Archaea on human skin

Arc…what? In my experience, archaea are the lesser-known microorganisms. When asked for typical microorganisms, most people, including my students, name bacteria, fungi and viruses (even though viruses are not actually organisms at all). However, archaea are usually forgotten.

Maybe I would neglect archaea too, if I didn´t complete my PhD thesis at one of the top research centers for archaea in Germany at that time, the Max Planck Institute for Terrestrial Microbiology in Marburg. This made me very aware of the existence of archaea, and that they are really fascinating.

The origins of archaea

“Archaea” is derived from Greek “archaios”, meaning “very” old, “ancient” or “primitive”. The first archaea (singular “archaeon”) were isolated from environments with extreme conditions such as lack of oxygen, acidic pH, high temperature or high salinity. Researchers assumed that organisms thriving happily in such extreme habitats might be closely related to the first (and ancient) microbial colonizers of our planet, which was also very extreme in its conditions at the very beginning. As archaea share many structural features with bacteria, marking both as prokaryotes (that is, organisms without a nucleus), they were first categorized as Archaebacteria and put alongside the Eubacteria on the taxonomic level, as two separate kingdoms within the prokaryotes [1].

However, in the 1970s, molecular taxonomic analyses conducted by Carl Woese, the godfather and pioneer of 16S rRNA gene sequencing, suggested that bacteria and archaea are only distantly related. Based on these and additional findings, life on earth is nowadays divided into three domains: Bacteria, Archaea and Eukaryota (for a summary of these historical findings see ref. [1]). In fact, it finally turned out that archaea and eukaryotes are more closely related to each other than bacteria and eukaryotes, meaning that we as humans share more genetic elements with archaea than with bacteria. Vice versa, bacteria are nowadays assumed to be more closely related to LUCA, the last universal common ancestor (the cell with which all life on Earth began) than archaea. Based on what we know now, “Archaea” is definitely a misleading name. “Neo-Bacteria” or “Bacteria 2.0.” might have been a better choice.

The close relationship of archaea with eukaryotic cells can even lead to the assumption that eukaryotic cells might originate from an uptake of bacteria-like cells as endosymbionts into an archaeal cell, resembling recently discovered members of the so-called Asgardarchaeota [2]. In plain words, eukaryotic, including human, cells might be a type of symbiotic mélange of bacterial and archaeal cells.

Unique metabolic pathways

The main differences and similarities between bacteria, archaea and eukaryotes are textbook knowledge. Differences, for example, include the unique metabolic pathways that are exclusively owned by archaea – one of which is methanogenesis.

Archaea are the only organisms on Earth that can produce quantitative amounts of methane (CH4), for example by using hydrogen (H2) and carbon dioxide (CO2)as substrates or by cleaving acetate. Methanogenesis takes place at the end of any degradation chain, in which organic matter is decomposed under anaerobic condition, that is, in the absence of oxygen. As methane is a strong greenhouse gas, the identification of methane sources is nowadays more important than ever. Such sources include seabed sediments, flooded soils, swamps and landfill sites, but also intestinal tracts – for example, of cattle. Clearly, methane emission from these sources needs to be reduced to prevent ongoing global warming. (Interestingly, we also detected methanogenic archaea in used kitchen sponges [3]; however, that does not imply that these kitchen utensils are significantly involved in global warming, too).

In contrast, generation of methane in digestion towers of wastewater treatments plants or agricultural biogas plants is an important method of renewable energy production. Obviously, a significant part of the climatic fate of our planet lies in archaeal hands. Why then is this group so neglected?

Archaea and human hosts

I assume the lack of attention is explainable by the fact that no pathogenic archaea have yet been identified. In the real world, fame or public awareness often arises from fear. However, there are no archaeal counterparts to plague, tuberculosis, smallpox, AIDS or COVID, or even to acne, athlete’s foot, bad breath or dandruff. It seems as though this group of microorganisms is just very friendly and peaceful with us, but also with animals, plants and even bacteria.

Molecular research over recent years has shown that a diverse community of archaea (collectively termed “the archaeome”) is also affiliated with various parts of the human body, such as gut, mouth and skin [4]. The presence of methanogenic archaea in the intestinal tract, including species such as Methanobrevibacter smithii or Methanosphaera stadtmanae, has been known for decades [5]. Depending on the number and activity of these methanogens and numerous other factors, particularly diet, humans can also emit methane, albeit ca. 2500 times less than cows (ca. 100 ml per day versus 250 l per day [6]). However, molecular microbiome studies suggest that besides methanogens, other archaeal taxa seem to be present too, maybe even in higher shares. A recent study from Korea [7] proved the presence of archaeal 16S rRNA gene signals in more than 40% of almost 900 investigated fecal samples, most of which were affiliated with haloarchaea – archaea with pronounced tolerance against high-salt concentrations. On average, archaea accounted for about 10% of the prokaryotic sequences.

The discovery of archaea as members of the human skin microbiota dates back to approximately 10 years ago and is closely related with Christine Moissl-Eichinger from Graz University in Austria. Her group was molecularly searching for archaeal contaminations in clean rooms used for the assembly of spacecraft vehicles. Such contaminations must be avoided to prevent contamination of Mars or other extraterrestrial objects with extremophilic organisms from Earth. While they failed to detect methanogenic methanogens (which might survive on Mars), they frequently detected archaeal sequences affiliated with the so-called Thaumarchaeota phylum (today classified as the Nitrososphaeria class within the Thermoproteota phylum) – aerobic, mesophilic archaea known for their ability to oxidize ammonia in various environments. Finally, they identified the humans working in the clean rooms as the only possible source for these organisms.

Based on these findings, Moissl-Eichinger and her group published two studies [8, 9] showing that archaea (and in particular the Thaumarchaeotamentioned above) represent low-abundant (relative abundances in the low single-digit range), but probably resident, members of the prokaryotic human skin microbiota. They suggested associations with age and some parameters of skin physiology and assumed that these organisms might be involved in skin nitrogen metabolism, in particular the oxidation of ammonia from sweat. Such removal of nitrogen might lower the skin pH and thus contribute to the skin acid mantle, suggesting a beneficial role of these organisms for skin physiology. However, further research will have to show whether this is really true. In particular, a very recent study [10] has suggested that the (already low) abundance and prevalence of Thaumarchaeota on skin might be significantly lower than expected.

In summary, archaea can definitely be counted as resident members of the human skin microbiota, although many questions regarding the structure and functionality of this skin archaeome still wait to be answered. Nevertheless, I am deeply convinced that as soon as we know a bit more about this fascinating group of organisms, the cosmetics industry will also make use of them – so maybe we can expect to see claims such as “…awakens the ancient microbial powers on your skin!” alongside our beauty and personal care products in the not-so-far future.

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References

1. Eme, L. & Doolittle, W. F. Archaea. Curr. Biol. 25, R851–R855 (2015).

2. Eme, L. et al. Archaea and the origin of eukaryotes. Nat. Rev. Microbiol. 15, 711–723 (2017).

3. Jacksch, S. et al. Metagenomic analysis of regularly microwave-treated and untreated domestic kitchen sponges. Microorganisms 8, 736 (2020).

4. Borrel, G. et al. The host-associated archaeome. Nat. Rev. Microbiol. 11, 622–636 (2020).

5. Miller, T. L. & Wolin, M. J. Enumeration of Methanobrevibacter smithii in human feces. Arch. Microbiol. 131, 14–18 (1982).

6. Sahakian, A. B. et al. Methane and the gastrointestinal tract. Dig. Dis. Sci. 55, 2135–2143 (2009).

7. Kim, J. Y. et al. The human gut archaeome: identification of diverse haloarchaea in Korean subjects. Microbiome 8, 114 (2020).

8. Probst, A. J. et al. Archaea on human skin. PLoS ONE 8, e65388 (2013).

9. Moissl-Eichinger, C. et al. Human age and skin physiology shape diversity and abundance of Archaea on skin. Sci Rep. 7, 4039 (2017).

10. Umbach, A. K. et al. Archaea are rare and uncommon members of the mammalian skin microbiome. mSystems 6, e0064221 (2021).

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