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Secondary metabolite variability in lichen genus Usnea in India: A potential

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G- Journal of Environmental Science and Technology 2(3): (2014) ISSN (Online): 2322-0228 (Print): 2322-021X

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Secondary metabolite variability in lichen genus Usnea in India: A potential source for
bioprospection
P. Shukla1, 2*, D.K. Upreti1 and L.M. Tewari2
1
Lichenology Laboratory, CSIR-National Botanical Research Institute, Rana Pratap Marg, Lucknow – 226001, U.P., INDIA
2
Department of Botany, DSB Campus, Kumaun University, Nainita, Uttarakhand- 263001, INDIA

ARTICLE INFO ABSTRACT

Received: 13 Jan 2015 The species of lichen genus Usnea are well known for their worldwide distribution and
medicinal properties due to presence of usnic acid. The genus is represented by more than 300
Revised : 20 Jan 2015
species in the world out of which 57 species are reported from India. In India, the species of
Accepted: 08 Feb 2015 Usnea grows profusely in higher altitudes of Western Ghats and Himalayan regions. 20 different
secondary metabolites are known from Indian Usnea species which have potential biological
and physiological significance. Salazinic acid, stictic acid, norstictic acid and barbatic acid are
Key words:
the most dominant secondary metabolites along with usnic acid. Apart from the natural thalli the
Usnic acid, mycobiont, natural cultivated mycobiont of Usnea species also produced many of these compounds in culture
products, secondary conditions. The secondary compounds present in Usnea species are significant source of natural
metabolites, species products for commercial uses.

1) INTRODUCTION Himalaya. The species of Usnea are known to be used in

Lichens are dual organism known to produce variety of traditional medicines, in dyeing and in spices in various parts
secondary metabolites that act as defence molecules against of the country. U. longissima Ach. has been widely used as
physical stress and biological attacks during their slow growth expectorant, as a wound dressing and in the treatment of ulcers
in nature [1] and involved in maintaining symbiotic The ‘Baiga’, a primitive tribe of Madhya Pradesh used this
equilibrium [2, 3]. Being a symbiotic organism, the secondary species along with other ingredients for treating bone fracture
metabolites produced by lichens are unique with respect to [7]. In Unani literature the medicinal use of Usnea spp. are
those of higher plants. The secondary metabolites in lichens mentioned as astringent, antidote, analgesic, cardiotonic,
are produced by mycobiont [4], that accumulate on resolvent and stomachic [8].
extracellular surface of fungal hyphae. Since synthetic drugs cause numerous side effects and
Lichens have evolved metabolic pathways to synthesize pathogenic micro-organisms develop antibiotic resistance, the
secondary metabolites, mainly Acetyl-polymalonate pathway natural compounds present in Usnea spp., are of great interest.
(APP), Shikimic acid pathway (SAP) and Mevalonic acid In recent years, Malhotra et al. [9] evaluated the bioactivity of
pathway (MAP). Most of the lichen compounds are phenolic various extracts of Usnea species and recorded their role in
compounds that come under orcinol/β-orcinol derivatives, discovery of new drugs. Santiago et al. [10] and Sultana &
dibenzofuranes, usnic acid, depsides (e.g. barbatic acid) & Afolayan [11] studied the antitumor activity, antioxidant
depsidones (e.g. salazinic acid). Due to the presence of useful activity and antimicrobial activity of Usnea spp., against
metabolic compounds, lichens are in use for medicines, various plants and animal pathogens. Rowe et al. [12] and
perfumes, dyes, cosmetics and as food from the ancient times. Cocchietto et al., [13] studied the wide-spectrum antibiotic
Many lichen secondary metabolites exhibit cytotoxic, properties of Usnea spp. Singh et al. [14] reported that novel
antibiotic and antiviral properties and reported as potential herbo-metallic preparation (nanoparticles) using extracts of U.
source of pharmaceutically useful chemicals [5]. The species longissima can inhibit bacterial quorum sensing. The isolated
of lichen genus Usnea are most common among the different usnic acid has also been commercialized and is widely used as
lichen groups used for mankind. constituent of pharmaceutical preparations like herbal
Lichen genus Usnea is globally distributed with more than 300
species [6]. In India, 57 species of Usnea are known which
grow luxuriantly in higher regions of Western Ghats and * Corresponding Author: M/s Preeti Shukla
Email address: pre.1988@gmail.com
29
medicines and cosmetics. Apart from usnic acid the Usnea bioactivity of lichen substances ranges from antimicrobial,
species also produced a number of beneficial bioactive antiviral, antitumor, antioxidant to analgesic, antipyretic and
secondary metabolites which are not so far identified, isolated cardiovascular protective activities. The number of lichen
and characterized. secondary metabolites with specific biological activities is
The present study is aimed to list all the potent and useful given in figure 2.
secondary metabolites other than usnic acid, present in the Majority of lichen substances present in Indian Usnea species
Indian lichen species of Usnea and their biological activity so have antimicrobial properties against plants and animal
far known. pathogens indicating that Indian Usnea species can be used as
potential source of pharmaceutical medicines, herbal
2) MATERIALS AND METHODS pesticides and microbicides.
More than 1500 specimens of lichen genus Usnea housed in Some lichen substances are antitumor agent while others are
herbarium of CSIR ̶ National Botanical Research Institute , antioxidant in nature. Only few lichen substances of Indian
Lucknow (LWG) were studied. The morphological and Usnea species are reported to be analgesic, antipyretic and
anatomical characters of species were examined using Leica cardiovascular protective activities.
S8APO stereo zoom microscope and Leica DM 500 micro-
system. The species were segregated using relevant keys and 4) CONCLUSION
monographs [15, 16, 17]. The chemistry of the species was According to Culberson et al. [37] and Stocker-Worgotter et
carried out using micro-crystallography and Thin Layer al. [38], the chemical variation in lichens seems to be
Chromatography (TLC) in solvent system A (180 ml toluene: genetically determined but the induction of biosynthetic
60 ml 1,4 dioxane: 8 ml acetic acid) and in solvent system C pathways for production of secondary metabolites is also
(85 ml Toluene: 15 ml acetic acid) following Orange et al. influenced by physiological and environmental factors. The
[18]. unique micro-climatic conditions prevailing in Indian
subcontinent makes it suitable habitat for chemically diverse
3) RESULTS AND DISCUSSION species of lichens, like that of Usnea. The variable abiotic
The Indian species of lichen genus Usnea contain many environmental factors of different geographic regions of the
biologically active secondary metabolites out of which only 21 country influence the production of lichen substances in
compounds have been isolated and identified till now (Table Usnea species resulting in high degree of chemotypes
1). Out of 57 Usnea species reported from the country, 12 formation.
species have more than one chemotypes. U. longissima, has The chemical variability in Indian Usnea species can serve as
maximum number of chemotypes as seven, followed by U. source of valuable bio-products and are potential source of
dasaea Stirt. and U. subfloridana Stirt which have five and bio-prospection.
four chemotypes respectively. Usnic acid, the most common
Acknowledgement
secondary metabolite exhibits its presence in all the species of
Authors are thankful to the Director, CSIR-National Botanical
genus Usnea. The ecological function attributed to usnic acid
Research Institute, Lucknow for providing necessary
is screening of excess light [19] as a result, species of Usnea
laboratory facilities (OLP-083). One of the author (PS),
growing on high altitudes could be potential source of high
thankful to the Department of Botany, Kumaun University,
concentration of usnic acid. Apart from usnic acid, barbatic
Nainital.
acid; norstictic acid; salazinic acid and stictic acids were the
other commonly occurring lichen secondary metabolites in
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162.

Figure 1. Graph showing number of lichen secondary metabolites present in various Indian species of Usnea.

90
80
70
60
50
Number of lichen

40
30
20
10
0

Secondary metabolites

Fig. 2. Graph showing the number of lichen secondary metabolites showing different biological activities.

20
substances with activities

18
16
14
Number of lichen

12
10
8
6
4
2
0
Antitumor Antimicrobial* Antioxidant Others

Biological activities of Lichen substances

* Antimicrobial properties including antiviral properties

32
Table 1. The secondary metabolites present in Indian Usnea species. Ale= Alectorialic acid, Bar= Barbatic acid, Bat= Barbatolic acid, Cap= Caperatic acid, Con= Constictic acid, Cry=
Cryptostictic acid, Dif= Differactaic acid, Evr= Evernic acid, Fum= Fumaroprotocetraric acid, Gal= Galbinic acid, Hyp= Hypoconstictic acid, Men= Menegazziaic acid, Nor=
Norstictic acid, Pro= Protocetraric acid, Prl= Protolichesterinic acid, Pso= Psoromic acid, Sal= Salazinic acid, Sqa= Squamatic acid, Stc= Stictic acid, Thm= Thamnolic acid, Usn=
Usnic acid, Und= undetermined spots.

Thm
Fum

Men
Hyp

Und
Cap

Con

Nor
Cry

Usn
Bar

Evr

Sqa
Gal
Bat

pro

Pso
Ale

Prl

Sal
Dif

Stc
S. No. Species

1. U. aciculifera Vain. + + +
2. U. albopunctata Nyl. + + +
3. U. angulata Ach. + +
4. U. austro-indica G. Awasthi (i) Strain I + +
(ii) Strain II + +
5. U.baileyi (Stirt.) Zahlbr (i) Strain I ± + + + +
(ii) Strain II + + +
6. U. bismolliuscula Zahlbr + +
7. U. bornmuelleri J. Steiner + +
8. U. certaina Ach. + +
9. U. complanata (Muell. Arg.) Motyka (i) Strain I + + + +
(ii) Strain II + +
10. U. compressa Taylor in Hook. f. + +
11. U. corallina Mot. + + + +
12. U. dasaea Stirt. (i) Strain I + + +
(ii) Strain II + +
(iii) Strain III + + ± + + +
(iv) Strain IV + +
(v) Strain V ± +
13. U. dendritica Stirt. + + + +
14. U. eumitrioides Motyka + +
15. U. firmula (Stirt.) Mot. + + +
16. U. fischeri G.Awasthi + +
17. U. fragilis Stirt. + +
33
18. U. fulvoreagens (Räsänen) Räsänen + + + +
19. U. ghattensis G. Awasthi + +
20. U. himalayana C. Bab. (i) Strain I + +
(ii) Strain II + +
(iii) Strain III + +
21. U. himantodes Stirt. + +
22. U. hirta Mot. + +
23. U. indica Motyka + +
24. U. inermis Mot. ± + +
25. U. longissima Ach. (i) Strain I +
(i) Strain II + + +
(i) Strain III + + + +
(i) Strain IV + +
(i) Strain V + + +
(i) Strain VI + + +
(i) Strain VII + + +
26. U. lucea Motyka + +
27. U. luridorufa Stirt. + + + +
28. U. maculata Stirt. (i) Strain I + +
(ii) Strain II +
29. U. mekista (Stirt.) G. Awasthi + +
30. U. nepalensis D.D. Awasthi in G. Awasthi +
31. U. nilgirica G. Awasthi + + +
32. U. nipparensis Ashahina + ± +
33. U. norketti G.Awasthi + + +
34. U. orientalis Mot. + +
35. U. pangiana Stirt. + + + +
36. U. pectinata Taylor + +
37. U. perplexans Stirt. + +
38. U. picta (i) Strain I ± ± + +
(ii) Strain II + +

34
39. U. pictoides G. Awasthi + +
40. U. pseudojaponica G. Awasthi + +
41. U. pseudosinensis Asahina + + +
42. U. rigidula (Stirt.) G. Awasthi (i) Strain I + +
(ii) Strain II + + +
(iii) Strain III + +
43. U. robusta Stirt. ± + +
44. U. rubicunda Stirt. (i) Strain I + + +
(ii) Strain II + +
45. U. sinensis Mot. +
46. U. sordida Mot. + +
47. U. spinosula Stirt. + +
48. U. splendens Stirt. + +
49. U. stigmata Mot. + + + + + + +
50. U. stigmatoides G. Awasthi + +
51. U. subflorida (Zahlbr.) Mot. ± + +
52. U. subfloridana Stirt. (i) Strain I + +
(ii) Strain II ± + +
(iii) Strain III + +
(iv) Strain IV + +
53. U. thomsonii + + +
54. U. trichodeoides Vain., (i) Strain I + +
(i) Strain II ± + +
55. U. vulneraria Mot. ± + + +
56. Usnea sp. 1 ± + +
57. Usnea sp. 2 + +

Total 2 12 2 2 3 1 5 1 5 3 1 2 17 5 1 4 23 3 21 1 81 14

35
 Secondary metabolites in
S. No. Structural information Activity References
Usnea
O COOH
H3 C
C O CH2 OH

1. Alectorialic acid Antiviral activity Omarsdottir et al. [20]

OH CH 3
OH
CHO OH

CH 3 CH3
COO OH
Antimicrobial activity, Martins et. al. [21];
2. Barbatic acid
antiproliferative activity Kumar & Muller [22]
HO COOH
CH3 CH3

O COOH
H3 C
C O CH2 OH

3. Barbatolic acid Antimicrobial activity Cobanoglu et al. [23]

OH CHO
OH
CHO OH

O O
O

4. Caperatic acid OH Antioxidant activity Ravaglia et al. [24]

OH

O OH

CH3 CH3
COO OH

5. Constictic acid Anticancerous activity Shrestha et al. [25]

HO O O O
COOH O
HO
H
36
 CH3 CH3
COO OH

6. Cryptostictic acid Antimicrobial activity Cobanoglu et al. [23]

CH3O O O
COOH O
HO
H

CH 3 CH3 Antifungal agent, antiviral,

COO OH
antitumor, analgesic and antipyretic;
7. Differactaic acid Kumar & Muller [22, 26]
CH3O OCH3 COOH
inhibition of leukotriene B4
CH3 CH3 biosynthesis (LTB) in leukocytes

HO OH

O Fungicidal, Total/Strong growth Halama & van Haluwin

HO O
8. Evernic acid inhibitor of plant pathogens; [27], Manojlovic et al.
CH3
O
antimicrobial activity [28]
CH3

O CH3

CH3 OOCCH = CHCOOH

OH
COO
9. Fumaroprotocetraric acid Antimicrobial activity Rankovic et al. [29]
O
COOH
OH
CHO CH3

CH3 CH2OAc
COO OH

10. Galbinic acid Antibacterial activity Sultana & Afolayan [11]

HO O O
CHO O
HO
H

37
 CH3 CH2OH
COO OH
Sultana & Afolayan [11],
11. Hypoconstictic acid Antibacterial and antitumor activity
O Kwabena et al. [30]
H3CO O
CH3 O
HO
H

CH3 CH3
COO OH

12. Menegazzaic acid Antibacterial activity Sultana & Afolayan [11]

H3CO O O
OH O
HO
H

CH3 CH3
COO OH

13. Norstictic acid Antibacterial activity Sultana & Afolayan [11]

HO O O
CHO O
HO
H

CH 3 CH 2OH
COO OH

14. Protocetraric acid Antimicrobial activity Rankovic and Misic [29]

HO O COOH

CHO CH 3

HOOC CH2 Sasidharan, N.K. et al.

Antibacterial and antifungal
15. Protolichesterinic acid [31], Hirayama et al. [32],
activities, antiproliferative activity
CH3(CH2)12 O O Manojlovic et al. [28]

38
 CH 3 CH3
COO OCH3
Antioxidant and cardiovascular
16. Psoromic acid Behera et al. [33]
protective activities
HO O
CHO COOH

CH3 CH2OH

OH
COO
Antibacterial activity, antioxidant Sultana & Afolayan [11],
17. Salazinic acid O O
C acitvity Amo De Paz et. al. [34]
OH
CHO CH O

OH
O CH 3
CH 3
C O OH

18. Squamatic acid Antimicrobial activity Manojlovic et al. [28]

OH COOH
H 3CO
COOH CH 3

CH3 CH3
COO OH Rankovic and Misic [29],
Antimicrobial, anticancer activity
19. Stictic acid Amo De Paz et. al. [34],
O and antioxidant acitvity
CH3O O B. Pejin et al. [35]
CHO O
HO
H

O CH 3
CH 3
C O COOH
20. Thamnolic acid Antimicrobial activity Manojlovic et al. [28]
OH OH OH
H 3CO
COOH CHO

39
 OH O
H3C Antitumor, antimutagenic,
H3C COCH 3 Sultana & Afolayan [11],
antioxidant, analgesic, antipyretic,
Manojlovic et al. [28],
21. Usnic acid enzyme inhibitory, hepato-
Mayer et al. [36], Behera
OH OH protective and antimicrobial
O et al. [33]
COCH 3 activities

Table 2. Details of secondary metabolites present in Indian Usnea species, their chemical structure, biological activities and references.

40

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