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Review

Modern Use of Bryophytes as a Source of Secondary Metabolites

by
Michał Dziwak
1,
Katarzyna Wróblewska
1,*,
Antoni Szumny
2 and
Renata Galek
3
1
Department of Horticulture, Wroclaw University of Environmental and Life Sciences, Grunwaldzki 24a, 50-363 Wrocław, Poland
2
Department of Food Chemistry and Biocatalysis, Wroclaw University of Environmental and Life Sciences, Norwida 25, 50-375 Wrocław, Poland
3
Department of Plant Genetics, Breeding and Seed Production, Wroclaw University of Environmental and Life Sciences, Grunwaldzki 24a, 50-363 Wrocław, Poland
*
Author to whom correspondence should be addressed.
Agronomy 2022, 12(6), 1456; https://doi.org/10.3390/agronomy12061456
Submission received: 25 April 2022 / Revised: 3 June 2022 / Accepted: 13 June 2022 / Published: 17 June 2022
(This article belongs to the Special Issue Chemical Diversity, Yield and Quality of Aromatic Plant)
Browse Figures
Versions Notes

Abstract

:
Bryophytes constitute a heterogeneous group of plants which includes three clades: approximately 14,000 species of mosses (Bryophyta), 6000 species of liverworts (Marchantiophyta), and 300 species of hornworts (Anthocerotophyta). They are common in almost all ecosystems, where they play important roles. Bryophytes lack developed physical barriers, yet they are rarely attacked by herbivores or pathogens. Instead, they have acquired the ability to produce a wide range of secondary metabolites with diverse functions, such as phytotoxic, antibacterial, antifungal, insect antifeedant, and molluscicidal activities. Secondary metabolites in bryophytes can also be involved in stress tolerance, i.e., in UV-absorptive and drought- and freezing-tolerant activities. Due to these properties, for centuries bryophytes have been used to combat health problems in many cultures on different continents. Currently, scientists are discovering new, unique compounds in bryophytes with potential for practical use, which, in the age of drug resistance, may be of considerable importance. The aim of this review is to present bryophytes as a potential source of compounds with miscellaneous possible uses, with a focus on volatile compounds and antibacterial, antifungal, and cytotoxic potential, and as sources of materials for further promising research. The paper also briefly refers to the methods of compound extraction and acquisition. Formulas of compounds were drawn by the authors using ChemDraw software (PerkinElmer, Boston, MA, USA) with reference to data published in various papers, the ACD/Labs dictionary database, PubChem, and Scopus. The data were gathered in February 2022.

1. Introduction

Bryophytes constitute a heterogeneous group of plants which includes three clades: mosses (Bryophyta), liverworts (Marchantiophyta), and hornworts (Anthocerotophyta) [1,2]. Their characteristic feature is the alternation of generations with the dominance of the haploid gametophyte. There are about 14,000 species of mosses, 6000 species of liverworts, and 300 species of hornworts in the world [3]. Representatives of this group are common in all ecosystems (except salt water ecosystems), where they play important roles [4]. Bryophytes can be found in tropical forests [5,6], Antarctica [7,8], and deserts [9,10,11], as well as other sites difficult for plants to access. Due to their tolerance of lack of light, they can develop in places with limited access to light, e.g., caves [12,13,14]. Bryophytes lack developed physical barriers, but they are rarely attacked by herbivores and pathogens [15]. This is due to their ability to produce a wide range of secondary metabolites which allow them to survive unfavorable abiotic conditions, protecting them against potential biotic stresses (Table 1).
For centuries, bryophytes have been used to combat health problems in many cultures on different continents. According to Indian and Chinese medicine, the spectrum of their applications is very wide, from being used to fight fevers through to treating skin infections and relieving pain [16,17]. Native Americans used a mixture of moss ash and honey as a disinfectant for wounds [17]. During World War I, dried sphagnum moss was used in Canada as a replacement for bandages. Its effectiveness is related to its high absorbency and bactericidal properties [18]. After thorough examinations, some of the species that were formerly considered to be therapeutic were found to be ineffective or even, in some cases, toxic, yet the aseptic and anti-cancer properties of numerous species have been confirmed. They have therefore been the object of increasing scientific interest. A significant number of bryophyte secondary metabolites have potential pharmacological, economic, or biotechnological uses. The biologically active compounds that can be obtained from bryophytes include antioxidants, compounds toxic to specific groups of organisms (potential plant-protection agents), inhibitors of certain enzymes, anti-cancer and anti-HIV-1 compounds, neurotrophic compounds, and compounds that relax muscles and strengthen the heart. They are also associated with numerous aromas (of carrots, cedar trees, mushrooms), pungency, and bitterness [19]. The aim of this review is to present bryophytes as a potential source of compounds with miscellaneous possible uses and as sources of materials for further promising research. The paper also briefly refers to the methods of compound extraction and acquisition.
Table
Table 1. The main classes of secondary metabolites among bryophytes and their potential activities.
Table 1. The main classes of secondary metabolites among bryophytes and their potential activities.
Class Potential Activity
Antibacterial and FungicidalCytotoxicInsecticidal and MolluscicidalPhytotoxicCold-TolerantDrought-TolerantAnti-UVReferences
Benzenoids+ + +[3,20,21,22]
Bibenzyls and bis(bibenzyls)++++ + [3,19,20,21,22,23,24]
Fatty acid
derivatives		+ + [3,20,21,22,23,24,25]
Flavonoids+ + +[3,20,21,22,25]
Phenylpropanoids + + +[3,20,22,23,24,25]
Terpenes and
terpenoids		++++ [3,19,20,21,22,23,24,25,26,27]

2. Ethnopharmacology

In ancient times, medical utility was indicated by the appearance of a plant, i.e., the shape and structure of its organs. It was a view presented by Paracelsus as the ‘doctrine of signatures’. Following this belief, the species Polytrichum commune Hedw. has been used to improve the condition of the hair. Tribal cultures of South India used hair-like thallus of Frullania ericoides (Nees) Mont. in a similar way. The Irular tribe of the Attappady valleys used the thalloid gametophytes of Targionia hypophylla L. to treat skin conditions due to its characteristic rough surface [17]. The thallus of Plagiochasma appendiculatum Lehm. & Lindenb. was used for skin diseases by Gaddi tribes of Himachal Pradesh, India [14]. American tribes used some mosses as remedies for burns: the Gasuite Indians used species from the genera Philonotis (Hedw.) Brid., Bryum Hedw., Mnium Hedw. and also from the Hypnaceae family, while Polytrichum juniperinum Hedw. was used by indigenous Alaskan and Cheyenne populations [23]. Alaskan Natives also made ointment from Sphagnum leaves mixed with tallow and grease to treat cuts [28].
Pre-Columbian Mesoamerican cultures found uses for 36 species of bryophytes, for ceremonial, craft and medical purposes [29]. Some of them were mentioned in Libellus de Medicinalibus Indorum Herbis (1552)—the oldest report of the medical use of bryophytes in Mesoamerica [30]. Marchantia sp. L. was used in combination with Begonia sp. L. and Lithanchne pauciflora (Sw.) P.Beauv. to treat mouth sores and fever [31]. Headaches were treated by washes made of Braunia secunda (Hook.) Bruch & Schimp boiled in water [29]. Tea prepared from Pleurochaete squarrosa (Brid.) Lindb. was used to relieve stomach ache and as a compress favoring the healing of wounds [29]. The moss Sematophyllum adnatum (Michx.) E. Britton was used to prepare medicinal tea [18]. Dendropogonella rufescens (Schimp.) E. Britton was used by the Zapotec community to treat the discomfort of women after childbirth. Smoking this moss with stalk of Agave americana L. and corn ear styles gave relief for muscle and bone pain [32]. Currently, D. rufescens is prepared as a drink to increase the appetite, for kidney and lung health, and as a treatment for blindness and diabetes-related ailments [32].
The bryophytes also have many other medical uses. The liverwort Conocephalum conicum (L.) Dum. was used in the form of a decoction as an antibacterial, antifungal, and antipyretic agent. It was applied to treat wounds, swelling, burns, and snake bites. Marchantia polymorpha L. was used as a medicine for inflammation, liver problems, bites and cuts, and as a diuretic [16,33], while Frullania tamarisci (L.) Dumort. was utilized as an antiseptic remedy [16]. Riccia L. species was used to cure ringworm, the fungal skin infection [28]. Reboulia hemisphaerica L. Raddi was used for hemostasis and to treat blotches, external wounds, and bruises. Funaria hygrometrica Hedw. served as a hemostatic to cure pulmonary tuberculosis, hematemesis, bruises, and athlete’s foot dermatophytosis [33]. The moss Bryum argenteum Hedw. was valued as an antipyretic and antifungal medicine. Due to their antimicrobial properties, members of the Sphagnaceae family were used to cover wounds, skin ailments, and to treat eye diseases [16]. During the Russo–Japanese War, Sphagnum L. mosses were used by the Japanese as a first-aid dressing on a large scale [28]. Furthermore, during World War I, dried Sphagnum sp. was used in Britain, Canada, and Germany as a cheap substitute for cotton bandages [18,34]. The aquatic moss Fontinalis antipyretica Hedw. boiled with beer was used as a footbath to treat chest fever, fever, microbial infections, and for detoxication [33].

3. Secondary Metabolites

The species of bryophytes express diverse functions, such as phytotoxic, antibacterial, antifungal, insect antifeedant, and molluscicidal activities [19]. They can be involved in stress tolerance, i.e., in UV-absorptive and drought- and freezing-tolerant activities (Table 1) [3,19,20,21,22,23,24,25,26]. Both extracts and isolated compounds of bryophytes are very popular in studies as sources for new applications. Treatment with extracts allows examination of the activities of all compounds contained in the plant material, including their interactions [35]. An important element in the preparation of extracts is the selection of appropriate solvents, as this determines the extracted compounds. With proper extraction methods, extracts often prove to be as effective as commercially synthesized substances.
Among the known species of bryophytes, biologically active compounds from different classes can be mentioned, such as benzenoids, bibenzyls, bis(bibenzyl)s, flavonoids, terpenoids, phenylpropanoids, and derivatives of fatty acids. The spectrum of application of compounds contained in this group of plants is considerable, as every group has at least a few activities (Table 1). Unfortunately, their use is hampered by the fact that some substances have not yet been identified and tested.

3.1. Volatile Compounds

Due to the presence of oil bodies, liverworts are characterized by the widest range of aromas among bryophytes [36]. The sources of odors are volatile mono- and sesquiterpenes and terpenoids, as well as low-molecular weight derivatives of fatty acids or phenylpropanoids [19]. Miscellaneous pleasant fragrances with potential for use in perfumery, pharmacy, and the food industry can be found in liverworts, but there are also odors that cause unpleasant sensations. Some of the aromas are specific only to a single species of liverwort. Valarenzo et al. [37] screened volatile metabolites in four liverwort species. Depending on the species studied, it was not possible to identify 10 to 15% of the essential oil compounds, and they require further research. The unknown compounds may include metabolites unique to bryophytes, to specific families, or to single species. Essential oils have also been found in mosses [38]. There have been several reports that some of them show antimicrobial activity against bacteria and fungi [39,40,41].
Unique aromas can also be found among other bryophytes, e.g., Takakia lepidozioides S. Hatt. & Inoue is characterized by an aromatic blend of cinnamon and roasted wheat due to the presence of coumarin [42] (Table 2). The smells of bryophytes depend not only on contents of volatile secondary metabolites in their essential oils (Table 2), but also on plant habitat conditions, e.g., Frullania species produce tamariscol (1, Figure 1) only when grown in high mountain sites [19]. According to Sakurai et al. [43], the aroma of the liverwort Cyathodium foetidissimum Schiffn. collected in Tahiti in 2016 was pleasant, described as ‘nostalgic’ or a ‘chest of drawers’, in contrast to the same species found on Ua Huka in Marquesas Islands in 2009 [44], which exuded the smell of urine and feces. These islands are located in French Polynesia, about 1400 km away.

3.2. Antimicrobial Compounds and Extracts

Secondary metabolites found in bryophytes, such as flavonoids, terpenes, fatty acid derivatives, bibenzyls, and bis(bibenzyl)s, constitute a chemical ‘barrier’ against potential pathogens, justifying the use of bryophyte extracts in the folk medicine of many cultures, in particular, the use of bryophytes in the treatment of infections and wound cleansing. Research on bryophytes has confirmed their antimicrobial properties. Table 3 presents examples of extracts obtained from bryophytes and the antibacterial and antifungal activities of their extracts against selected pathogens. Gram-negative bacteria show greater sensitivity to extracts obtained from bryophytes. This makes them potential complements for antibiotics, as conventional antibiotics tend to be more active against Gram-positive bacteria [18,61]. This phenomenon is rare in higher plants [62]. The metabolites showing antibacterial activity isolated from the extracts are unique to bryophytes. Among them, lunularin (21), marchantin A (29), polygodial (30), riccardiphenol C (32), and sacculatal were isolated (Table 4, Figure 2). They show activity against, i.e., Acinetobacter calcoaceticus, Bacillus cereus, B. subtilis, Cryptococcus neoformans, Pseudomonas aeruginosa, Salmonella typhimurium, Staphylococcus aureus, and Streptococcus mutans.
Apart from their antibacterial potential, bryophyte extracts show antifungal properties. The results of the research show that the extracts of certain species of mosses and liverworts do not exhibit these properties, despite their antibacterial effects [73,79,80]. Such selectivity may have industrial or medical applications [47,91,92,93]. On the other hand, the isolated antifungal substances show activity against numerous pathogenic fungi (Table 5, Figure 3) [75,88,89,90,94,95,96,97].

3.3. Cytotoxic Compounds

The bryophyte extracts, apart from their antimicrobial activities, showed cytotoxic activities in vitro [3,87]. The same was corroborated for some particular compounds. Some of them showed cytotoxic activities against drug-resistant neoplasms, e.g., prostate cancer PC3. These compounds were tested on several human and mouse tumor lines: breast cancer MCF-7, cellosaurus P388, chemoresistant prostate cancer PC3, glioblastoma multiforme U-251, leukemia HL-60, liver cancer HepG2, melanoma RPMI-7951, and monocytic leukemia U937 (Table 6, Figure 4).

3.4. Other Compounds

In several species of the Radula Dumort. genus, cannabinoid compounds have been discovered. The benzyl cis-THC, (-)-perrottetinene (cis-PET) (Figure 5) was isolated from Radula perrottetii Gottsche ex Stephani [107,108], Radula marginata (Hook.f. & Taylor) Gottsche, Lindenb. & Nees [108,109], and Radula laxiramea Steph. [108,110]. Tests on mouse brains showed that this compound is bioavailable and selectively binds to CB1 and CB2 receptors at nanomolar concentrations in vitro. Cis-PET induced similar effects to Δ9–trans-THC, including antinociception, hypothermia, catalepsy, and hypolocomotion [111].

4. Bryophytes in Tissue Cultures

A large number of compounds isolated in extracts have the potential to be used in medicine and in industry. However, the isolation of secondary metabolites requires large amounts of plant material. Harvesting from nature can negatively affect the environment and contribute to the loss of biodiversity, one of the biggest concerns of the modern world. In vitro cultures may be a solution to this problem.
The history of in vitro cultures of bryophytes is over 100 years old. The first reports of successful culture induction date back to 1906 [112] and 1913 [113], while the article describing the first seed plant culture appeared in 1925 [114]. The advantages of tissue cultures in the cultivation of mosses are the ease of obtaining aseptic spores and, in the case of liverworts, the vegetative regenerative potential. The next milestone was the identification of environmental conditions stimulating the development of explants. Significant factors were: photoperiod, light intensity, medium composition, and air temperature [115]. The conditions favoring the production of secondary metabolites are equally important. Becker [116] described that the qualitative and quantitative compositions of bryophytes grown in tissue cultures under certain conditions corresponded to those of bryophytes obtained from the natural environment, justifying the mass production of secondary metabolites from this group of plants, e.g., in photobioreactors.
The methodology of growing bryophytes in in vitro conditions and isolating secondary metabolites from them was developed by Sabovljevic et al. [117]. This publication describes the recommended media parameters and culture conditions appropriate for a given stage of culture. The paper touches upon aspects of sterilization of gametophytes and sporophytes, spore germination, establishing primary and secondary protonema, multiplication, bud induction, liquid cultures, preparation of bryophyte extracts, and HPLC analysis.
Another set of means of obtaining metabolites are biotechnological methods. In this context, Bryophyta cultures kept in bioreactors are used and secrete metabolites into culture media. Studies have shown that bryophytes produce secondary metabolites in vitro in similar quantities and of similar quality to bryophytes obtained from the natural environment. The concentration of produced metabolites changes during seasons [118]. Therefore, optimization of the micro-reproduction process and the determination of physical and chemical conditions will allow for the stable and effective production of secondary metabolites. Moreover, plant material from in vitro cultures is devoid of endophytic microorganisms that may distort the results of research conducted on bryophyte extracts [119,120,121].

5. Conclusions

Bryophytes are important for biodiversity and other ecosystem services. They can retain huge amounts of water and therefore act as moisture buffers in many ecosystems [94] and may be used in the management of stormwater [122]. They also provide habitats for many microorganisms and invertebrates [123,124]. Cyanobacteria symbiotic with bryophytes assimilate atmospheric nitrogen [125,126,127], which is especially important during the process of primary succession [128,129]. Due to their potential for capture of large amounts of particulate matter from air, both organic [130,131] and inorganic [132], they can be used for monitoring air pollution [133,134].
Bryophytes are also a valuable source of biologically active compounds useful in medicine, pharmacy, and in industry. Their full potential has not been recognized yet. New metabolites characteristic of this group of plants are still under research. Among them, many antibacterial (Table 5), antifungal (Table 6), and cytotoxic compounds can be mentioned. They can offer solutions to increasing pathogen resistance and be used against cancer target lines. Metabolites such as marchantin A, plagochilin E, and riccardin C exhibit cytotoxic activities against chemoresistant prostate cancer [3,100]. In addition to the aforementioned active compounds, those with antioxidant [135,136,137], anti-inflammatory [138,139,140], psychoactive [111], antiviral [141], muscle-relaxing [142], neuroprotective [142,143], anti-HIV [144], and insecticidal activities can be distinguished [145,146]. Compounds with nematicidal activity have potential in agricultural industry as natural plant-protection products. Some volatile compounds can be used as repellents, e.g., polygodial (30) shows stronger repellent activity against mosquitoes than commercial products [24]. Specific aromatic compounds (Table 2) obtained from bryophytes can be used in perfumery and pharmacy. Additionally, the optimization of production conditions will allow the maximization of the production of secondary metabolites by bryophytes. The methodology for the extraction and isolation of metabolites from bryophytes was described by Asakawa and Ludwiczuk [147]. For a less detailed extraction instruction, but including directions for HPLC analysis, see Sabovljevic et al. [117].
Obtaining plant material from nature is problematic due to the degradation of ecosystems. However, it is now possible to reproduce bryophytes massively with less environmental impact. For this purpose, in vitro cultures can be used, which enable the mass production of biomass with the use of various types of photobioreactors [91]. There are several articles describing the practicalities and problems of in vitro bryophyte cultivation [148,149,150]. The optimization of production conditions will maximize production of secondary metabolites by bryophytes.
To conclude, in the last 40 years, knowledge of bryophytes has significantly deepened. Currently, scientists are discovering new, unique compounds with potential for practical use, which in the age of drug resistance may be of considerable importance. Further research will allow the determination of the real therapeutic value of these metabolites.

Author Contributions

Conceptualization, K.W., M.D. and A.S.; writing—original draft preparation, M.D.; writing—review and editing, K.W.; supervision, A.S. and R.G. All authors have read and agreed to the published version of the manuscript.

Funding

The APC/BPC is financed by Wroclaw University of Environmental and Life Sciences.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Agronomy 12 01456 g001 550
Figure 1. Chemical structures of compounds mentioned in Table 2 (1: tamariscol; 2: scatole; 3: methyl cinnamate; 4: bicyclogermacrene; 5: isolepidozene; 6: lunularin; 7: p-ethylphenol; 8: geosmin; 9: grimaldone; 10: bicyclohumulenone; 11: R-pulegone; 12: coumarin).
Figure 1. Chemical structures of compounds mentioned in Table 2 (1: tamariscol; 2: scatole; 3: methyl cinnamate; 4: bicyclogermacrene; 5: isolepidozene; 6: lunularin; 7: p-ethylphenol; 8: geosmin; 9: grimaldone; 10: bicyclohumulenone; 11: R-pulegone; 12: coumarin).
Agronomy 12 01456 g001
Agronomy 12 01456 g002 550
Figure 2. Chemical structures of compounds mentioned in Table 4 (13: marchantin A; 14: polygodial; 15: sacculatal; 16: riccardiphenol C).
Figure 2. Chemical structures of compounds mentioned in Table 4 (13: marchantin A; 14: polygodial; 15: sacculatal; 16: riccardiphenol C).
Agronomy 12 01456 g002
Agronomy 12 01456 g003 550
Figure 3. Chemical structures of compounds mentioned in Table 5 (17: asterelin A, R=H; 18: asterelin B, R=Me; 19: bazzanin B, R=Cl; 20: bazzanin S, R=H; 21: isoplagiochin D; 22: isoriccardin C; 23: gymnomitrol; 24: marchantin H; 25: neomarchantin A, R=H; 26: neomarchantin B, R=OH; 27: riccardin C).
Figure 3. Chemical structures of compounds mentioned in Table 5 (17: asterelin A, R=H; 18: asterelin B, R=Me; 19: bazzanin B, R=Cl; 20: bazzanin S, R=H; 21: isoplagiochin D; 22: isoriccardin C; 23: gymnomitrol; 24: marchantin H; 25: neomarchantin A, R=H; 26: neomarchantin B, R=OH; 27: riccardin C).
Agronomy 12 01456 g003
Agronomy 12 01456 g004 550
Figure 4. Compounds mentioned in Table 6 (28: jungermannenone A, R=OH; 29: jungermannenone B, R=H; 30: marsupellone; 31: pallidisetin A; 32: pallidisetin B; 33: plagiochin E; 34: trewiasine).
Figure 4. Compounds mentioned in Table 6 (28: jungermannenone A, R=OH; 29: jungermannenone B, R=H; 30: marsupellone; 31: pallidisetin A; 32: pallidisetin B; 33: plagiochin E; 34: trewiasine).
Agronomy 12 01456 g004
Agronomy 12 01456 g005 550
Figure 5. Chemical structures of perrottetinene (35) and tetrahydrocannabinol (THC, 36).
Figure 5. Chemical structures of perrottetinene (35) and tetrahydrocannabinol (THC, 36).
Agronomy 12 01456 g005
Table
Table 2. Selected species of bryophytes, their aromas and main volatile compounds.
Table 2. Selected species of bryophytes, their aromas and main volatile compounds.
SpeciesFamilyMajor Volatile Components 1OdorRef.
Asterella species
P.Beauv.		AytoniaceaeSkatole (2)Feces-like, unpleasant[45]
Conocephalum conicum
(L.) Dum.		Conocephalaceae(–)-sabinene, (+)-bornyl acetate,
methyl cinnamate (3)		Camphoraceous,
distinctly mushroomy		[46,47]
Cyathodium foetidissimum
Schiffn.		CyathodiaceaeSkatole (2), bicyclogermacrene
and isolepidozene (5), lunularin (6)		Feces, urine, unpleasant[43,48,49]
Frullania tamarisci
(L.) Dumort.,
F. nepalensis
(Spreng.) Lehm. & Lindenb.,
F. asagrayana
Montagne		FrullaniaceaeTamariscol (1)Oak moss-like[50,51]
Jungermannia obovata
Nees		Jungermanniaceae4-hydroxy-4-methylcyclohex-2-en-1-oneCarrot-like[19,52]
Leptolejeunea elliptica
Lehm. & Lindenb.		Lejeuneaceaep-ethylphenol (7),
p-ethyl phenyl acetate		Naphtalene and dried fish[53,54]
Lophocolea heterophylla
(Schrad.) Dumort.,
Lophocolea bidentata
(L.) Dumort.		Lophocoleaceae(–)-2-methylisoborneol, geosmin (8)Strong and distinctly mossy[19,55]
Mannia fragrans
(Balbis) Frye et L.Clark		AytoniaceaeGrimaldone (9)Strong sweet-mossy[56,57]
Plagiochila sciophila
Nees		PlagiochilaceaeBicyclohumulenone (10)Sweet-mossy and woody[19]
Plagiochila rutilans
Lindenb.		PlagiochilaceaeR-pulegone (11) and several other menthane monoterpenoidsPeppermint-like[58,59]
Symphyogyna brongniartii
Mont.		PallaviciniaceaeGeosmin (8)Distinctly earthy/musty[60]
Takakia lepidozioides
S. Hatt. & Inoue		TakakiaceaeCoumarin (12)Cinnamon and burnt
wheat		[44]
1 Bold numbers refer to the chemical structures of compounds are presented in Figure 1.
Table
Table 3. Antimicrobial activities of some bryophyte extracts.
Table 3. Antimicrobial activities of some bryophyte extracts.
DivisionSpeciesExtractsTested BacteriaTested FungiRef.
BryophytaAtrichum
undulatum
(Hedw.) P.Beauv.		Water,
ethanol		Bacillus mycoides,
Escherichia coli,
Proteus mirabilis,
Staphylococcus aureus,
Salmonella typhii		Aspergillus fumigatus,
Fusarium oxysporum		[63,64]
Dimethyl sulfoxydeBacillus cereus,
Escherichia coli,
Micrococcus flavus,
Staphylococcus aureus		Aspergillus fumigatus,
Penicillium funiculosum,
P. ochrocholoron,
Trichoderma viride		[65,66]
Bryum
argenteum
Hedw.		EthanolEscherichia coli,
Bacillus subtilis,
Micrococcus luteus,
Staphilococcus aureus		Aspergillus niger,
Penicillium ochrochloron,
Candida albicans,
Trichophyton mentagrophyes		[67]
Dicranum scoparium
Hedw.		EthanolEnterococcus faecalis,
Escherichia coli,
Klebsiella pneumonia,
Staphylococcus aureus,
Streptococcus pyogenes		N.T.[68]
Fontinalis antipyretica
Hedw.		MethanolEscherichia coli,
Salmonella enteritidis,
Shigella epidermidis,
Bacillus subtilis,
Micrococcus flavus		Aspergillus flavus,
A. fumigatus,
A. niger,
Penicillium funiculosum,
P. ochrochloron,
Trichoderma viride		[69]
Hypnum cupressiforme
Hedw.		MethanolBacillus subtilis,
Escherichia coli,
Micrococcus flavus,
Shigella enteritidis,
S. epidermidis		Aspergillus flavus,
A. fumigatus,
A. niger,
Penicillium funiculosum,
P. ochrochloron,
Trichoderma viride		[69]
Water *N.S.Candida albicans,
Saccharomyces cerevisiae		[70]
Plagiomnium cuspidatum
(Hedw.) T.J.Kop.		n-hexaneBacillus subtilis,
Moraxella catarrhalis,
Staphylococcus aureus,
Shigella epidermidis,
Streptococcus pyogenes,
S. pneumonianiae		N.T.[71]
Polytrichum commune
Hedw.		Water *Escherichia coli,
Enterococcus faecalis,
Streptococcus mutans,
Pseudomonas aeruginosa,
Staphylococcus aureus		N.T.[72]
Chloroform, ethanolBacillus cereus,
Escherichia coli,
Enterococcus faecalis,
Streptococcus mutans,
Pseudomonas aeruginosa,
Staphylococcus aureus		N.S.[73]
Polytrichum juniperinum
Hedw.		MethanolBacillus subtilis,
Pseudomonas aeruginosa,
Staphylococcus aureus		N.T.[74]
EthanolEnterococcus faecalis,
Escherichia coli,
Klebsiella pneumonia,
Staphylococcus aureus		N.T.[68]
Syntrichia
ruralis
(Hedw.) F. Weber & D. Mohr		EthanolEnterococcus faecalis,
Escherichia coli,
Klebsiella pneumonia,
Staphylococcus aureus		N.T.[68]
MarchantiophytaBazzania trilobata L.Dichloromethane, methanolN.T.Botrytis cinerea,
Candida albicans,
Cladosporium cucumerinum,
Phythophthora infestans,
Pyricularia oryzae,
Septoria tritici		[75]
EthanolBacillus subtilis,
Listeria monocytogenes,
Staphylococcus aureus		N.S.[76]
Frullania
dilatata
(L.) Dumort.		Water,
ethanol		Staphylococcus aureusN.T.[77]
Lophozia ventricosa
(Dicks.) Dumort.		Methanol, ethyl acetateBacillus cereus,
Listeria monocytogenes,
Micrococcus flavus,
Staphylococcus aureus		Aspergillus niger,
A. fumigates,
A. ochraceus,
A. versicolor,
Penicillium funiculosum,
P. ochrochloron,
Trichoderma viride		[78]
Lunularia
cruciata
(L.) Lindb.		Acetone, chloroform, ethanol, methanol, waterAgrobacterium tumefaciens,
Staphylococcus aureus,
Shigella epidermidis,
Streptococcus faecalis,
Proteus mirabilis,
P. vulgaris,
Pseudomonas aeruginosa,
Escherichia coli,
Salmonella typhi,
Klebsiella pneumoniae,
Enterobacter cloacae,
E. aerogenes,
Citrobacter diversus,
Bacillus subtilis,
Xanthomonas phoseoli,
Erwinia chrysanthemi		N.S.[79,80]
Marchantia polymorpha L.Chloroform, methanol Escherichia coli,
Staphylococcus aureus,
Proteus mirabilis,
Pasturella multocida,
Xanthomonas oryzae		Candida albicans,
Fusarium oxysporum, Rhizoctonia solani,
Sclerotium rolfsii,
Trichophyton mentagrohtytes,
Tilletia indica		[81,82]
Dimethyl sulfoxydeBacillus cereus,
Escherichia coli,
Micrococcus flavus,
Staphylococcus aureus		Aspergillus fumigatus,
Penicillium funiculosum,
P. ochrocholoron,
Trichoderma viride		[65,66]
Porella
arboris-vitae
(With.) Grolle		Methanol, ethanol, ethyl acetateSalmonella enteritidis,
Escherichia coli,
Listeria monocytogenes		Aerobasidium pullulans,
Pichia membranaefaciens,
Pichia anomala,
Saccharomyces cerevisiae,
Zygosaccharomyces bailii		[83]
Reboulia
Hemisphaerica(L.) Raddi		MethanolBacillus cereus, B. subtilis,
Escherichia coli,
Enterococcus faecalis,
Pseudomonas aeruginosa,
Staphylococcus aureus		Aspergillus niger,
Penicillium notatum		[84]
Scapania aspera
M. Bernet & Bernet		Methanol, ethanol, ethyl acetateSalmonella enteritidis,
Escherichia coli,
Listeria monocytogenes		Aerobasidium pullulans,
Pichia membranaefaciens,
P. anomala,
Saccharomyces cerevisiae,
Zygosaccharomyces bailii		[61]
Targionia
hypophylla L.		MethanolBacillus substilis,
Escherichia coli,
Staphylococcus aureus		Aspergillus niger,
Botrytis cinerea,
Penicillium chrysogenum,
P. expansum,
Trichoderma viridae		[85,86]
* Distillation. N.T.—not tested; N.S.—not shown.
Table
Table 4. Antimicrobial activities of compounds isolated from bryophytes.
Table 4. Antimicrobial activities of compounds isolated from bryophytes.
CompoundsSpeciesFamilyActivity AgainstReferences
Lunularin (6)Dumortiera hirsuta (Sw.) NeesDumortieraceaePseudomonas aeruginosa (MIC 64 mg/mL)[87]
Marchantin A (13)Marchantia species L.MarchantiaceaeAcinetobacter cacoaceticus (MIC 12.5 μg/mL),
Bacillus cereus (12.5 μg/mL),
Bacillus megaterium (MIC 25 μg/mL),
Bacillus subtilis (MIC25 μg/mL),
Cryptococcus neoformans (MIC 12.5 μg/mL), Staphylococcus aureus (MIC 3.13–25),
Salmonella typhimurium (MIC 100 μg/mL)		[88,89]
Polygodial (14)Porella vernicosa Lindb.PorellaceaeStreptococcus mutans (LD50 100 μg/mL)[19]
Sacculatal (15)Pellia endiviifolia (Dicks.) Dumort.PelliaceaeStreptococcus mutans (LD50 8 μg/mL)[19]
Riccardiphenol C (16)Riccardia crassa Schwägr.AneuraceaeBacillus subtilis[90]
LD50—lethal dose: the amount of a compound that it takes to kill 50% of tested pathogen cells; MIC—minimum inhibitory concentration. Bold numbers refer to the chemical structures o Bold numbers refer to the chemical structures of compounds are presented in Figure 1 and Figure 2.
Table
Table 5. Antifungal activities of compounds isolated from bryophytes.
Table 5. Antifungal activities of compounds isolated from bryophytes.
CompoundsSpeciesFamilyActivity AgainstReferences
Asterelin A, (17, R=H)
Asterelin B (18, R=Me)		Asterella angusta (Stephani) Pandé, K.P. Srivast. & Sultan KhanAytoniaceaeCandida albicans[94]
Bazzanin B (19, R=Cl)
Bazzanin S (20, R=H)		Bazzania trilobata L.LepidoziaceaeBotrytis cinerea (IC50 18.9),
Cladosporium cucumerinum (IC50 17.5),
Pyricularia oryzae (IC50 3.9),
Zymoseptoria tritici (IC50 23.5)		[75]
Isoplagiochin D (21)Bazzania trilobata L.,
Lepidozia incurvata
Lindenb.		LepidoziaceaeZymoseptoria tritici (IC50 15.9)[95]
Isoriccardin C (22)Plagiochasma intermedium
Lindenb. & Gottsche		AytoniaceaeCandida albicans[95]
Gymnomitrol (23)Bazzania trilobata L.,
Gymnomitrion obtusum (Lindb.) Pears.		Lepidoziaceae,
Gymnomitriaceae		Phytophthora infestans,
Pyricularia oryzae,
Zymoseptoria tritici		[75,98]
Marchantin A (13)Marchantia species L.MarchantiaceaeAspergillus niger (MIC 25-100 μg/mL),
Pyricularia oryzae (MIC 12.5 μg/mL),
Rhizoctonia solani (MIC 50 μg/mL),
Saccharomyces cerevisiae (MIC 3.13 μg/mL),
Trichophyton mentagrophytes (MIC 3.13 μg/mL)		[88,89]
Marchantin H (24)Marchantia polymorpha L.,
Plagiochasma intermedium Lindenb. & Gotische		Marchantiacea,
Aytoniaceae		Candida albicans (MIC 256 μg/mL)[97]
Neomarchantin A
(25, R=H)
Neomarchantin B
(26, R=OH)		Marchantia polymorpha L.MarchantiaceaeCandida albicans[96]
Riccardin C (27)Asterella angusta (Stephani) Pandé, K.P. Sri-vast. & Sultan Khan,
Plagiochasma intermedium Lindenb. & Gotische		Aytoniaceae,
Aytoniaceae		Candida albicans[97]
Riccardiphenol C (16)Riccardia crassa Schwägr.AneuraceaeCandida albicans,
Trichophyton mtagropbytes		[90]
IC50: the concentration of a drug that is required for 50% inhibition in vitro; MIC—minimum inhibitory concentration. Bold numbers refer to the chemical structures o Bold numbers refer to the chemical structures of compounds are presented in Figure 2 and Figure 3.
Table
Table 6. Cytotoxic compounds isolated from bryophytes with modern uses.
Table 6. Cytotoxic compounds isolated from bryophytes with modern uses.
CompoundsSpeciesFamilyActivity AgainstRef.
Jungermannenone A (28, R=OH),
Jungermannenone B (29 R=H)		Jungermannia species L.JungermanniaceaeHuman leukemia HL-60 cells
(JA IC50 1 1.3 μM),
PC3 (JA 1.5 μmol/L, JB 5 μmol/L)		[3,99]
Lunularin (6)Dumortiera hirsuta (Sw.) NeesWeisnerellaceaeHepG2 (IC50 = 7.4 μg/mL)[87]
Marchantin A (13)Marchantia species L.MarchantiaceaeHuman MCF-7 breast
cancer (IC50 4.0 μg/mL),
chemoresistant prostate cancer PC3 cells,
A375 melanoma cells
(IC50 = 7.45–11.97 μg/mL)		[3,100,101]
Marsupellone (30)Marsupella emarginata
(Ehrh.) Dumort.		GymnomitriaceaeaP388 cancer cell line
(ID50 1 μg/mL)		[88]
Neomarchantin A
(25, R=H),
Neomarchantin B
(26, R=OH)		Marchantia polymorpha L., Schistochila glaucescens
(Hook.) A.Evans		Marchantiaceae,
Schistochilaceae		P388 cell line (IC50 8–18 μg/mL)[102]
Pallidisetin A (31)
Pallidisetin B (32)		Polytrichum pallidisetum FunckPolytrichaceaeMelanoma (RPMI-7951),
Glioblastoma multiforme (U-251)		[103]
Plagiochin E (33)Plagiochasm intermedium
Lindenb. & Gottsche		AytoniaceaeChemoresistant prostate cancer PC3 cells (IC50 5.99 µmol/L)[100]
Riccardin C (27)Plagiochasma intermedium
Lindenb. & Gottsche,
Reboulia hemisphaerica, (L.) Raddi		AytoniaceaeChemoresistant prostate cancer PC3 cells (IC50 3.22 µmol/L), [100,104]
Riccardiphenol C (16)Riccardia crassa Schwägr.AneuraceaeBSC cells [90]
Sacculatal (15)Pellia endiviifolia
(Dicks.) Dumort.		PelliaceaeHuman melanoma (IC50 2–4 µmol/L), Lu1 (IC50 5.7 µmol/L),
KB (IC50 3.2 µmol/L),
LNCaP and ZR-75-1 cells
(IC50 7.6 µmol/L)		[105]
Trewiasine (34)Isothecium subdiversiforme Broth,
Thamnobryum sandei Besch.		Brachytheciaceae,
Neckeraceae		U937 cells, ascitic tumors S180, hepatoma, U14, solid tumor Lewis lung carcinoma[106]
1 IC50: the concentration of a drug that is required for 50% inhibition of cell growth in vitro. Bold numbers refer to the chemical structures o Bold numbers refer to the chemical structures of compounds are presented in Figure 3 and Figure 4.
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Dziwak, M.; Wróblewska, K.; Szumny, A.; Galek, R. Modern Use of Bryophytes as a Source of Secondary Metabolites. Agronomy 2022, 12, 1456. https://doi.org/10.3390/agronomy12061456

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Dziwak M, Wróblewska K, Szumny A, Galek R. Modern Use of Bryophytes as a Source of Secondary Metabolites. Agronomy. 2022; 12(6):1456. https://doi.org/10.3390/agronomy12061456

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Dziwak, Michał, Katarzyna Wróblewska, Antoni Szumny, and Renata Galek. 2022. "Modern Use of Bryophytes as a Source of Secondary Metabolites" Agronomy 12, no. 6: 1456. https://doi.org/10.3390/agronomy12061456

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