“Anatomy Promotes Neutral Coexistence of Strains in the Human Skin Microbiome”, Arolyn Conwill, Anne C. Kuan, Ravalika Damerla, Alexandra J. Poret, Jacob S. Baker, A. Delphine Tripp, Eric J. Alm, Tami D. Lieberman2022-01-06 (, )⁠:

What enables strains of the same species to coexist in a microbiome? Here, we investigate whether host anatomy can explain strain co-residence of Cutibacterium acnes, the most abundant species on human skin.

We reconstruct on-person evolution and migration using whole-genome sequencing of C. acnes colonies acquired from healthy subjects, including from individual skin pores, and find considerable spatial structure at the level of pores. Although lineages (sets of colonies separated by <100 mutations) with in vitro fitness differences coexist within centimeter-scale regions, each pore is dominated by a single lineage. Moreover, colonies from a pore typically have identical genomes. An absence of adaptive signatures suggests a genotype-independent source of low within-pore diversity.

We therefore propose that pore anatomy imposes random single-cell bottlenecks; the resulting population fragmentation reduces competition and promotes coexistence. Our findings suggest that therapeutic interventions involving pore-dwelling species might focus on removing resident populations over optimizing probiotic fitness.

[Media:

C. acnes is naturally occurring, and the most abundant bacteria on skin. Its link to acne, the skin disease, is not clear, said Tami Lieberman, a professor at MIT and an author of the new paper. If biologists want to unpack the relationship between your face’s inhabitants and its health, it will be an important step to understand whether varying strains of C. acnes have their own talents or niches, and how the strains are distributed across your skin.

To collect their samples, Dr. Lieberman and her colleagues used commercially available nose strips and old-fashioned squeezing with a tool called a comedone extractor. They then smeared samples, each a bit like a microscopic glacial core, from within pores on Petri dishes. They did the same with samples from toothpicks rubbed across the surface of participants’ foreheads, cheeks and backs, which picked up bacteria living on the skin’s surface rather than in the pores. They allowed the bacteria to grow, then sequenced their DNA to identify them.

Each person’s skin had an unique combination of strains, but what surprised the researchers most was that each pore housed a single variety of C. acnes. The pores were different from their neighbors, too—there was no clear pattern uniting the pores of the left cheek or forehead across the volunteers, for instance.

What’s more, judging from the sequencing data, the bacteria within each pore were essentially identical. “There’s a huge amount of diversity over one square centimeter of your face”, said Arolyn Conwill, a postdoctoral researcher who is the study’s lead author. “But within a single one of your pores, there’s a total lack of diversity.”

What the scientists think is happening is that each pore contains descendants of a single individual. Pores are deep, narrow crannies with oil-secreting glands at the bottom, Dr. Lieberman said. If a C. acnes cell manages to get down there, it may proliferate until it fills the pore with copies of itself. This would also explain why strains that don’t grow very quickly manage to avoid being outcompeted by speedier strains on the same person. They’re not competing with each other; they’re living side by side in their own walled gardens.

Intriguingly, these gardens are not very old, the scientists think. They estimate that the founding cells in the pores they studied took up residence only about one year before. What happened to the bacteria that previously lived there? The researchers don’t know—perhaps they were destroyed by the immune system, fell prey to viruses or were unceremoniously yanked out by a nose strip, clearing the way for new founders.]

[This raises a lot of questions about acne. If each pore is clonal, then presumably each acne cyst/instance is also clonal. So it’s not a ‘community’ effect—is there a specific bacteria which runs amok in each pore? Or do the acne instances all share some specific mutations? And if they turn over on an annual basis, why do many cysts seem to recur in the same spot? (Or do they not, and merely recur in an adjacent spot where an acne pore managed to colonize neighboring pores?)

Since acne takes time to form, does this suggest that a reason Westerners get so much acne compared to other civilizations is that being indoors or otherwise so Western reduces turnover speed, and so the reason acne is practically unknown to hunter-gatherers etc is something like “they get so much sunlight that every pore is nuked by UV light before the bad bacteria can go bad and then the pore is immediately recolonized”?]