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Review

Cyanobacteria as Valuable Tool in Biotechnology

by
Agnieszka Śliżewska
* and
Ewa Żymańczyk-Duda
Department of Biochemistry, Molecular Biology and Biotechnology, Faculty of Chemistry, Wrocław University of Science and Technology, Wybrzeże Stanisława Wyspiańskiego 27, 50-370 Wrocław, Poland
*
Author to whom correspondence should be addressed.
Catalysts 2021, 11(11), 1259; https://doi.org/10.3390/catal11111259
Submission received: 3 September 2021 / Revised: 13 October 2021 / Accepted: 18 October 2021 / Published: 20 October 2021
(This article belongs to the Special Issue Biosynthesis and Biocatalysis)
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Abstract

:
Cyanobacteria constitute an interesting group of photosynthetic microorganisms due to their morphological and genetic diversity that is related to their extremely long evolution process, which created the need for them to adapt to immensely heterogeneous environmental conditions. Cyanobacteria grow in salt and fresh waters as well as on the surface of soils and rocks. The diverse cell structure is characterized by the fact that they occur in many morphological forms, from small single cells through to larger ones as well as branches, threads, or spirals. Taking into account the presence of cyanobacteria in virtually all possible conditions and places on Earth, cyanobacteria represent an unexplored potential that is worth investigating. This review presents the possibilities of using algae in chosen areas of biotechnology: e.g., as biocatalysts or in industries such as the pharmaceutical industry. It covers the characteristics of secondary metabolites along with their division and the potential of using them as sources of effective drugs for many diseases. It presents an overview of the possibilities of using cyanobacteria in biotransformation processes. These processes are of great importance in the case of, for example, the neutralization of municipal, industrial, or chemical waste, the amount of which is constantly growing every year, and they are also an easier and cheaper path to obtain chemical compounds.

1. Introduction

Although biocatalysis is a powerful and promising tool used for organic synthesis, it can nevertheless generate problems related, for example, to the transfer of scale from laboratory to industrial or environmental issues [1]. Both the traditional synthesis processes and the green chemistry processes (e.g., biocatalysis) should undergo an environmental impact assessment. The E factor (environmental factor) is an indicator that allows the assessment of the environmental footprint of biocatalysis. It shows how much environmental waste is generated by the green chemistry processes. This factor will take into account all parameters of the process, e.g., reaction solvents and other chemicals yields [1,2].
The reduction of the number of steps in the synthesis of chemical compounds or the possibility of carrying out the processes of lower amount of solvents and of higher selectivity comparing to chemical synthesis are among others the few advantages of using cyanobacteria as biocatalysts [3]. In contradiction to the application of microorganisms requiring carbohydrate compounds, which usually increases the costs of bioprocesses, applying the phototrophic cyanobacteria can be a cheaper alternative thanks to their photoautotrophic metabolism [4]. Thus, autotrophs are an interesting biotransformation tool.
Basically, cyanobacteria exist as populations of mixed cultures, unialgal cultures, and axenic cultures. In the environment, algae live not only with other microorganisms but also with plants or animals as a part of biocenosis. Isolation of the axenic culture is a time-consuming and relatively difficult task, because it requires the restoration of natural conditions with the simultaneous elimination of other organisms or algae. This increases the cost-effectiveness in the case of bioprocesses, which employ cyanobacteria [5]. Cyanobacteria are an attractive research object due to the above features. Figure 1 presents the issues described in detail in the article, which are a part of the possible applications and characteristics of these microorganisms.

2. Cyanobacteria—Unique Microorganisms

The use of tools provided by nature to facilitate, for example, chemical synthesis is worth exploring. In case of cyanobacteria, photosynthesis, which allows converting the inorganic matter into organic one under the influence of light energy, is the advantage above other microbes, which require organic carbon sources for living [3]. Microalgae appear in various morphological forms, and there are different models of metabolism [6]. They are microorganisms capable of oxygenic photosynthesis, which is related to the presence of two photosystems connected in series [7]. Cyanobacterial thylakoid membranes are unique, since their lipid bilayers include the entire system of respiratory electron transport chains enabling the photosynthesis process. The photosystem of these microorganisms consists of photosystem I (PSI), photosystem II (PSII), cytochrome (Cyt)b6f, and ATP synthase (ATPase) complexes [8]. As cyanobacteria belong to the prokaryote kingdom and also possess plant traits, this results in them having the positive characteristics of both. The ability to carry out oxygenic photosynthesis such as plants and the susceptibility to genetic manipulation make them suitable candidates for many processes, e.g., biofuel production or to enrich soil with nitrogen compounds (bio-fertilizers) [9]. Cyanobacteria are unique microorganisms in many respects. The Krebs cycle in cyanobacteria is a special process because it does not normally follow the conversion of 2-oxoglutarate to succinyl-CoA by 2-OGDH (2-oxoglutarate dehydrogenase)—this enzyme is not present in cyanobacteria. However, there is an alternative transformation pathway using two enzymes: 2-oxoglutarate decarboxylase (2-OGDC) and succinic semialdehyde dehydrogenase (SSADH). The resulting intermediate is succinic semialdehyde, from which succinate is obtained (Scheme 1) [10]. Cyanobacteria as Gram-negative prokaryotic microorganisms have an outer membrane that is composed of liposaccharides. Additionally, the system of intercellular communication is very important in the case of multicellular organisms. This system is referred to as septal junctions (SJs) [11]. There are also lipids in cell membranes, mainly triglycerides. Their content is related to the response to environmental stress, e.g., salt stress [12]. During cold shock, fatty acids are desaturated. This is because low temperature induces up the expression of the desaturase genes [13]. Their respond to adaptation to changes in their environment (stress caused by temperature, salinity, osmotic stress, etc.) is a change in the composition of fatty acids [14].

3. Cyanobacteria as Biocatalysts

One of the best known and most widespread biocatalysis reactions among these catalyzed by cyanobacteria is the reduction of C = C bonds and carbonyl functionalities. The strain Synechococcus sp. PCC 7942 is able to reduce enones asymmetrically. After biotransformation, S-trans enones give products in the form of corresponding (S)-ketones. The obtained (S)-ketones were formed in some cases with the enantiomeric excess 98% and yield more than 99% (Scheme 2) [15].
The bioreductive abilities of the following cyanobacteria strains have been demonstrated: Arthrospira maxima, Leptolyngbya foveolarum, Nodularia sphaerocarpa, and Synechococcus bigranulatus. They are able to reduce acetophenone, and depending on the applied strain and on the biotransformation conditions, appropriate chiral alcohols (1-(S)-phenylethanol, 1-(R)-phenylethanol) were received with enantiomeric excess ranging from 36.9% to 95.7% depending on the strain used (Scheme 3) [16].
By examining cyanobacteria in terms of their reducing abilities, the influence of light on the biotransformation process was also investigated. The Synechococcus elongatus PCC 7942 and Synechosystis sp. PCC6803 strains are capable of reducing (+) and (-) camphorquinones to corresponding hydroxyketones. In the case of the two tested strains and the use of (+)-camphorquinone as a substrate, the isomer from the resulting mixture of isomers that is formed with the highest yield (over 90%) is (-)-(3S)-exo-hydroxycamphor (Scheme 4). It has been observed that the process also takes place in the dark, but these are low selective comparing to the light conditions. (-)-(3S)-exo-hydroxycamphor was formed slowly and with the following efficiency: 72% (Synechococcus elongatus PCC 7942) and 68% (Synechosystis sp. PCC6803) [17].
The literature data note that the biocatalytic features of cyanobacteria can be improved by mutations or genetic engineering methods, directing to the enzymes activities’ improvement [18,19]. It has been shown that the inclusion of the YqjM enate reductase gene from genomic DNA from Bacillus subtilis into the genome of Synechocystis sp. PCC 6803 results in the ability of cyanobacteria to convert the substrate 2-methyl-N-methylmaleimide. For this process, the control of the light-inducible psbA2 promoter is crucial. The substrate is reduced to (R)-2-methyl-N-methylsuccinimide, which is characterized by high optical purity: enantiomeric excess was over 99% [20]. Cyanobacteria can also be used for chiral phosphonate synthesis and more specifically for the enantioselective bioreduction of diethyl esters of oxophosphonic acids. The Nodularia sphaerocarpa strain is capable of enantioselective bioreduction of the diethyl 2-oxo-2-phenylethylphosphonate to diethyl (S)-2-hydroxy-2-phenylethylphosphonate with a degree of conversion of 99% and an enantiomeric excess of 92% (Scheme 5) [21].
Whole cells can be used without enzyme isolation, which also reduces the costs of the process. An interesting example is the use of the Synechocystis sp. strain for bioconversion of the 6-deoxypseudoanisatin into a product that has a substrate-like MS spectrum—this may indicate that the product is a substrate isomer. The aim of the experiment was to search for compounds of biological activity and of industrial applicability (e.g., pharmaceuticals production). The biotransformation product has a lower polarity than the substrate. This paves the way for the future of secoprezizaane-type sesquiterpenes, which could potentially be used in medicine [22].

4. Secondary Metabolites

Cyanobacteria are not only natural machines for transforming chemicals into desired products but also the source of many compounds of various activities, which are synthesized via secondary metabolic pathways. The secondary metabolites of cyanobacteria constitute a diverse group of compounds, including mainly peptides (e.g., anabaenopeptin E), terpenes (e.g., β-carotene), polyketides (e.g., cylindrocyclophane A), alkaloids (e.g., hapalindole A), lipids (e.g., lyngbic acid), and others. Data confirm the number of over 1100 compounds, and most of them are identified for strains of the genus: Lyngbya, Microcystis, Nostoc, and Hapalosiphon [23]. These metabolites can have a positive and negative function. Examples of metabolites of toxic features include, for example, the groups of hepatotoxins, neurotoxins, or cytotoxins, while the group of non-toxic properties includes phytohormones, UV-protective compounds, or metabolites of antimicrobial properties [24]. Table 1 shows selected natural compounds of positive action toward human health, depending on their activity, along with exemplary strains producing the indicated metabolites. Research related to the cyanobacteria applications are still in progress mostly because these organisms are not fully explored, so their possible applications are still in front of us, waiting to be discovered. They have the ability to adapt to a variety of environmental conditions. It is estimated that cyanobacteria already existed 3.5 billion years ago [25].

4.1. Antimicrobial Compounds

Growing antibiotic resistance and pathogen mutations are currently a big problem in the treatment of many infectious diseases. It is necessary to look for new biologically active compounds with anti-infective properties. Cyanobacteria may be a potential source of such metabolites, but it still requires careful investigation due to the cytotoxicity of many secondary metabolites isolated from cyanobacteria [69]. The most efficient in terms of the amount of produced metabolites are the cyanobacteria belonging to Oscillatoriales, Nostocales, Chroococcales, and Synechococcales [23]. A significant problem and a challenge is to understand the mechanism of action of biologically active compounds derived from cyanobacteria. Some filamentous cyanobacteria have the ability to produce antibiotics to fight other strains of cyanobacteria as a defense mechanism to help them survive in a given environment [70]. Examples of such compounds are cyanobacterin LU-1 and LU-2, isolated from the Nostoc linckia strain, which inhibit the growth of other cyanobacteria (photosynthesizing organisms). These compounds did not show similar activity against non-photosynthetic microorganisms [71]. Hapalindole-related alkaloids isolated from the strain Fischerella ambigua show antimicrobial activity. Their activity was tested against the following strains: M. tuberculosis, B. anthracis, Staphylococcus aureus, M. smegmatis, E. coli, and C. albicans. The compound fischambiguine B against M. tuberculosis showed an impressive effect due to the minimum inhibitory concentration of 2 µM [72].

4.2. Antifungal Compounds

Hassallidins isolated from cyanobacterial species belonging to, inter alia, Anabaena, Nostoc, and Planktothrix exhibit antifungal activity [73]. Tests performed with Aspergillus fumigatus and Candida albicans confirmed the antifungal activity of hassallidin A isolated from Hassallia sp. Hassallidins are glycosylated lipopeptides [74]. Hassallidin A is active against several Candida strains, Cryptococcus neoformans, and Aspergillus species. Concentrations that show the minimum inhibitory concentration are between 4 and 8 µg/mL [75]. Hassallidin B, isolated from the same family of cyanobacteria, has similar antifungal properties as hassallidin A, but it has better water solubility [63].

4.3. Antiviral Compounds

The search for drugs against human immunodeficiency virus (HIV) is an equally important problem of global concern as the search for anticancer drugs. Cyanobacteria are also a source of compounds with antiviral activity. An example of a compound with potential anti-HIV properties is scytovirin (SVN). Structurally, it is a protein with a molecular weight of 9713 Da and consists essentially of two apparent domains. This compound was isolated from the strain Scytonema varium [76]. For scytovirin to be used as an anti-HIV drug, research is needed to understand how it binds to the viral carbohydrate glycoproteins. A detailed study of its structure provided a lot of valuable information, among others that the structure of this compound introduces a new fold and a new twist to carbohydrate-binding proteins. [77]. This compound was also tested for the inhibition of replication of other viruses. Studies investigating the effect of scytovirin on Zaire Ebola virus have provided information about its positive effect, resulting in nine out of 10 infected mice being cured (dose of 30 mg/kg/day), and all untreated mice died. The mechanism of action is based on a specific bond with the mucin region glycosylated envelope glycoprotein [78].

4.4. Anticancer Compounds

An extremely important topic is the search for active biological compounds of anticancer properties. These compounds are not only potential compounds for future use but also already a reality in the treatment of certain types of cancer [79]. Compounds of anti-tumor features derived from cyanobacteria mainly belong to the group of peptides [80]. It is very important to understand the mechanisms of action of biologically active compounds; e.g., they can inhibit angiogenesis or influence the tubulin–microtubule balance, and they have other abilities, too. There are some peptides of anticancer activity; however, their action has not been examined yet. [81]. Biologically active compounds derived from cyanobacteria can also induce apoptotic death or affect the cell signaling paths through activation of the members of the protein kinase-c family of signaling enzymes [82]. An interesting example is largazole from the cyanobacterial genus Symploca. The initial screening tests have shown its effectiveness against inter alia colorectal cancer, breast cancer, lung cancer, prostate cancer, or human malignant melanoma, and interestingly, the mechanism of action is different depending on the type of cancer cells [83]. Largazole has been shown to be active against highly invasive human mammary epithelial cells (MDA-MB-231) [44]. The source of another interesting bioactive compound—ankaraholides A (belonging to glycosylated swinholides) is a strain of cyanobacteria Geitlerinema sp. from the Madagascar field collection. Studies have shown that the isolated compound is able to inhibit the expanding the following cell lines: NCI-H460 (human lung cancer), Neuro-2a (mouse neuroblastoma), and MDA-MB-435 (the human melanoma) [50]. In addition, lagunamides A and B, which are structurally cyclic depsipeptides, showed a very broad activity in terms of potential anticancer properties. These compounds come from a strain that is the source of many compounds of biological activity—Lyngbya majuscula. Lagunamide A has been tested over a wider range of targets than lagunamides B, which has been tested (with a positive but lower effect than that of the first compound) on the P388 and HCT8 cell lines. Lagunamide A showed inhibitory effects on the following cell lines: P388, HCT8, A549, PC3, and SK-OV3 [84]. Considering the mechanisms of action of biologically active compounds causing cancer cell death, a noteworthy example is desmethoxymajusculamide C (DMMC)—cyclic depsipeptide, which has been tested in the cyclic form but also in the ring-opened form in terms of potential actin depolymerization. It was isolated from Lyngbya majuscula. The mechanism of action induced the complete disruption of cellular microfilament networks and generated binucleated cells [85]. Cyanobacteria are a potential source of anticancer drugs, as evidenced by numerous studies. The mechanisms of action are highly varied and require detailed research. In the case of the compound with anticancer activity, which is largazole, the mechanism of action is based on HDAC (histone deacetylases) inhibition. This was confirmed with human HCT116 colon cancer cells [86].

4.5. Sunscreen Compounds

Cyanobacteria, as photoautotrophs, in order to protect themselves against excessive ultraviolet radiation, are capable of producing metabolites that exhibit photoprotective properties. These include scytonemin and mycosporine-like amino acids (MAAs), which are photostable compounds of antioxidant properties [87]. The novel scytonemin-3a-imine isolated from the cyanobacterial strain Scytonema hoffmani or Scytonema spp. apart from the above-mentioned properties, e.g., high probability against reactive oxygen species, additionally shows a very important function of protection against water loss, which can help cyanobacteria survive under stressful conditions such as intense sunlight [88].
In addition, carotenoids produced by microalgae are important not only as sunscreen compounds, as demonstrated by the increase in their concentration when exposed to UV-A radiation, but also as powerful antioxidants. It is related to their singlet oxygen quenching, releasing excessive light energy and radical scavenging [89].

5. Cyanobacterial Toxins

Secondary metabolites derived from cyanobacteria are not only biologically active compounds of positive properties. Compounds of toxic properties are also a very interesting group. These allow microorganisms to survive under extreme conditions and fight for their position in a given environment, but they pose serious threats to human health and the environment [90]. The bioaccumulation and bioconcentration of toxins inside aquatic organisms can be a serious problem here, which results in the introduction of toxins (e.g., neurotoxins) to the organisms representing the next stages of the food chain. The consequence of this is a negative impact on human health and life [91]. Table 2 shows the basic division of cyanotoxins into hepatotoxins, neurotoxins, and dermatoxins with examples.

5.1. Hepatotoxin

Undoubtedly, microcystin, nodularins, and cylindrospermopsin, which are classified as hepatotoxins, not only have a negative impact on human health but can also lead to the death of other animals [103]. It is related among others to their presence in drinking water—mainly microcystins. Therefore, it is very important to use effective and sensitive methods to detect these compounds in water, so that their concentration does not exceed the guidelines for drinking water [104]. The mechanism of action of microcystins is based on the inhibition of protein phosphatases 1 (PP1) and protein phosphatases 2A (PP2A): they are strong and specific inhibitors [105]. In terms of structure, microcystins and nodularins are cyclic peptides, while cylindrospermopsin is a cyclic guanidine alkaloid [106]. Compared to microcystins, the mechanism of action of nodularins mainly involves the inhibition of PPA2, and similar to other hepatotoxins, it causes liver damages. Taking into account the threat they pose, it has been shown that the organisms of the Baltic Sea have the highest concentration of nodularins [107]. The mechanism of action of the other hepatoxin, cylindrospermopsin, is different, as it also differs in structure from the other toxins. The mechanism of action of cylindrospermopsin is based on the inhibition of reduced glutathione and protein synthesis and inhibition of cytochrome P450 activity [108]. Cylindrospermopsin poses a serious threat to animals in Australia due blooms of cyanobacteria in lakes and freshwater reservoirs [109].

5.2. Neurotoxin

Cyanobacterial neurotoxins include a large number of compounds: β-N-methylamino-L-alanine, anatoxin-a, homoanatoxin-a, anatoxin-a (s), and saxitoxins [96,97,98,99,100]. β-N-methylamino-L-alanine (Figure 2) is structurally a non-protein amino acid.
An extremely interesting fact is the suspicion that this compound may cause amyotrophic lateral sclerosis/parkinsonism–dementia complex (ALS/PDC). Research has shown the presence of this neurotoxin in the brain tissues of people suffering from Alzheimer’s disease [96]. Anatoxin-a (Figure 3) is a bicyclic amine and belongs to the family of alkaloids [110].
Neurotoxins have also been shown to exhibit phytotoxic activity. In addition to its negative effect on mammals, it also affects aquatic plants (e.g., Ceratophyllum demersum) and terrestrial plants (e.g., Medicago sativa). This effect is observed through reduced photosynthetic oxygen production, increased peroxidase (POD) and glutathione S-transferase (GST) activities (aquatic plants), and the inhibition of seed germination and decrease in the root growth (terrestrial plant) [111]. Another toxin, although it may be confused with anatoxin-a in terms of its name, is anatoxin-a(s) (Figure 4), which is fundamentally different in structure from the previous one.
The mechanism of action of anatoxin-a(s) is based on the inhibition of the activity of acetylcholinesterase, and in terms of its structure, it can be classified as organophosphate [112]. Homoanatoxin-a (Figure 5), unlike anatoxin-a(s), is structurally similar to anatoxin-a [113].
This compound increases the acetylcholine release, the consequence of which is a neuromuscular depolarizing blockade of nicotinic cholinergic receptors in the muscles of mammals [114]. This toxin led to the death of five dogs in New Zealand in 2005. This was due to the presence of cyanobacteria blooms in the Hutt River, which the dogs had contacted [115]. Blocking voltage-gated sodium channels in neurons is how saxitoxin (Figure 6) works [116]. This toxin is structurally a trialkyl tetrahydropurine [117]. Saxitoxin poses a threat to the environment, which is similar to all neurotoxins. On the other hand, a noteworthy example of its negative effects is a disease called paralytic shellfish poisoning (PSP). The reason for its formation is the presence of saxitoxins in seafood, which may result in, for example, headaches or breathing problems, which may be a threat to human life [118].

5.3. Dermatoxin

Debromoaplysiatoxin can cause erythematous pustular folliculitis or cause dermatitis in humans [119]. Structurally, it is a bicyclic diolide. Contact dermatitis caused by this toxin is called swimmers itch [120]. A study in mice showed that injecting the toxin causes diarrhea, while at a dose of 10 μg/mouse, it resulted in death in 12 h [121]. Lyngbyatoxin-a, due to the fact that it is a potent activator of protein kinase C (PKC), may contribute to the formation of skin cancer [122]. It turns out that dermatitis is not the only effect that can occur after contact with this toxin. Additional but rare symptoms may include swelling of the face and eyes, throat irritation, and fatigue [123]. Aplysiatoxins have an analogous effect to lyngbyatoxins on the skin and also due to the fact that they are activators of protein kinase C (PKC), they can be tumor promoters [124].

6. Conclusions

Taking into account the examples of cyanobacterial features presented above, it is justified to conclude that cyanobacteria can be considered as a very versatile tool for biotechnology. To start, they are the source of a variety of secondary metabolites, which are formed inside the cells as a response for the environment impact, and we finish with an analysis of their usefulness in biocatalysis. The diversity of the metabolites’ structures derived from cyanobacteria are not accidental; they allow these organisms to adapt to diverse environmental conditions, leading to their presence all over the globe, acting as e.g., antioxidants or antimicrobial factors. The identification and understanding of the mechanisms of action of these metabolites is a scientifically important task, which leads to introducing them into the different areas of human needs (e.g., medicine). In addition, the other field of biotechnology, biocatalysis, is enriched by the enzymatic systems of cyanobacteria, regarding their uniqueness as photosynthesis-dependent organisms. The presented examples proved that this space has been explored in a very narrow scope; however, the described data proved that as biocatalysts, they differ from other commonly applied organisms such as fungi. It can be predicted that the number of applications of cyanobacteria will be growing with time as a consequence of deep exploring of the biochemistry of their metabolic pathways and their culturing requirements.

Author Contributions

Conceptualization, A.Ś. and E.Ż.-D.; writing—original draft preparation, A.Ś. and E.Ż.-D.; writing—review and editing, A.Ś. and E.Ż.-D. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by a subsidy from the Ministry of Education and Science for the Faculty of Chemistry of Wrocław University of Science and Technology (subsidy nr: 8211104160).

Conflicts of Interest

The authors declare no conflict of interest.

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Catalysts 11 01259 g001 550
Figure 1. Selected applications of cyanobacteria.
Figure 1. Selected applications of cyanobacteria.
Catalysts 11 01259 g001
Catalysts 11 01259 sch001 550
Scheme 1. Conversion of 2-oxoglutarate to succinate in the TCA cycle in cyanobacteria [10]. 2-OGDH—2-oxoglutarate dehydrogenase, 2-OGDC—2-oxoglutarate decarboxylase, SSADH—succinic semialdehyde dehydrogenas.
Scheme 1. Conversion of 2-oxoglutarate to succinate in the TCA cycle in cyanobacteria [10]. 2-OGDH—2-oxoglutarate dehydrogenase, 2-OGDC—2-oxoglutarate decarboxylase, SSADH—succinic semialdehyde dehydrogenas.
Catalysts 11 01259 sch001
Catalysts 11 01259 sch002 550
Scheme 2. Biotransformation of enone to S-ketone using Synechococcus sp. PCC 7942 as biocatalysts [15].
Scheme 2. Biotransformation of enone to S-ketone using Synechococcus sp. PCC 7942 as biocatalysts [15].
Catalysts 11 01259 sch002
Catalysts 11 01259 sch003 550
Scheme 3. Acetophenone reduction reaction to 1-(S)-phenylethanol and 1-(R)-phenylethanol using a cyanobacterial strain as a biocatalyst [16].
Scheme 3. Acetophenone reduction reaction to 1-(S)-phenylethanol and 1-(R)-phenylethanol using a cyanobacterial strain as a biocatalyst [16].
Catalysts 11 01259 sch003
Catalysts 11 01259 sch004 550
Scheme 4. The biotransformation process of (+)-camphorquinone to (-)-(3S)-exo-hydroxycamphor with yield of 94% by the strain Synechosystis sp. PCC6803 [17].
Scheme 4. The biotransformation process of (+)-camphorquinone to (-)-(3S)-exo-hydroxycamphor with yield of 94% by the strain Synechosystis sp. PCC6803 [17].
Catalysts 11 01259 sch004
Catalysts 11 01259 sch005 550
Scheme 5. The bioreduction reaction of diethyl 2-oxo-2-phenylethylphosphonate to diethyl (S)-2-hydroxy-2-phenylethylphosphonate with a Nodularia sphaerocarpa strain [21].
Scheme 5. The bioreduction reaction of diethyl 2-oxo-2-phenylethylphosphonate to diethyl (S)-2-hydroxy-2-phenylethylphosphonate with a Nodularia sphaerocarpa strain [21].
Catalysts 11 01259 sch005
Catalysts 11 01259 g002 550
Figure 2. β-N-methylamino-L-alanine.
Figure 2. β-N-methylamino-L-alanine.
Catalysts 11 01259 g002
Catalysts 11 01259 g003 550
Figure 3. Anatoxin-a.
Figure 3. Anatoxin-a.
Catalysts 11 01259 g003
Catalysts 11 01259 g004 550
Figure 4. Anatoxin-a(s).
Figure 4. Anatoxin-a(s).
Catalysts 11 01259 g004
Catalysts 11 01259 g005 550
Figure 5. Homoanatoxin-a.
Figure 5. Homoanatoxin-a.
Catalysts 11 01259 g005
Catalysts 11 01259 g006 550
Figure 6. Saxitoxin.
Figure 6. Saxitoxin.
Catalysts 11 01259 g006
Table
Table 1. Selected biologically active compounds derived from cyanobacteria.
Table 1. Selected biologically active compounds derived from cyanobacteria.
Biological ActivityActive CompoundCyanobacteria Ref.
antibacterialcybastacines A and BNostoc sp.[26]
crossbyanols B,C,DLeptolyngbya crossbyana[27]
nostotrebin 6Nostoc sp. str. Lukešová 27/97[28]
c-phycocyaninSpirulina platensis[29]
comnostins A–ENostoc commune[30]
kawaguchipeptin BMicrocystis aeruginosa NIES-88[31]
hapalindole TFischerella sp.[32]
lyngbyazothrins A−DLyngbya sp. 36.91[33]
anticancerapratoxin A,DLyngba majuscula, Lyngba sordida[34,35]
veraguamides A-C and H-Lcf. Oscillatoria margaritifera[36]
tasiamide, tasiamide BSymploca sp.[37,38]
desmethoxymajusculamide C (DMMC)Lyngba majuscula[39]
c-phycocyaninSpirulina platensis[40]
coibamide ALeptolyngbya sp.[41]
calothrixin ACalothrix[42]
laxaphycins B4 and A2Hormothamnion enteromorphoides[43]
largazoleSymploca sp.[44]
dolastatin 10Symploca sp. VP642[45]
bisebromoamideLyngba sp.[46]
merocyclophanes A,BNostoc sp. UIC 10062[47]
curacin ALyngba majuscula[48]
palmyramide ALyngba majuscula[49]
ankaraholides AGeitlerinema sp. [50]
hantupeptin ALyngba majuscula[51]
antiviralcyanovirin-N (CV-N)Nostoc ellipsosporum[52]
scytovirinScytonema varium[53]
nostoflanNostoc flagelliforme[54]
o. agardhii agglutinin (OAA)Oscillatoria agardhii NIES-204[55]
sulphoquinovosyl diacylglycerolSpirulina platensis[56]
debromoaplysiatoxinTrichodesmium erythraeum[57]
3-methoxydebromoaplysiatoxinTrichodesmium erythraeum[27]
antifungallaxaphycins A and BAnabaena laxa FK-1-2[58]
hectochlorinLyngbya majuscula[59]
lyngbyabellin BLyngbya majuscula[60]
majusculamide CLyngbya majuscula[61]
balticidins A−D
hassallidin B		Anabaena cylindrica Bio33
Hassallia sp.		[62]
[63]
protease inhibitorspumiginsNodularia spumigena AV1
Nodularia spumigena CCY9414		[64]
molassamideDichothrix utahensis[65]
anabaenopeptin NZ 857Nostoc punctiforme PCC 73102[66]
nostamide ANostoc punctiforme PCC 73102[66]
anabaenopeptin A, B, CAnabaena sp. strain 90[66]
nodulapeptin B, CNodularia spumigena CCY9414[66]
microviridin JMicrocystis UOWOCC MRC[67]
microviridin BMicrocystis aeruginosa NIES298[67]
oscillapeptins BOscillatoria agardhii NIES-204[68]
oscillapeptins C-EOscillatoria agardhii NIES-205[68]
oscillapeptins FOscillatoria agardhii NIES-596[68]
sunscreenmycosporine-like amino acids (MAAs)Synechocystis sp. PCC 6803, Gloeocapsa sp. CU-2556, Aphanothece halophytica, Gloeocapsa sp., Euhalothece sp., Microcystis aeruginosa, Arthrospira sp. CU2556, Lyngbya sp. CU2555, Leptolyngbya sp., Phormidium sp., Lyngbya cf. aestuarii, Microcoleus chthonoplastes, Microcoleus sp., Oscillatoria spongelidae, Trichodesmium spp., Anabaena sp., Anabaena doliolum, Anabaena variabilis PCC 7937, Nostoc sp., Nostoc commune var. Vaucher, Nostoc commune, Scytonema sp., Nostoc punctiforme ATCC 29133, Nostoc sp. HKAR-2 and HKAR-6, Nodularia baltica, Nodularia harveyana, Nodularia spumigena, Aphanizomenon flos-aquae, Chlorogloeopsis PCC 6912[23]
carotenoidsall[23]
Table
Table 2. Cyanobacterial toxins.
Table 2. Cyanobacterial toxins.
Biological ActivityActive CompoundCyanobacteria Ref.
hepatotoxinmicrocystinMicrocystis aeruginosa PCC 7806[92,93]
Anabaena spp.
Oscillatoria agardhii
nodularinsNodularia spumigena[94]
cylindrospermopsinCylindrospermopsis raciborskii
Aphanizomenon ovalisporum,
Raphidiopsis curvata
Umezakia natans		[95]
neurotoxinβ -N-methylamino-L-alanineNostoc PCC 7107
Anabaena variabilis ATCC 29413		[96]
anatoxin-aAnabaena flos-aquae[97]
homoanatoxin-aOscillatoria formosa[98]
anatoxin-a(s)Anabaena flos-aquae NRC-525-17[99]
saxitoxinsAnabaena circinalis
Lyngbya wollei		[100]
dermatoxinlyngbyatoxins A-CLyngbya majuscula[101]
debromoaplysiatoxinLyngbya majuscula
Oscillatoria nigroviridis
Schizothrix calcicole		[102]
aplysiatoxinsLyngbya
Schizothrix
Planktothrix (Oscillatoria)		[102]
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Śliżewska, A.; Żymańczyk-Duda, E. Cyanobacteria as Valuable Tool in Biotechnology. Catalysts 2021, 11, 1259. https://doi.org/10.3390/catal11111259

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Śliżewska A, Żymańczyk-Duda E. Cyanobacteria as Valuable Tool in Biotechnology. Catalysts. 2021; 11(11):1259. https://doi.org/10.3390/catal11111259

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Śliżewska, Agnieszka, and Ewa Żymańczyk-Duda. 2021. "Cyanobacteria as Valuable Tool in Biotechnology" Catalysts 11, no. 11: 1259. https://doi.org/10.3390/catal11111259

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