Time for re-wilding? Western lifestyle and the human skin microbiota

Holidays are approaching and with them, the arduous choice of choosing a holiday destination!

Admittedly, I love the convenience of a 5-star hotel: ultra-clean apartments, room service providing new towels and bed sheets every day, air conditioning, appealing breakfast buffets, crystal clean pool water (with a subtle smell of chlorine), and so forth. However, my wife loves camping. Therefore, following the undisputed ’Happy-Wife-Happy-Life’ paradigm, we will spend our family holidays on a 1-star camping site in France. The 1-star rating suggests, I hope, that at least the environment will be beautiful. Interestingly, recent research suggests that not only my wife but also my microbiota will become happy, and maybe even healthier, during such a holiday in the ’wilderness’.

Worldwide industrialization and urbanization, along with massive environmental changes, dramatically threatens factors essential to human health and well-being, such as air and water pollution, global warming and loss of animal and plant biodiversity. It is estimated that, if global warming proceeds unrestrained, by 2070, ca. one-third of the global plant and animal species could be extinct [1]. Interestingly, the human microbiota also seems to be negatively influenced by industrialization or a so-called western lifestyle.

A typical western lifestyle and human microbiota

It’s hard to clearly define a ‘westernized’ or ‘industrialized’ lifestyle. However, browsing through a few articles [2,3] dealing with the industrialized microbiota, it is, among others, characterized by the following features: life in (polluted, stressful) urban environments; less contact with (unpolluted, stressless) natural environments; consumption of highly processed, conserved and easy digestible food and almost sterile drinking water; filtered indoor air; increased use of antibiotics, disinfectants and other biocides to control microbial life; modern medicine techniques, such as Caesarean section; and a strong trend towards individualization.

Typically, most research on the effects of a western lifestyle focuses on the human intestinal tract, where the vast majority of microbes are located. Studies comparing the microbiota of indigenous ethnic groups with the microbiota of people living in industrialized countries, or the monitoring of time-dependent changes of the microbiota for those who have immigrated from non-industrialized into industrialized countries, suggest that the industrial microbiota appears to have a lower structural (species inventory) and functional (gene content) diversity [2].

Taxa that have been lost or reduced in individuals living in the industrialized world were termed “VANISH” (volatile and/or associated negatively with industrialized societies of humans). For instance, traditional gut microbiota are characterized by a larger and more diverse collection of carbohydrate-active enzymes, that is, enzymes that preferably digest plant polysaccharides. As a typical western diet is limited in dietary fibres, bacteria specialized in other carbohydrate sources become enriched in an industrialized microbiota – for example, bacteria that degrade the mucus of the gut epithelia as a backup food source [2].

Implications for human health and disease

It is anticipated, but currently unconfirmed, that these vanished microbes may be at least partly responsible for the significant increase in non-communicable diseases (NCDs) observed since industrialization began, including stroke, heart diseases, some cancers, diabetes, dementia and allergies, which are all believed to be driven by chronic inflammation [2,3].

Effects of industrialization have further been investigated within the human skin ecosystems [3], suggesting similar effects as observed in the intestinal tract. Rates of allergy in asthma, allergic rhinitis and eczema in rural Karelia (North-Western Russia) were found to be associated with cutaneous Acinetobacter bacteria [4]. While people in the Russian part of Karelia live in closer contact with nature, the Finish part of Karelia is geographically close by, but more industrialized. Here, eczema rates are ten times higher, while the abundance of Acinetobacter was significantly lower on skin and nasal epithelia. Notably, Acinetobacter species have previously shown ameliorating immune effects in atopic diseases [5].

In a landmark study [6], McCall and co-workers investigated human, animal and household samples along an urbanization gradient in South America, spanning from a remote village to a metropolis. The number of chemicals (surface cleaner, detergents, personal care products, pharmaceuticals) used in a household increased with urbanization. While the diversity of household and skin fungi, including potentially pathogenic species, also increased with urbanization, the richness in skin bacteria, particularly on the hands and arms decreased. Specifically, environmental bacteria, not typically associated with humans, decreased or even disappeared. Interestingly, a negative correlation between skin bacterial diversity and detergents was observed, suggesting that these products might at least partly be responsible for the observed loss in skin bacterial diversity. Higher proportions of potentially pathogenic bacteria and fungi were found with increasing urbanization, suggesting a role in typical western NCDs, such as acne or atopic dermatitis [6,7]

Finding a fix

What are the (practical) implications? Clearly not the development of new cosmetic skin care formulations containing (maybe just even dead fragments of) one or a few microbial species that were detected on the skin of some remotely living ethic groups, but are missing on the skin of people nowadays. Admittedly, marketing would be easy and probably successful (“Back to Nature”, “Re-Wilder your skin ecosystem”, “Palaeo-Cosmetics” and so on), but in practice the development of such products would not be simple, and beneficial effects on the skin ecosystem hard to prove.

Rather, researchers [2] suggest more sustainable, long-term strategies, given the fact that still little is known about the functionality of many members of the skin ecosystem. For instance, more research, on the functionality of the VANISH microbes is needed to better understand whether a re-introduction into the human microbiome might be beneficial or even unhealthy (which would be the case if pathogens or parasites were re-introduced). Such research should also include the preservation of microbes that are currently vanishing from the human microbiome, similar to the establishment of seed banks to preserve the loss of (ancient) crop plants.

Researchers also point out that much more research is needed to evaluate the long-term effects of environmental and other external factors on the human microbiome, such as diet (food, drinking water), personal care, home care, housing and living conditions, occupation, recreational activities, medical treatments and so on. Wherever possible, ‘microbiota-friendly’ strategies should be adopted or developed that do not negatively interfere with the human microbiota. Some ideas for more sustainable microbial ecosystem management approaches with positive feedback on the human microbiota are presented by Sonnenburg and colleagues [2]. For instance, contradicting the long-term view that wound healing demands sterility, the introduction of commensal skin bacteria into wounds might reduce infections and minimize the need for antibiotic treatments [2, 8].

Finally, it is suggested that a healthy human microbiota is inevitably linked with a healthy environment, an idea also known as the ‘One World, One Health’ approach [9]. Therefore, all strategies aiming to preserve or restore local, regional and global nature and biodiversity will also benefit a healthy human microbiome. Allowing contact with a healthy and microbially diverse natural environment while trying to avoid pathogens, in particular during pregnancy and at infant age, is seen as the most important way to achieve a health-supporting microbiota [2, 3].

Therefore, I will definitely enjoy our forthcoming camping holiday. I will take a daily extra dive into the lake close by the camping site to ‘re-wild’ my skin microbiota. Directly after the holidays, I will attend a big microbiology conference in Switzerland, ‘unfortunately’ residing in a 3-star hotel. Maybe, rising to speak for my microbiota, I will propose (during the plenary session) that the next conference should be held at a camping site…

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1. https://eu.usatoday.com/story/news/nation/2020/02/14/climate-change-study-plant-animal-extinction/4760646002 [accessed 29-06-22]

2. Sonnenburg JL, Sonnenburg ED. Vulnerability of the industrialized microbiota. Science. 2019 Oct 25;366(6464):eaaw9255. doi: 10.1126/science.aaw9255.

3. Prescott SL, Larcombe DL, Logan AC, West C, Burks W, Caraballo L, Levin M, Etten EV, Horwitz P, Kozyrskyj A, Campbell DE. The skin microbiome: impact of modern environments on skin ecology, barrier integrity, and systemic immune programming. World Allergy Organ J. 2017 Aug 22;10(1):29. doi: 10.1186/s40413-017-0160-5.

4. Ruokolainen L, Paalanen L, Karkman A, Laatikainen T, von Hertzen L, Vlasoff T, Markelova O, Masyuk V, Auvinen P, Paulin L, Alenius H, Fyhrquist N, Hanski I, Mäkelä MJ, Zilber E, Jousilahti P, Vartiainen E, Haahtela T. Significant disparities in allergy prevalence and microbiota between the young people in Finnish and Russian Karelia. Clin Exp Allergy. 2017 May;47(5):665-674. doi: 10.1111/cea.12895.

5. Hanski I, von Hertzen L, Fyhrquist N, Koskinen K, Torppa K, Laatikainen T, Karisola P, Auvinen P, Paulin L, Mäkelä MJ, Vartiainen E, Kosunen TU, Alenius H, Haahtela T. Environmental biodiversity, human microbiota, and allergy are interrelated. Proc Natl Acad Sci U S A. 2012 May 22;109(21):8334-9. doi: 10.1073/pnas.1205624109.

6. McCall LI, Callewaert C, Zhu Q, Song SJ, Bouslimani A, Minich JJ, Ernst M, Ruiz-Calderon JF, Cavallin H, Pereira HS, Novoselac A, Hernandez J, Rios R, Branch OH, Blaser MJ, Paulino LC, Dorrestein PC, Knight R, Dominguez-Bello MG. Home chemical and microbial transitions across urbanization. Nat Microbiol. 2020 Jan;5(1):108-115. doi: 10.1038/s41564-019-0593-4.

7. Callewaert C, Ravard Helffer K, Lebaron P. Skin Microbiome and its Interplay with the Environment. Am J Clin Dermatol. 2020 Sep;21(Suppl 1):4-11. doi: 10.1007/s40257-020-00551-x.

8. Johnson TR, Gómez BI, McIntyre MK, Dubick MA, Christy RJ, Nicholson SE, Burmeister DM. The Cutaneous Microbiome and Wounds: New Molecular Targets to Promote Wound Healing. Int J Mol Sci. 2018 Sep 11;19(9):2699. doi: 10.3390/ijms19092699

9. van Helden PD, van Helden LS, Hoal EG. One world, one health. Humans, animals and the environment are inextricably linked–a fact that needs to be remembered and exploited in our modern approach to health. EMBO Rep. 2013 Jun;14(6):497-501. doi: 10.1038/embor.2013.61. Epub 2013 May 17

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