The Chemistry Column Claire Gormley

Lessons from lichens

Claire Gormley

When the calendar changes, I fall into the habit of looking back at the events of the past year. This year, as it was for many, my calendar was filled with cancelled holidays, missed birthdays, and, for the most part, emptiness. The disappointment and grief many of us have felt over 2020 still lingers— an ache made even more poignant for those of us in another lockdown. But as I sat down on my familiar couch (in my all too familiar sweatpants) to research Usnea spp. I was reminded of three important lessons of this lockdown experience: (1) the responsibility we all have to take care of one another; (2) the importance of looking after ourselves; and (3) the duty we have to protect our planet. When I remember these lessons, the year does not feel so empty, and I can look forward to each coming day knowing that I am doing my part. Lichens are unique because they are not a single organism; they are a symbiotic relationship between photobionts and fungus (Cocchietto, Skert and Sava, 2002). The two organisms live together, each contributing to the survival of the other. The photobionts, like algae or cyanobacteria, provide food for both organisms through the process of photosynthesis. Likewise, the fugus provides structural support which protects the algae from drying out, and also water and minerals (Grass, 2017; Cocchietto, Skert and Sava, 2002). These organisms rely on one another to do their part so they both can live, much like our symbiosis with healthcare and other essential workers. Unlike the lichen, it can be all too easy for us to forget who we are protecting; it goes against our nature to avoid social contact. Yet we have found new ways to connect with those we love, while sustaining the symbiosis. Whether it’s a distanced doorstep dinner with our neighbours, or a zoom happy hour with colleagues, we are playing our part in the relationship so that the other can survive. We have also learned how to truly take care of ourselves. The healing power of a walk in the fresh air was finally recognized when the opportunity to do so was limited. Rest became normalized. Many of us began cooking for ourselves (even beyond banana bread and sourdough) and prioritizing our mental and physical health. Even so, how many of us remain unaware of the expansive roles lichen play in our health? Like plants, lichens produce large numbers of bioactive substances, which provide protection against a range of viral, bacterial, and protozoan parasites, as well as animal predators, plant competitors, and environmental factors like ultraviolet (UV) rays (Cocchietto, Skert and Sava, 2002). One genus of lichen, Usnea, commonly referred to as ‘Old Man’s Beard’ (an obvious name for the scruffy, greyish-green strands), has been utilised by humans for centuries for its properties— sometimes as food, but also as medicine, as witnessed in the ninth century Al-Kindi botanical formulary (Cocchietto, Skert and Sava, 2002). Since WWII, these beard lichens have been the focus of many studies,

particularly for one compound they produce⎯ usnic acid. Usnic acid is a secondary metabolite produced by the fungal partner of Usnea spp. that has antibacterial, antiviral, anti-inflammatory, antiprotozoal, antipyretic and analgesic properties (Fitriani et al, 2019; Cocchietto, Skert and Sava, 2002; Guo et al., 2008). Because of its versatility, usnic acid is found in a variety of products, from perfume and sunscreens, toothpaste, vaginal creams, foot creams, and shampoo (Guo et al., 2008). Interest in Usnea’s antibacterial properties was renewed in the 1980s, amid increasing instances of antibiotic resistance. Studies have shown usnic acid to be an effective treatment against mycobacteria and Gram-positive bacterial, like Streptococcus mutants, and Staphylococcus aureus (Cocchietto, Skert and Sava, 2002; Guo et al., 2008). Gram-positive bacteria are characterised by thick layers of peptidoglycan surrounding the plasma membrane, and no outer membrane— which is only present in Gram-negative bacteria (Silhavy, Kahne, and Walker, 2010). The sophisticated series of membranes and peptidoglycan, called the bacterial cell envelope, provides protection by only allowing selective molecules in and out (ibid.). A review in 2002 described usnic acid’s uncoupling capabilities as the basis of its antimicrobial activity (Guo et al., 2008). An uncoupling agent disrupts oxidative phosphorylation⎯ a process used to create the energy-carrying molecule, Adenosine Triphosphate (ATP) ⎯effectively dissociating the Electron Transport Chain and the ATP Synthase. Usnic acid accomplishes this in mitochondria by diffusing across the inner membrane into the matrix, where it is ionised to form usneate anion. The anion can then diffuse back to the proton-rich inter-membrane space where it binds to a proton and reforms usnic acid. This cycle of diffusion continues, causing a proton leak which demolishes the proton gradient needed to power the ATP Synthase (Guo et al., 2008). The review concluded that the same uncoupling mechanism is used to disrupt bacterial cell membranes (ibid.). A more recent study, however, has found the inhibition of RNA and DNA synthesis is responsible for usnic acid’s antibacterial activity (Maciag-Dorszyńska, Węgrzyn, and Guzow-Krzemińska, 2014). The group added varying concentrations of usnic acid to the nutrient media of four bacterial strains and measured the incorporation of radio-labelled precursors of DNA, RNA and proteins. They found that the growth of the two Gram-positive bacteria tested was inhibited even at low concentrations of usnic acid (ibid.). Regardless of how Usnea perform their antibacterial activities, their use in medicines and other products contribute significantly to our health. However, usnic acid also has the potential to be damaging at high concentrations. Therapeutic doses of usnic acid are not concerning because the compound is slowly and inefficiently absorbed (Grass, 2017), but the toxic effects of higher concentrations in the weight loss product, LipoKinetix, prompted the Food and Drug Administration to request the manufacturer remove it from market in 2001 (Guo et al., 2008). What may be more concerning, however, is the susceptibility of Usnea to pollutants. Because Usnea are so sensitive to pollutants, their presence is often considered a sign of a healthy ecosystem (Askham, 2020). Yet Usnea readily absorb pollutants from the air and can accumulate toxic heavy metals, which can have adverse effects on both the lichen and its consumer (Grass, 2017). One of the most significant pollutants in the UK is nitrogen dioxide. This pollutant, which forms when heated nitrogen combines with oxygen, comes primarily from road traffic and is damaging to Usnea, as well as to humans (Askham, 2020). Usnea numbers have been declining in the UK due to this pollution (Pescott et al., 2015), but there is hope for recovery. A model produced by NASA has shown a reduction in nitrogen dioxide concentrations by nearly 20% since the start of the Covid-19 pandemic (Streiff, 2020). This is just one of the positive effects this empty year has had on our climate. In this past year, we have witnessed the remarkable kindness and support of strangers, and felt mentally and physically revitalised. We witnessed the beauty of wildlife returning to our towns, and watched waters clearing of

pollution (Yunus, Masago, and Hijioka, 2020). This is our final lesson. If we heed it well, as a reward for playing our part, we may yet witness the return of Usnea.

References Askham, B. (2020) Nature and pollution: what lichens tell us about toxic air. [online] Natural History Museum. [Accessed 17 Jan. 2020]. Cocchietto, M., Skert, N., and Sava, P. (2002) A review on usnic acid, an interesting natural compound. The Science of Nature, 89(4): 137146. Fitriani, L., Afifah, Ismed, F, and Bakhtiar, A. (2019) Hydrogel Formulation pf Usnic Acid and Antibacterial Activity Test Against Propionibacterium acne. Scientia Pharmaceutica, 87(1): 1-8. Grass Roots Remedies (2017). Herb Profile: Old Man’s Beard Lichen. [online] [Accessed 17 Jan. 2020]. Guo, L., Shi, Q., Fang, J., Mei, N., Ali, A., Lewis, S., Leakey, J., and Frankos, V. (2008) Review of Usnic Acid and Usnea barbata Toxicity. J Environ Sci Health C Environ Carcinog Ecotoxicol, 26(4): 317-338. Maciag-Dorszyńska, M., Węgrzyn, G., and Guzow-Krzemińska, B. (2014) Antibacterial activity of lichen secondary metabolite usnic acid is primarily caused by inhibition of RNA and DNA synthesis. Federation of European Microbiological Societies Microbiology letters, 353: 57-62. Pescott, O., Simkin, J., August, T., Randle, Z., Dore, A., and Botham, M. (2015) Air pollution and its effect on lichens, bryophytes, and lichen-feeding Lepidoptera: review and evidence from biological records. Biological Journal of the Linnean Society, 115, 611-635. Silhavy, T., Kahne, D., and Walker, S. (2010) The Bacterial Cell Envelope. Cold Spring Harbor Laboratory Perspectives in Biology, 2(5): a000414. Streiff, L. (2020) NASA model reveals how much COVID-related pollution levels deviated from the norm. [online] NASA. [Accessed 17 Jan. 2020]. Yunus, A., Masago, Y., and Hijioka, Y. (2020) Covid-19 and surface water quality: Improved lake water quality during the lockdown. Science of the Total Environment [online] 731, 1-8. [Accessed 17 Jan. 2020].

Skin

Khadija Meghrawi

You are delivered to the world in an envelope. It is the soft, flexible covering of skin. Technically the largest organ, but with the purpose of enveloping the rest of them; tissue paper that tears and stretches.

Skin has three main functions: protection, regulation, and sensation. Five different types of receptors respond to pain and touch. This is an instrument fine-tuned to each sensation. Vitamin D, essential for bone growth and energy, is a product of the touch of your skin against sunlight. Body temperature is adjusted— depending on the extent or absence of outside warmth —with a precision no thermostat could hope to achieve. Your skin also protects you from outside infection and disease, but not by shielding you. Instead, it interacts with the outside environment— your hands gloved in a living, breathing barrier through which you can still feel. Friendly microbes roam across the skin’s surface; a bustling crowd that leaves little room for more harmful infiltrates.

The composition of your skin varies across the surface of your body. Under your eyes, for example, it is thinnest, which is why it is one of the first areas to be wrinkled by the passage of time. But your body knows where it needs to grow thick skin— it’s found over the soles of the feet and the palms of your hands, where you make contact with the outside world. No hair is found there, because warmth cannot be provided at the expense of better protection against the external elements. You’re feeling everything here so much more closely.

Three layers make up your skin, and the hypodermis is the deepest layer. It is the body’s major store of fat tissue— a loose blanket of insulation, varying in size from person to person, depending on the amount of fat they have. The next layer, your dermis, is far more structured— providing tensile strength in the face of stress, while being knitted with connective tissue that cushions the body from strain. The uppermost layer of your skin contains keratinocytes. They are responsible for producing keratin, the substance that forms your protective barriers. These cells move from the bottom to the top of your skin layers and, as they do, they undergo a process of their own destruction, removing more and more of their inner components as they migrate. The higher they rise, the more of themselves they lose. Eventually, they are entirely surface— they have lost all their capacity for renewal and reproduction, now all they do is produce. The skin we see is the most superficial, and the most dead.

Your skin sheds itself every 28 days, without a trace. Reptiles leave dramatic relics behind, some discarding their entire skin in one piece. They abandon their old outsides to the world like carcasses. But the renewal that happens within us is rarely visible. Dead skin creates a billion tons of dust in the earth’s atmosphere, yet we move through the world unaware of the remains we leave behind. Your skin records, remembers. Deficiencies, disease, damage are scrawled across your body like a notebook. Warning signs of systems breaking down inside are flashed on the surface, to the outside world. Changes in your skin can sometimes signal changes in your overall health. These can be dramatic but disproportionate. Boils, while oozing and alarming, can disappear after a course of antibiotics— but all too often, they’re the only indication of something far more dangerous. Moles can be brown, small, unremarkable— and cancerous. Your chances of survival depend on how quickly you can see a change in a birthmark you’ve ignored for most of your life. A spot-the-difference game you don’t even know you’re playing— except it’s not a game, and the stakes are devastatingly high. Sometimes the signs appear and disappear as quickly as a magic trick; spider naevi are red spots that burst across the stomach like webs and indicate long-standing liver disease. Bruises aren’t

always the black and bloody evidence of destruction inflicted on you by others, sometimes they’re a stain of blood spilling out under the skin like an upturned glass. Other times, they’re markers of an underlying disorder— where your blood runs too thin, or where it cannot knit itself back together the way it should.

Sometimes, life’s marks remain. Months of malnutrition quickly become years of brittle nails and yellowing fingertips, visible even when you’re well-nourished again. If exposed to repeated friction, your skin can form a callus of additional thickness, furnishing a temporary toughness to carry you through the increased pressure. But sometimes life proves too much. You tear, ripping through layers, into sudden exposure that must quickly be covered again. You’re in no condition to protect yourself on your own anymore and must rely on being cloaked by something else— a plaster or bandage —while you heal underneath. Severe damage leaves behind scars. They’re discoloured and messily aligned because they are rapidly formed; an immediate, but illconsidered response, instead of a rehearsed plan. Their tissue is of inferior functional quality to that of the original it has replaced— less resistant to radiation, for example, and unable to reform hair follicles and sweat glands. You’ve healed, but not everything can grow back.

Your skin is not a notebook, in fact, but a page— written on, then written on again, and again— but never rewritten.