolites such as short-chain fatty acid (SCFA), (7) a disturbed gut-brain axis (GBA) and hypothalamus–pituitary–adrenal axis (HPA), and (8) altered signalling metabolites influencing organ functionality (Gupta et al 2022)

 

Limitations of Current Research

The specific effect of air pollution on the human microbiome is a relatively new area of research, which is why human-based studies remain limited. Additionally, Filardo et al’s (2022) review of research in this domain highlights how different researchers tends to adopt different  designs for their metagenomic studies, and this lack of standardisation makes it difficult to compare results across studies [10]. They further suggest that standardizing methods of sample collection and storage as well as DNA extraction and gene amplification will allow for more accurate and comparable results [10]. Ultimately, a comprehensive understanding of the interactions between common air pollutants and human microbiota will better inform the regulation of these chemicals in our environment. Finally, as research in this area continues to evolve, it will be beneficial to explore potential interventions to mitigate the impacts of air pollution on the human microbiome, such as through targeted probiotics or other microbiome-based therapies which seek to enhance microbial composition [11].

 

References

[1] Turnbaugh, P. J., Ley, R. E., Hamady, M., Fraser-Liggett, C. M., Knight, R., & Gordon, J. I. (2007). The Human Microbiome Project. Nature, 449(7164), 804–810. https://doi.org/10.1038/nature06244

[2] Mousavi, S. E., Delgado-Saborit, J. M., Adivi, A., Pauwels, S., & Godderis, L. (2022). Air pollution and endocrine disruptors induce human microbiome imbalances: A systematic review of recent evidence and possible biological mechanisms. Science of the Total Environment, 816, 151654. https://doi.org/10.1016/j.scitotenv.2021.151654

[3] DeGruttola, A. K., Low, D., Mizoguchi, A., & Mizoguchi, E. (2016). Current Understanding of Dysbiosis in Disease in Human and Animal Models. Inflammatory Bowel Diseases, 22(5), 1137–1150. https://doi.org/10.1097/mib.0000000000000750

[4] Bailey, M. J., Naik, N. N., Wild, L. E., Patterson, W. B., & Alderete, T. L. (2020). Exposure to air pollutants and the gut microbiota: a potential link between exposure, obesity, and type 2 diabetes. Gut Microbes, 11(5), 1188–1202. https://doi.org/10.1080/19490976.2020.1749754

[5] Fouladi, F., Bailey, M. J., Patterson, W. B., Sioda, M., Blakley, I. C., Fodor, A. A., Jones, R. B., Chen, Z., Kim, J. S., Lurmann, F., Martino, C., Knight, R., Gilliland, F. D., & Alderete, T. L. (2020). Air pollution exposure is associated with the gut microbiome as revealed by shotgun metagenomic sequencing. Environment International, 138, 105604. https://doi.org/10.1016/j.envint.2020.105604

[6] Bailey, M. J., Holzhausen, E. A., Morgan, Z. E. M., Naik, N., Shaffer, J. P., Liang, D., Chang, H. H., Sarnat, J., Sun, S., Berger, P. K., Schmidt, K. A., Lurmann, F., Goran, M. I., & Alderete, T. L. (2022). Postnatal exposure to ambient air pollutants is associated with the composition of the infant gut microbiota at 6-months of age. Gut Microbes, 14(1). https://doi.org/10.1080/19490976.2022.2105096

[7] Claus, S. P., Guillou, H., & Ellero-Simatos, S. (2016). The gut microbiota: a major player in the toxicity of environmental pollutants? Npj Biofilms and Microbiomes, 2(1). https://doi.org/10.1038/npjbiofilms.2016.3

[8] Gupta, N., Yadav, V. K., Gacem, A., Al-Dossari, M., Yadav, K. K., Abd El-Gawaad, N. S., Ben Khedher, N., Choudhary, N., Kumar, P., & Cavalu, S. (2022). Deleterious Effect of Air Pollution on Human Microbial Community and Bacterial Flora: A Short Review. International Journal of Environmental Research and Public Health, 19(23), 15494. https://doi.org/10.3390/ijerph192315494

[9] Hamidou Soumana, I., & Carlsten, C. (2021). Air pollution and the respiratory microbiome. Journal of Allergy and Clinical Immunology, 148(1), 67–69. https://doi.org/10.1016/j.jaci.2021.05.013

[10] Filardo, S., Di Pietro, M., Protano, C., Antonucci, A., Vitali, M., & Sessa, R. (2022). Impact of Air Pollution on the Composition and Diversity of Human Gut Microbiota in General and Vulnerable Populations: A Systematic Review. Toxics, 10(10), 579. https://doi.org/10.3390/toxics10100579

[11] Keulers, L., Dehghani, A., Knippels, L., Garssen, J., Papadopoulos, N., Folkerts, G., Braber, S., & van Bergenhenegouwen, J. (2022). Probiotics, prebiotics, and synbiotics to prevent or combat air pollution consequences: The gut-lung axis. Environmental Pollution, 302, 119066. https://doi.org/10.1016/j.envpol.2022.119066

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