Lichen

A lichen is a stable, self-sustaining composite organism arising from the mutualistic symbiosis between a structural filamentous fungus—the mycobiont—and one or more extracellular photosynthetic partners—the photobionts, which may be eukaryotic green microalgae (chlorobionts) or prokaryotic cyanobacteria (cyanobionts). Rather than existing as a simple mixture of cells, lichenization triggers a coordinated developmental program in the fungal partner, producing a differentiated, layered vegetative body (thallus) that bears no morphological resemblance to either symbiont grown in isolation and enables lichens to colonize approximately 6–8% of Earth's terrestrial surface, from polar nunataks and alpine scree to hyper-arid deserts and tropical rainforest canopies.

For centuries following Theophrastus (c. 300 BCE, who coined leichen for cortical growths on olive bark) and Carl Linnaeus (1753), naturalists classified lichens as a single autonomous group of primitive plants between algae and mosses. In 1867, the Swiss botanist Simon Schwendener proposed the dual hypothesis of lichens, demonstrating microscopically that the colourless filamentous framework of a lichen is a fungus enveloping captive algal cells (gonidia). Although initially rejected by leading lichenologists who viewed symbiosis as impossible, Schwendener's discovery inspired Albert Bernhard Frank (1877) and Heinrich Anton de Bary (1879) to coin the biological term symbiosis ("living together").

In 2016, Toby Spribille and colleagues (Science) demonstrated through metatranscriptomics and fluorescence in situ hybridization that the upper cortex of many parmelioid macrolichens (such as Bryoria fremontii and Bryoria tortuosa) harbors a third obligate partner: unicellular basidiomycete yeasts in the class Cystobasidiomycetes, alongside a structured bacterial microbiome (bacteriobiont). Under the International Code of Nomenclature for algae, fungi, and plants, the scientific binomial of a lichen refers strictly to its primary mycobiont.

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The Mycobiont (Fungal Partner)

Approximately 20,000 described fungal species (~20% of all known fungi) are obligate lichen-formers. Because the lichen lifestyle has evolved independently at least 8–12 times across Dikarya and Beenkenia via coevolution with photobionts, lichens represent a polyphyletic nutritional guild rather than a single monophyletic taxon:

• Ascomycota (~98% of all lichens): Nearly all ascolichens belong to the subphylum Pezizomycotina, predominantly within the class Lecanoromycetes (~15,000 species, including Cladonia, Parmelia, Usnea, and Xanthoria), alongside Arthoniomycetes, Dothideomycetes, Eurotiomycetes (order Verrucariales), and Lichinomycetes.
• Basidiomycota (~2% of all lichens): Basidiolichens belong to Agaricomycetes—such as the arctic-alpine mushroom lichen Lichenomphalia umbellifera, the tropical bracket-like Cora glabrata (Dictyonema), and Multiclavula—in addition to the widespread cortical Cystobasidiomycetes yeasts embedded in ascolichen thalli.

The Photobiont (Photosynthetic Partner)

In stark contrast to the ~20,000 mycobiont species, fewer than 150 photobiont species (across ~40 genera) account for the vast majority of lichen symbioses:

• Chlorolichens (~85% of lichens): Partner with unicellular or filamentous green microalgae (Chlorophyta, chiefly class Trebouxiophyceae and Ulvophyceae). The single genus Trebouxia (and the closely related Asterochloris) associates with over 50% of all known lichens, while filamentous Trentepohlia (rich in orange β-carotene pigments) dominates crustose and epiphytic lichens in humid subtropical and tropical forests.
• Cyanolichens (~10% of lichens): Partner exclusively with filamentous or colonial cyanobacteria—chiefly Nostoc, Scytonema, Stigonema, or Gloeocapsa—which perform both oxygenic photosynthesis and biological nitrogen fixation.
• Tripartite Lichens (~3–4% of lichens): Foliose and fruticose macrolichens such as lungwort (Lobaria pulmonaria), Peltigera aphthosa, and Stereocaulon house green microalgae as the primary carbon-fixing photobiont across the main thallus while sequestering Nostoc cyanobacteria inside specialized internal or external gall-like pockets called cephalodia, where low O₂ tension protects the oxygen-sensitive nitrogenase enzyme complex.

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Heteromerous vs. Homoiomerous Thallus Architecture

Most foliose and fruticose lichens possess a stratified (heteromerous) thallus (~100–1,000 μm thick) differentiated into four functional tissue layers:

1. Upper Cortex: A dense, tightly cemented outer layer (10–60 μm thick) of conglutinated fungal hyphae forming a pseudoparenchymatous tissue embedded in hydrophilic extracellular polysaccharides (lichenan and isolichenan). The upper cortex provides mechanical protection, limits evaporative water loss, and accumulates crystallized UV- and high-light-screening secondary metabolites (such as yellow usnic acid, orange parietin in Xanthoria parietina, or dark melanins).
2. Photobiont (Algal) Layer: Directly beneath the upper cortex lies a continuous or discontinuous band (30–100 μm thick) where photobiont cells are enveloped by specialized fungal appressoria or intracellular wall-contact haustoria. This sub-cortical depth optimizes photosynthetically active radiation (PAR, 400–700 nm) while facilitating rapid CO₂ diffusion.
3. Medulla: Making up the bulk of the thallus thickness (100–500 μm), the medulla consists of loosely interwoven, thick-walled fungal hyphae separated by extensive air spaces. To prevent waterlogging from blocking internal CO₂ diffusion during wet metabolic periods, medullary hyphae are coated in a hydrophobic layer of rodlet proteins (hydrophobins) and crystallized depsides or depsidones, maintaining air-filled gas channels flanked by cyphellae or pseudocyphellae (breathing pores).
4. Lower Cortex and Attachment Structures: A compacted ventral fungal layer that anchors the thallus to rock, bark, or soil via root-like hyphal bundles (rhizines), a felt-like tomentum, or a single central holdfast (umbilicus, as in rock tripe Umbilicaria).

By contrast, gelatinous cyanolichens (such as Collema and Leptogium) possess an unstratified (homoiomerous) thallus in which fungal hyphae and Nostoc chains are distributed uniformly within a mucilaginous polysaccharide matrix.

Major Morphological Growth Forms and Reproduction

Lichen thalli are classified into six primary morphological growth habits:

• Crustose: Tightly appressed crusts lacking a lower cortex whose medullary hyphae penetrate directly between mineral grains of rock or bark cells, making them impossible to remove intact (e.g., yellow map lichen Rhizocarpon geographicum, Caloplaca).
• Squamulose: Composed of small, overlapping scale-like lobes partially lifted from the substrate (e.g., the primary basal thallus of Cladonia pixie-cup lichens).
• Foliose: Dorsiventrally flattened, leaf-like lobes with distinct upper and lower cortices attached loosely by rhizines (e.g., Parmelia sulcata, Flavoparmelia caperata, Xanthoria parietina).
• Fruticose: Three-dimensional, radially symmetric or strap-shaped branching shrubs or pendulous beard-like strands attached at a single basal holdfast (e.g., reindeer lichen Cladonia rangiferina, old man's beard Usnea, oakmoss Evernia prunastri).
• Leprose: Powdery masses of fungal hyphae and algal cells lacking any cortical organization (e.g., Lepraria incana).
• Gelatinous: Homoiomerous, dark rubbery thalli that swell to many times their dry volume when hydrated (e.g., Collema).

Lichens reproduce via two contrasting pathways:

• Vegetative Co-Dispersal (Symbiotic Propagules): To disperse both partners simultaneously, lichens produce soredia (microscopic powdery clusters of a few photobiont cells wrapped in fungal hyphae, erupted from cortical soralia) or isidia (corticated, finger-like or cylindrical outgrowths of the upper surface that detach brittlely under mechanical abrasion or raindrop impact).
• Sexual Reproduction (Mycobiont Only): The fungal partner forms cup-shaped apothecia or flask-shaped perithecia, ejecting sexual meiotic ascospores that contain no algal cells. To survive, a germinating ascospore must encounter and capture a compatible free-living photobiont cell on the substrate (horizontal re-lichenization).

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Bidirectional Carbon, Nitrogen, and Polyol Transport

Using ¹⁴CO₂ pulse-chase autoradiography in the 1960s, David C. Smith and David H. Lewis elucidated the biochemical currency of the lichen symbiosis. In the lichenized state, the fungal partner renders the photobiont plasma membrane permeable to fixed carbon, causing the photobiont to export 70–90% of its total photosynthate to the mycobiont within minutes of fixation:

• Chlorobiont Sugar Alcohol (Polyol) Export: Green algal photobionts synthesize and export acyclic polyols—specifically five-carbon ribitol (in Trebouxia, Asterochloris, and Coccomyxa), four-carbon erythritol (in Trentepohlia), or six-carbon D-sorbitol (in Hyalococcus).
• Cyanobiont Glucose and Ammonium Export: Cyanobacterial partners (Nostoc) export D-glucose directly to the fungus. Simultaneously, the mycobiont suppresses about 90% of the cyanobiont's own glutamine synthetase activity, forcing Nostoc heterocysts (which rise from ~4% of cells in free-living Nostoc to 20–35% in cephalodia) to release newly fixed ammonium (NH₄⁺) into the fungal apoplast via the nitrogenase reaction:

N₂ + 8 H⁺ + 8 e⁻ + 16 ATP → 2 NH₃ + H₂ + 16 ADP + 16 P_i

• Fungal Sink Conversion: Upon absorbing ribitol, erythritol, sorbitol, or glucose, the mycobiont immediately converts the imported carbohydrate into the fungal hexitol D-mannitol and the pentitol D-arabitol. Because photobionts cannot metabolize mannitol, this biochemical one-way valve maintains a steep concentration gradient driving continuous carbon efflux from photobiont to mycobiont while supplying polyols that act as non-toxic osmolytes and cryoprotectants.

Poikilohydric Anhydrobiosis and Astrobiological Extremotolerance

Unlike vascular plants, lichens lack roots, vascular xylem/phloem, and waxy cuticular stomata. They are poikilohydric: their internal water content equilibrates passively with atmospheric relative humidity, dew, fog, and precipitation. During drought, a lichen dries down to 2–10% water content by dry weight and enters anhydrobiosis (metabolic cryptobiosis), stabilizing cell membranes and photosynthetic reaction centers with high intracellular concentrations of D-mannitol, arabitol, sucrose, and antioxidative glutathione. Upon rewetting by morning dew or humid air, respiration resumes within seconds and net photosynthesis recovers within minutes.

This anhydrobiotic architecture confers resistance to extreme physical stressors. In 2005, aboard the European Space Agency's BIOPAN-5 facility on the Russian Foton-M2 satellite, thalli of the alpine-polar crustose lichens Rhizocarpon geographicum and Xanthoria elegans were exposed directly to outer-space hard vacuum (10⁻⁷ Pa), cosmic radiation, temperature swings from −20 °C to +20 °C, and full solar ultraviolet radiation (λ > 110 nm) for 14.6 days. Upon return to Earth, both species recovered full photosystem II quantum yield (F_v/F_m) and mycobiont viability within 24 hours of rehydration.

Pedogenesis, Lichenometry, and SO₂ Air-Quality Bioindication

Lichens synthesize over 1,000 unique secondary metabolites ("lichen substances," comprising 1–30% of dry thallus weight) via the fungal acetate-polymalonate polyketide pathway, including depsides (atranorin, lecanoric acid), depsidones (salazinic and fumarprotocetraric acids), and dibenzofurans (usnic acid). Secreted onto mineral surfaces alongside oxalic acid, these phenolic acids act as multidentate ligands that chelate metal cations (Fe³⁺, Al³⁺, Mg²⁺, Ca²⁺) from basalt, granite, and limestone. Combined with hyphal turgor wedging, lichen biogeochemical weathering accelerates silicate dissolution by 10- to 100-fold, driving primary soil formation (pedogenesis) and drawing down atmospheric CO₂ over geological timescales.

Because crustose lichens such as Rhizocarpon geographicum grow radially at slow, predictable rates (0.05–1.5 mm yr⁻¹) and live for 1,000 to >5,000 years, geomorphologists use the maximum thallus diameter on exposed boulders to date Little Ice Age and Holocene glacial moraines—a geochronological technique invented by Roland Beschel (1950) termed lichenometry.

Conversely, because lichens absorb water and dissolved gases directly across their entire thallus surface without a protective cuticle or deciduous leaf shedding, they are acutely sensitive to atmospheric sulfur dioxide (SO₂) and acid deposition—a phenomenon closely linked to historical industrial melanism in peppered moths (Biston betularia). Dissolved SO₂ hydrates into sulfurous acid and bisulfite ions (HSO₃⁻):

SO₂ + H₂O ⇌ H⁺ + HSO₃⁻ ⇌ 2 H⁺ + SO₃²⁻

At cortical pH < 4.5, H⁺ and HSO₃⁻ displace the central Mg²⁺ ion from the tetrapyrrole porphyrin ring of photobiont chlorophyll a, irreversibly degrading it into grey-brown phaeophytin a and halting photosynthesis:

Chlorophyll a [Mg²⁺] + 2 H⁺ → Phaeophytin a [2H⁺] + Mg²⁺

In 1970, David L. Hawksworth and Francis Rose calibrated a 10-zone qualitative epiphytic lichen scale across England and Wales correlating species assemblages directly with mean winter atmospheric SO₂ concentrations (from Zone 0 "lichen deserts" at >170 μg SO₂ m⁻³ to Zone 10 old-growth Lobaria and Usnea communities at <10 μg SO₂ m⁻³).

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Why do green-algal lichens export sugar alcohols (polyols) whereas cyanolichens export glucose?

In the lichenized state, green algal photobionts (Trebouxia, Trentepohlia) channel Calvin-cycle triose phosphates into acyclic polyols (ribitol, erythritol, or sorbitol), which double as compatible osmolytes that protect membranes during repeated desiccation–rehydration cycles. Cyanobacteria (Nostoc) lack the polyol biosynthetic pathway and instead enzymatically cleave intracellular glucan storage granules into free D-glucose. In both cases, the mycobiont converts the imported sugar into D-mannitol, maintaining a one-way concentration gradient.

How does sulfur dioxide (SO₂) pollution kill lichens?

Because lichens lack a waxy cuticle or stomata, gaseous SO₂ dissolves directly into the hydrated thallus film to form acidic bisulfite ions (HSO₃⁻) and protons (H⁺). Under acidic conditions, protons strip the central Mg²⁺ ion out of the photobiont's chlorophyll a porphyrin ring, converting it into non-functional phaeophytin a, while bisulfite ions generate free radicals that bleach thylakoid membranes and inactivate cyanobacterial nitrogenase.

What role do basidiomycete yeasts play in the lichen symbiosis?

Discovered by Toby Spribille and colleagues in 2016, unicellular Cystobasidiomycetes yeasts are embedded within the polysaccharide matrix of the upper cortex of many macrolichens. Metatranscriptomic analyses demonstrate that these cortical yeasts remain metabolically active alongside the primary ascomycete mycobiont and influence cortical architecture and secondary metabolite synthesis, such as the accumulation of toxic vulpinic acid in Bryoria tortuosa vs. Bryoria fremontii.

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1. Schwendener, S. (1869). Die Algentypen der Flechtengonidien. Basel: C. Schultze. https://doi.org/10.3931/e-rara-26646
2. Hawksworth, D. L., & Rose, F. (1970). "Qualitative scale for estimating sulphur dioxide air pollution in England and Wales using epiphytic lichens." Nature, 227(5254), 145–148. https://doi.org/10.1038/227145a0
3. Sancho, L. G., de la Torre, R., Horneck, G., Ascaso, C., de los Rios, A., Pintado, A., Wierzchos, J., & Schuster, M. (2007). "Lichens survive in space: results from the 2005 LICHENS experiment." Astrobiology, 7(3), 443–454. https://doi.org/10.1089/ast.2006.0046
4. Spribille, T., Tuovinen, V., Resl, P., Vanderpool, D., Wolinski, H., Aime, M. C., Schneider, K., Stabentheiner, E., Toome-Heller, M., Thor, G., Mayrhofer, H., Johannesson, H., & McCutcheon, J. P. (2016). "Basidiomycete yeasts in the cortex of ascomycete macrolichens." Science, 353(6298), 488–492. https://doi.org/10.1126/science.aaf8287