The Skinny

Did you know, as humans our largest organ – skin – plays a crucial role in hosting microbes that help train the immune system. Is it the same for bees? asks science writer Dave Black as he explores an emerging field of research.

By Dave Black

The largest organ in your body is your skin. More than just an inert cover, and more than a way of regulating your temperature and water level, skin is a complex structure vital to your immune system. Weighing about 5kg, and covering about 1.75 square metres, it is also home to fairly stable communities of resident microbes that are an essential part of how it operates, microbes passed to you from your mother and close family.

 Whether dry, oily, or damp, the human skin is home to between 600 and 2million microbes for every cm2, which are an essential part of how it operates. Science is now seeking to determine whether a similar relationship could be at play for honey bees.

Different kinds of microbes choose different parts of your skin, some preferring dry bits, or oily bits, or damp bits, but there will be between 600 and 2million for every cm2. The outermost layer is made up of flattened dead cells called corneocytes in a matrix of lipids and keratin. Each day a new layer of cells is produced, and an old, outer layer is shed into the air or removed by abrasion, (or ‘washing’, as some call it). It’s estimated a healthy skin will shed 100 million particles each day, about 10% of which contain viable bacteria.

It’s De-facto

These, mostly bacteria, but bacteriophages, viruses, fungi, and archaea[i] too, begin to colonise your skin within six hours or so of you being born. If we consider the total size of the habitat available to microbes, including the hair follicles, sweat, and sebaceous glands, the total skin habitable area is closer to 30m2, not dissimilar to the habitable area provided by that other bacterial playground, the human gut[ii]. It’s not all about the germs on the outside.

Your skin is literally the interface between you and the world. While there are bits we might think of as physical ‘scaffolding’, it is a live-in marriage of microbes that actually respond to what’s out there, and in doing so they ‘train’ your immune-system. As designed, your skin cells are providing a habitat the immune-system can learn from, and in return they glean information and protection from an environment in delicate balance [iii], [iv]. You and your bacteria are de-facto partners not enemies, inside and out.

When you stop to think about it, the outside of a honey bee might be covered with microbes too. Are they just as important?

A Honey Bee’s ‘Skin’

A honeybee exoskeleton, or cuticle, is physically very different to ours and not completely developed until after it starts to forage[v]. The layer on the outside is the waterproof, lipid ‘envelope’. Besides its barrier function the layer is enriched with hydrocarbon molecules (cuticular hydrocarbons or CHCs) which defend against pathogens, lubricate mobile body parts, and provide information about the individual’s physical, sexual, and social condition. The CHCs are synthesised in specialised cells and travel via the bee’s blood using special carrier cells called lipophorins, and migrate to the surface through pores in the cuticle.

The rigid structure we’re used to seeing from the outside comes from deeper layers, a darker exocuticle made with cells containing chitin, and beneath that, the endocuticle which includes a protein called sclerotin. The chitin is hard but flexible, the sclerotin is strong and rigid. The cuticle is constructed to allow or prevent movement in particular places, and is penetrated by apertures for sensory organs and hairs[vi].  You might think, not a promising substrate for microbes to reside on. You’d be wrong.

Germs on the Outside

Nearly all the current research about the honeybee’s microbiome looks at its gut, although one group from July last year, considered a ‘Social Resource Niche’ that includes “all the collection of aerobic or microaerophilic niches including stored and secreted nutrition, and host anatomical features”[vii] (in other words, the hive, and anywhere that supports oxygen-using [aerobic, aerophilic] microbes, as opposed to the anaerobic ‘gut’ kind).

In January this year a group of scientists from St Petersburg, Russia, has looked specifically at the microbial communities that might inhabit the bees exoskeleton surface[viii]. On its own you might not think the study particularly convincing, but there are now half-a-dozen or so where a cutaneous microbiome becomes a plausible feature and the others aren’t Russian.[ix] Unsurprisingly, it turns out all sorts of bees are covered on the outside by all sorts of microbes.

Just because we weren’t looking doesn’t mean it isn’t there.

So, What’s the Skinny?

One thing that everyone is interested in at the moment are the cuticular hydrocarbons (those defenders-against-pathogens mentioned earlier). That’s partly because they are studying varroa mites and there is pretty good evidence to show varroa use some CHCs to choose which bee to prey on and when. The bees also use different CHCs to detect parasitised and dying larvae in order to clear them out of the brood nest.

However, CHCs are not all smelly/tasty signals like pheromones and karimones. Another group of CHCs are antimicrobial peptides or AMPs. These target specific bacteria and make their cell membranes ‘leaky’ (or stop proteins folding properly) so they die. So far four families of AMPs (i.e., apidaecins, abaecin, hymenoptaecin and defensins) are well-known for the honey bee[x], but the curious thing is AMPs are not necessarily made by the bee. Bacteria make them too, and some AMPs can be a joint effort!

I’d be interested to know if, say, American foulbrood bacteriophages might be found here too. And while ‘nobody died’, none of us know what something like oxalic or formic acid (or whatever) might do to a bee’s CHC profile.

If our own physiology is any kind of example, we shouldn’t dismiss microbes as just temporary or aberrative contamination of our honey bee superorganism’s outside. It’s more than likely they are a permanent part of the system. As in our case, a microbe-infested skin is not something that separates them from their environment, it’s what joins them to their environment. As one of the journal articles suggests, there is a whole new micro bee-ology out there[xi].

Dave Black is a commercial-beekeeper-turned-hobbyist, now retired. He is a regular science writer providing commentary on “what the books don't tell you”, via his Substack Beyond Bee Books, to which you can subscribe here.

References

[i] Zhu, Y., Yu, X., Cheng, G., 2023. Human skin bacterial microbiota homeostasis: A delicate balance between health and disease. mLife 2, 107–120. https://doi.org/10.1002/mlf2.12064

[ii] Gallo, R.L., 2017. Human Skin Is the Largest Epithelial Surface for Interaction with Microbes. Journal of Investigative Dermatology 137, 1213–1214. https://doi.org/10.1016/j.jid.2016.11.045

[iii] Zhu, Y., Yu, X., Cheng, G., 2023. Human skin bacterial microbiota homeostasis: A delicate balance between health and disease. mLife 2, 107–120. https://doi.org/10.1002/mlf2.12064

[iv] Swaney, M.H., Kalan, L.R., 2021. Living in Your Skin: Microbes, Molecules, and Mechanisms. Infect Immun 89, e00695-20. https://doi.org/10.1128/IAI.00695-20

[v] Falcón, T., Ferreira-Caliman, M.J., Franco Nunes, F.M., Tanaka, É.D., Do Nascimento, F.S., Gentile Bitondi, M.M., 2014. Exoskeleton formation in Apis mellifera: Cuticular hydrocarbons profiles and expression of desaturase and elongase genes during pupal and adult development. Insect Biochemistry and Molecular Biology 50, 68–81. https://doi.org/10.1016/j.ibmb.2014.04.006

[vi] Stell, I., 2012 Understanding Bee Anatomy: a full colour guide. Catford Press. ISBN 978-09574228-0-3

[vii] Anderson, K.E., Copeland, D.C., 2024. The honey bee “hive” microbiota: meta-analysis reveals a native and aerobic microbiota prevalent throughout the social resource niche. Front. Bee Sci. 2, 1410331. https://doi.org/10.3389/frbee.2024.1410331

[viii] Kaschenko, G., Taldaev, A., Adonin, L.S., Smutin, D., 2024. Investigating Aerobic Hive Microflora: Role of Surface Microbiome of Apis mellifera. https://doi.org/10.20944/preprints202412.1053.v1

[ix] See also; ,Thamm, M., Reiß, F., Sohl, L., Gabel, M., Noll, M., Scheiner, R., 2023. Solitary Bees Host More Bacteria and Fungi on Their Cuticle than Social Bees. Microorganisms 11, 2780. https://doi.org/10.3390/microorganisms11112780, and Reiß, F., Schuhmann, A., Sohl, L., Thamm, M., Scheiner, R., Noll, M., 2023. Fungicides and insecticides can alter the microbial community on the cuticle of honey bees. Front. Microbiol. 14, 1271498. https://doi.org/10.3389/fmicb.2023.1271498

[x] Kaltenpoth, M., Engl, T., 2014. Defensive microbial symbionts in Hymenoptera. Functional Ecology 28, 315–327. https://doi.org/10.1111/1365-2435.12089

[xi] There is also a ‘micro beeota’... Smutin, D., Lebedev, E., Selitskiy, M., Panyushev, N., Adonin, L., 2022. Micro”bee”ota: Honey Bee Normal Microbiota as a Part of Superorganism. Microorganisms 10, 2359. https://doi.org/10.3390/microorganisms10122359