Mycology

CHAPTER EIGHT: LICHENS AND THEIR BIOLOGICAL SIGNIFICANCE

Written by MicroDok

8.1        OVERVIEW OF LICHENS

Lichen is simply a symbiotic association of slow-growing microorganisms that is composed mainly of a fungus and cyanobacteria or green algae. They are a composition of twin or double organisms, and are very rich in chemical compounds as expressed by the varying colours that they produce on the surfaces where they form. Lichens produce important secondary metabolites that are of pharmaceutical, industrial and medical importance. Lichens grow on a wide variety of surfaces including tree trunks, roof tops of houses, bare soils and rock surfaces where they form colourful growths that may include yellow, red, black, white, oranges, green and brown [Figure 8.1]. Though an association between cyanobacteria (a prokaryote) and fungi (a eukaryote) are often the most versatile lichen association known; green algae (a eukaryote) can also go into association with a fungus (a eukaryote) to form a lichen relationship. Lichens are widespread and can be found in both terrestrial and aquatic environments. They can reproduce sexually and asexually. The morphology of lichens is usually made up of a lichen thallus that comprises of fungal hyphae (used for attachment to surfaces) and photobiont or phycobiont cells (used for photosynthetic activity) from the partnering cyanobacteria or green algae.

The fungal hyphae of the lichen are the main determinants of lichen structure or morphology, and it is generally referred to as mycobiont. Cyanobacteria are assemblages of bacteria that have the innate ability to carry out oxygenic photosynthesis. The two partners in a lichen association are usually a fungus and a cyanobacteria or green algae. The fungal partner is called a mycobiont while the cyanobacteria partner is known as a phycobiont. Notably, it is not all species or genera of fungi and cyanobacteria that can form a mutualistic lichen association. Ascomycetes (commonly known as sac fungi) are the class of fungi that go into symbiotic association with a cyanobacterium to form lichens. Both organisms in a lichen association interact amongst each other on only a mutual basis. They both derive a reciprocated type of benefit from each other such as nutrient sharing and protection from untoward effects in their surrounding environment.

Figure 8.1: A photograph of lichen formation on a tree trunk. Lichen forms or produce different colouration on the surfaces it grows as depicted in this illustration.

While the fungus mainly provides structure, absorb water and provide protection for the cyanobacterium; the cyanobacteria on the other hand is highly photosynthetic and thus acts as the primary food producer by providing carbohydrates for both itself and its fungal partner in the lichenized association. Their ability to colonize any surface is based on this mutual relationship between the two organisms in the lichen association. Most lichen association use cyanobacteria as their photosynthetic partner. Due to their ability to tolerate extreme conditions in their environment, cyanobacteria are widespread and ubiquitous in the soil, water and on rock surfaces. On the surfaces of lakes, streams, rivers and ponds, cyanobacteria (for example, Nostoc spp. and Anabaena spp.) are notorious in forming blooms (community of microorganisms comprising mainly of algae and cyanobacteria) that cover water surfaces and render it almost unhygienic and dirty-looking.

8.2       CATEGORY OF LICHENS

Lichens are amongst one of the least forms of life known to mankind. Their very nature which comprises of a symbiosis of two different organisms (i.e., a fungus and a cyanobacterium) is unique; and this gives them the expertise to inhabit environmental areas which are usually harsh to other forms of microbial life. Lichens unlike other forms of microbial life, come in various colours and structures as shown in Figure 8.1; and they can inhabit a wide variety of surfaces such as tree barks, rocks, streams, wood, and leave surfaces. Lichens are usually classified based on their shape/morphology or by their growth form on their substrates. They provide microhabitats for other forms of life such as insects and other small animals. Lichens exist in three different forms including crustose lichens, fruticose lichens and foliose lichens.

  • CRUSTOSE LICHENS

Crustose lichens are crust-like lichens which usually inhabit the bark of trees, soils and rock surfaces. They have a flat structure (thallus) that is securely adhered to the lower surfaces of its substrate. The algae partner in crustose lichens is usually dispersed from their fungal partner. Crustose lichens are usually hard to remove from their attached surfaces; and the substrate on which they are growing can be damaged in the process of removal. The structure of the crustose lichen can also be damaged during removal from attached surfaces due to their strong attachment to their substrates. Crustose lichens are pressed against their substrates. They form a variety of colours that includes yellow, green and red. Crustose lichens can also be called crust or crusty, because they are known to form a crust or covering over their substrate or surface upon which they are growing. Examples of crustose lichens include Acarospora species and Lecanora species.

  • FRUTICOSE LICHENS

Fruticose lichens are the most highly developed forms of lichens. They can also be referred to as stalked lichens due to their structure and ability to form fruiting bodies. Fruticose lichens have different top and bottom layer; and their algae partner is usually within the fungal partner which forms a round branching fungal layer on the outside. Structurally, fruticose lichens are hair-like, upright and shrubby; and they can also be called shrubby due to their characteristic morphology that resembles the beard of an old man. Usnea species, the source of usnic acids used as potential lead compounds for antiviral drug development belong to this category of lichens. Fruticose lichens form on trees and on soils; and they generally have a vertical growth pattern even though some may assume flat branches that tangle or coil with each other.

  • FOLIOSE LICHENS

Foliose lichens are also known as leafy lichens due to their characteristic morphology. Lichens in this category are leafy-like in nature; and they are made up of several bumps and ridges that also define their morphology. They are leaf-like lichens which also form on tree trunks and rock surfaces. Foliose lichens have their algae partner in the middle of the surrounding fungal layer; and they usually have different top and bottom layers. They have a characteristic puffed body with a black undersurface. Examples of foliose lichens include Pseudocyphellaria species and Hypogymnia species.

8.3     SYNOPSIS OF LICHEN METABOLISM

All microorganisms carry out two modes of metabolism during their lifetime, and these are mainly primary metabolism and secondary metabolism. Primary metabolism is very indispensable to the survival of all microbial cells as it is during this metabolic activity that important compounds (known as primary metabolites) such as nucleic acids, amino acids, vitamins and enzymes are synthesized, broken down and utilized for the sustenance of the organism. Primary metabolism is very significant to the survival of microorganisms and once inhibited, the organism loses its viability and dies. These metabolic intermediates produced in primary metabolism are mainly synthesized during the logarithmic (exponential) phase of their growth. On the other hand, microbial cells produce other classes or types of metabolic intermediates after their normal development (usually at the stationary stage of growth). These other class of compounds have no implications whatsoever on the growth or sustenance of the organism. These compounds are known as secondary metabolites.

The process by which these other groups of metabolic intermediates are produced is called secondary metabolism; while the compounds produced are known as secondary metabolites. Secondary metabolites are often regarded as microbial by-products and examples include: antibiotics, steroids, enzyme inhibitors, immunomodulating agents, alkaloids, toxins and other range of bioactive and antimicrobial products. A large pool of secondary metabolites of microbial origin have been discovered and harnessed to improve the health and living standards of humanity, animals and even plants in terms of: better medication, better foods, improved crop production, enhanced industrial processes and environmental sustainability. Secondary metabolites unlike primary metabolites have no role whatsoever on the growth and reproduction of a microbial cell. They are therefore the natural products of microorganisms (including the lichens).

Many secondary metabolites from microorganisms and other natural sources such as lichens form the lead sources of bioactive compounds for the development of novel drugs and other pharmaceuticals because of their recognized antimicrobial potentials. Lichens exhibit a complex biochemical pathway which gives credence to the vast amount of bioactive compounds that they synthesize. Over 800 secondary metabolites (known as lichen acids) are known to be synthesized by lichens. These lichen acids are usually insoluble in water, and they serve a variety of functions in the lichen association including protection from other competing or rival organisms in their surrounding environments. Lichen acids are the secondary metabolites produced by lichens, and they possess significant bioactive activities. The production of secondary metabolites by lichens is mediated by three key biochemical/biosynthetic pathways in the lichenized fungi, and these pathways include polyketide pathway, mevalonate pathway and shikimic acid pathway.

8.3.1  THE POLYKETIDE (ACETYL-POLYMALONYL) PATHWAY

The polyketide (acetyl-polymalonyl) pathway make use of acetyl-CoA and malonyl-CoA (both derivatives of coenzyme A) to synthesize lichen acids. The secondary metabolites produced by this pathway include dibenzofurans, depsidones, depsones, depsides, usnic acids, chromones, xanthones, and anthraquinones. Acetyl-polymalonyl biosynthetic pathway is derived from the polymalonyl pathway, and a large group of lichens produce their secondary metabolites via this pathway. This biosynthetic pathway is responsible for the synthesis of most of the secondary metabolites produced by lichens. Usnea species lichens which produces usnic acid with potent antiviral activity use this pathway to produce their secondary metabolites. Usnic acid is known to be efficacious against some viral candidates such as Arenoviridae viruses. Usnic acid is also used as a lead compound in the development of potent antiviral agents.

8.3.2  THE MEVALONATE PATHWAY

The secondary metabolites produced by this pathway include diterpenes, triterpenes, carotenoids, and steroids. Mevalonate biosynthetic pathway is also used by other organisms aside lichens to produce secondary metabolites. It produces more secondary metabolites than the shikimic acid pathway. The mevalonate biosynthetic pathway is derived from the acetyl-CoA of the glycolytic pathway. Heterodermia species lichens use this pathway for the synthesis of its secondary metabolites.

8.3.3  THE SHIKIMIC ACID PATHWAY

Shikimic acid pathway is a biochemical pathway that plays significant role in the metabolism of carbohydrates and aromatic amino acids. Lichens make use of this pathway for the synthesis of some of its secondary metabolites. Pulvinic acid and terphenylquinones are the secondary metabolites produced by this pathway. Shikimic biosynthetic pathway is derived from the pentose phosphate cycle and amino-acid biosynthesis. This biosynthetic pathway which is only unique to lichens produces only a small group of lichen secondary metabolites including pulvinic acid derivatives which often appear as bright yellow pigments. The Acarospora species and Candelariella species lichens makes use of this pathway to produce their secondary metabolites. Majority of the secondary metabolites produced by lichens are produced by the polyketide biosynthetic pathway (acetyl-polymalonyl) with only few of these metabolic intermediates produced by the mevalonate and shikimic pathway respectively.

8.4    SOME SPECIFIC FUNCTIONS OF LICHEN ACIDS (SECONDARY METABOLITES)

Lichens produce two types of metabolites: primary metabolites (for example, carbohydrates and amino acids) and secondary metabolites (for example, alkaloids and lichen acids). Primary metabolites (which are intracellularly secreted) are critical to the survival of the lichens while secondary metabolites are rarely involved in the metabolism or growth of the lichenized fungi. Secondary metabolites of lichens are generally called lichen acids, and they are usually deposited on the surface of the lichen hyphae. Thus, secondary metabolites of lichens are extracellular secretions of lichenized fungi, and they are primarily produced by the mycobiont (i.e., the fungi partner) of the lichen formation. Lichen acids exhibit numerous amounts of biological and non-biological activities; and these have been exploited by mankind to solve many health related and non-health problems. The secondary metabolites produced by lichens (which are numerous) are unique, and they are rarely sourced from other natural sources. It is noteworthy that lichens only produce secondary metabolites when a suitable fungus is in association with a functional and compatible cyanobacterium and/or green algae. Thus, a suitable fungal partner and an appropriate phycobiont are essential for the secretion of biologically active compounds of lichens. However, some of the biological functions or activities of lichen secondary metabolites are elucidated in this section.

  • Lichen acids protect the cyanobacteria (phycobiont) from drying.
  • They serve as anti-herbivores, thus preventing herbivorous animals from feeding on them.
  • They protect the lichenized formation from possible microbial assault.
  • They are used in the systematic and phylogeny of lichen classification.
  • Lichen acids are used as lead compounds in drug development.
  • They are used in the formulation of dyes, perfumes and even food.
  • Lichen secondary metabolites possess anti-tumor, antiviral and cytotoxic activities.
  • They help make the lichenized association to be pollution tolerant.
  • Lichen secondary metabolites are used for the development of antibiotics, analgesics, anti-pyretics, and antioxidants.

8.4.1  ANTIMICROBIAL PROPERTIES OF LICHEN SECONDARY METABOLITES

Lichens possess varying antimicrobial properties; and they have been shown to be active against a plethora of pathogenic microorganisms including bacteria, fungi and viruses. Lichens and lichen compounds have long been used by Native Americans, the Chinese, Europeans, Africans and the Indians as not just medicinal agents (because of the bioactive constituents that they inherently possess) but as important source of food, and for other industrial and economic purposes. The versatile and well-documented bioactive nature of lichen secondary metabolites often referred to as lichen acids is very promising for the development of potent antimicrobial agents. Lichens have been used since time immemorial for different medicinal purposes and this is due to the fact that their secondary metabolites (i.e., lichen acids) contain unique biologically active compounds that serve many antimicrobial purposes. These macro-fungi population (a community of fungi and cyanobacteria) have attracted the attention of researchers, industrialists and professionals in the medical and pharmaceutical industry because of the important bioactive compounds that they synthesize. The biological and/or antimicrobial activities of lichen secondary metabolites are numerous, and they include: antibacterial activity, antifungal activity, antiviral activity, anti-inflammatory, antipyretic activity, anti-herbivore activity and cytotoxic activity. These have been briefly summarized in Table 8.1 of this section.

8.4.2  ANTIBACTERIAL ACTIVITY OF LICHENS

Lichen secondary metabolites possess antibacterial activity. They exhibit significant level of inhibitory effect on both Gram positive and Gram negative bacteria. Some lichens with antibacterial activity include those in the genus Ramalina, Parmelia, Umbilicaria, and Cladonia. Some available synthetic conventional antibiotics are not too effective for the treatment of some bacterial related infectious diseases owing to the growing level of antibiotic resistance in pathogenic bacteria. Usnic acid, salazinic acid, stictic acid, and vulpinic acid are some examples of lichen secondary metabolites that have been effective to inhibit pathogenic bacteria effectively. Thus, lichen acids known to have sizeable antibacterial activities could serve as lead compounds in the development of novel antibacterial agents to contain the upward trend in bacteria resistance to some antibiotics.

Table 8.1: Synopsis of antimicrobial activities of some lichens

Lichen

Reported antimicrobial activity

Pathogen

References

Parmelia perlata (L.) Ach. Antiviral Yellow fever virus, polio virus Esimone et al., (2007)
Ramalina farinacea Antiviral HIV-1, Respiratory synctial virus (RSV) Esimone et al., (2009)
Ramalina farinacea Antiviral Adenoviruses, herpes simplex virus (HSV) Esimone et al., (2009)
Ramalina celastri Antiviral Arenavirus Fazio et al., (2007)
Caloplaca regalis Antibacterial Gram positive bacteria Paudel et al., (2008)
Usnea ghattensis (G.) Awasthi Antibacterial Gram positive and Gram negative bacteria Srivastava et al., (2013)
Roccella belangeriana (Awasthi) Antibacterial Gram negative bacteria Devi et al., (2011)
Caloplaca cerina Antifungal Fungi Manojlovic et    al.,  (2005)
Rubia tictorum Antifungal Fungi Same as above
Rhamnus frangula Antifungal Fungi Same as above

8.4.3  ANTIVIRAL ACTIVITY OF LICHENS

Lichen acids also exhibit antiviral activities against some human viral pathogens including respiratory synctial virus (RSV), herpes simplex virus (HSP), human papillomavirus virus (HPV), arenaviruses, and adenoviruses. Lichens exhibit antiviral activities aside other antimicrobial actions they express, and thus could be used as potential drug candidates for the development of novel antiviral drugs. Usnic acid and parietin produced by the lichen genera Usnea and Ramalina are some lichen compounds with antiviral activity.

8.4.4  ANTICANCER OR ANTIPROLIFERATIVE ACTIVITY OF LICHENS

Lichens possess antitumour or anticancer activity. They inhibit some malignant cancerous growth, and even cause apoptosis (programmed cell death) in other related tumours. Usnic acid is one of the widely studied lichen acids, and it has been found to be very effective in addition to other secondary metabolites to inhibit some human cancerous cell lines such as breast cancer cell and prostate cancer cell lines. Lichen secondary metabolites (especially usnic acid) have been found to effectively inhibit the cell growth and proliferation of some human cancerous cell lines. The reported apoptotic activity and anti-mutagenic effect of lichen secondary metabolites is promising in developing novel anticancer drugs.

8.4.5  ANTI-HERBIVORE ACTIVITY OF LICHENS

Secondary metabolites of lichens also protect lichens against herbivorous invertebrates that usually feed on them. Lichens derive survival benefits from the secondary metabolites they synthesize as these compounds have the potential to ward off herbivores and other invertebrates that may want to prey or feed on them.

8.4.6    ANTIFUNGAL ACTIVITY OF LICHENS

The secondary metabolites of lichens (for example, usnic acid) also possess antifungal activity against some fungal species (for example, Candida albicans and Aspergillus). Usnea species, Calaplaca and Parmelia are some lichenized fungi with antifungal activities.

8.4.7  OTHER BIOLOGICAL ACTIVITY OF LICHENS

The wide variety of antimicrobial activity expressed by secondary metabolites of lichens on other organisms including animals and microbes makes them putative composites for the development of antiviral agents. Other reported biological activities of lichen secondary metabolites are antipyretic activity, anti-cytotoxic activity, and anti-inflammatory and antioxidant activity. The huge secondary metabolites produced by lichens stand out to be the cure and answer to the growing demand of potent antimicrobial agents (inclusive of antibacterials, antifungal and antivirals) due to the pertinent and growing nature of multidrug resistant strains of pathogenic microbes now experienced in the health sector world over. Thus, it is critical to step up research towards harnessing some of these good qualities of lichen secondary metabolites especially in the area of developing novel antimicrobial agents for therapeutic purposes. Aside their strong antimicrobial activities and application in the medical and pharmaceutical industry, lichens are also used as food or fodder, dyes and perfumes. Lichens provide their own food; and as a producer, they can provide food for other organisms in the ecosystem. Lichens can also serve as habitat for other organisms including insects, and other small invertebrates that may use lichen formation to camouflage from potential prey in their ecosystem. Though lichens are slow-growing in nature; lichen secondary metabolites holds sway to revolutionized healthcare delivery across the world in terms of better therapeutic agents and other biological significance which they confer.

References

Anaissie E.J, McGinnis M.R, Pfaller M.A (2009). Clinical Mycology. 2nd ed. Philadelphia, PA: Churchill Livingstone Elsevier. London.

Bačkorová M, Jendželovský R, Kello M, Bačkor M, Mikeš J, Fedoročko P (2012). Lichen secondary metabolites are responsible for induction of apoptosis in HT-29         and A2780 human cancer cell lines. Science Direct, 26(3)462-468.

Baumgardner D.J (2012). Soil-related bacterial and fungal infections. J Am Board Fam Med, 25:734-744.

Beck R.W (2000). A chronology of microbiology in historical context. Washington, D.C.: ASM Press.

Calderone R.A and Cihlar R.L (eds). Fungal Pathogenesis: Principles and Clinical Applications. New York: Marcel Dekker; 2002.

Chakrabarti A and Slavin M.A (2011). Endemic fungal infection in the Asia-Pacific region. Med Mycol, 9:337-344.

Champoux J.J, Neidhardt F.C, Drew W.L and Plorde J.J (2004). Sherris Medical Microbiology: An Introduction to Infectious Diseases. 4th edition. McGraw Hill Companies Inc, USA.

Chung K.T, Stevens Jr., S.E and Ferris D.H (1995). A chronology of events and pioneers of microbiology. SIM News, 45(1):3–13.

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