Cyanobacteria as Biocatalysts

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This entry is adapted from the peer-reviewed paper 10.3390/catal11111259

Cyanobacteria constitute an interesting group of photosynthetic microorganisms due to their morphological and genetic diversity that is related to their extremely long evolution process. 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. In the field of biotechnology, biocatalysis, is enriched by the enzymatic systems of cyanobacteria, regarding their uniqueness as photosynthesis-dependent organisms.

cyanobacteria biocatalysts green chemistry

1. Cyanobacteria- short introduction

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 ^[1]. Microalgae appear in various morphological forms, and there are different models of metabolism ^[2]. They are microorganisms capable of oxygenic photosynthesis, which is related to the presence of two photosystems connected in series ^[3]. 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 ^[4]. 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) ^[5]. 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) ^[6]. 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) ^[7]. There are also lipids in cell membranes, mainly triglycerides. Their content is related to the response to environmental stress, e.g., salt stress ^[8]. During cold shock, fatty acids are desaturated. This is because low temperature induces up the expression of the desaturase genes ^[9]. 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 ^[10].

Scheme 1. Conversion of 2-oxoglutarate to succinate in the TCA cycle in cyanobacteria ^[6]. 2-OGDH—2-oxoglutarate dehydrogenase, 2-OGDC—2-oxoglutarate decarboxylase, SSADH—succinic semialdehyde dehydrogenas.

2. 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) ^[11].

Scheme 2. Biotransformation of enone to S-ketone using Synechococcus sp. PCC 7942 as biocatalysts ^[11].

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) ^[12].

Scheme 3. Acetophenone reduction reaction to 1-(S)-phenylethanol and 1-(R)-phenylethanol using a cyanobacterial strain as a biocatalyst ^[12].

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. PCC 6803 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. PCC 6803) ^[13].

Scheme 4. The biotransformation process of (+)-camphorquinone to (-)-(3S)-exo-hydroxycamphor with yield of 94% by the strain Synechosystis sp. PCC 6803 ^[13].

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 ^[14]^[15]. 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% ^[16]. 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) ^[17].

Scheme 5. The bioreduction reaction of diethyl 2-oxo-2-phenylethylphosphonate to diethyl (S)-2-hydroxy-2-phenylethylphosphonate with a Nodularia sphaerocarpa strain ^[17].

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 ^[18].

References

Jodlbauer, J.; Rohr, T.; Spadiut, O.; Mihovilovic, M.D.; Rudroff, F. Biocatalysis in Green and Blue: Cyanobacteria. Trends Biotechnol. 2021, 39, 875–889.
Abed, R.M.M.; Dobretsov, S.; Sudesh, K. Applications of cyanobacteria in biotechnology. J. Appl. Microbiol. 2009, 106, 1–12.
Blankenship, R.E.; Hartman, H. The origin and evolution of oxygenic photosynthesis. Trends Biochem. Sci. 1998, 23, 94–97.
Casella, S.; Huang, F.; Mason, D.; Zhao, G.-Y.; Johnson, G.N.; Mullineaux, C.W.; Liu, L.-N. Dissecting the Native Architecture and Dynamics of Cyanobacterial Photosynthetic Machinery. Mol. Plant 2017, 10, 1434–1448.
Lu, X. A perspective: Photosynthetic production of fatty acid-based biofuels in genetically engineered cyanobacteria. Biotechnol. Adv. 2010, 28, 742–746.
Steinhauser, D.; Fernie, A.R.; Araújo, W.L. Unusual cyanobacterial TCA cycles: Not broken just different. Trends Plant Sci. 2012, 17, 503–509.
Kieninger, A.-K.; Maldener, I. Cell–cell communication through septal junctions in filamentous cyanobacteria. Curr. Opin. Microbiol. 2021, 61, 35–41.
Singh, S.; Sinha, R.P.; Häder, D. Role of Lipids and Fatty Acids in Stress Tolerance in Cyanobacteria. Acta Protozool 2002, 41, 297–308.
Ntambi, J.M. (Ed.) Stearoyl-CoA Desaturase Genes in Lipid Metabolism; Springer: New York, NY, USA, 2013; ISBN 978-1-4614-7968-0.
de la Rosa, F.; De Troch, M.; Malanga, G.; Hernando, M. Differential sensitivity of fatty acids and lipid damage in Microcystis aeruginosa (cyanobacteria) exposed to increased temperature. Comp. Biochem. Physiol. Part C Toxicol. Pharmacol. 2020, 235, 108773.
Shimoda, K.; Kubota, N.; Hamada, H.; Kaji, M.; Hirata, T. Asymmetric reduction of enones with Synechococcus sp. PCC 7942. Tetrahedron Asymmetry 2004, 15, 1677–1679.
Żymańczyk-Duda, E.; Głąb, A.; Górak, M.; Klimek-Ochab, M.; Brzezińska-Rodak, M.; Strub, D.; Śliżewska, A. Reductive capabilities of different cyanobacterial strains towards acetophenone as a model substrate—Prospect of applications for chiral building blocks synthesis. Bioorg. Chem. 2019, 93, 102810.
Utsukihara, T.; Chai, W.; Kato, N.; Nakamura, K.; Horiuchi, C.A. Reduction of (+)- and (−)-camphorquinones by cyanobacteria. J. Mol. Catal. B Enzym. 2004, 31, 19–24.
Sandoval, B.A.; Hyster, T.K. Emerging strategies for expanding the toolbox of enzymes in biocatalysis. Curr. Opin. Chem. Biol. 2020, 55, 45–51.
Obexer, R.; Godina, A.; Garrabou, X.; Mittl, P.R.E.; Baker, D.; Griffiths, A.D.; Hilvert, D. Emergence of a catalytic tetrad during evolution of a highly active artificial aldolase. Nat. Chem. 2017, 9, 50–56.
Köninger, K.; Gómez Baraibar, Á.; Mügge, C.; Paul, C.E.; Hollmann, F.; Nowaczyk, M.M.; Kourist, R. Recombinant Cyanobacteria for the Asymmetric Reduction of C=C Bonds Fueled by the Biocatalytic Oxidation of Water. Angew. Chem. Int. Ed. 2016, 55, 5582–5585.
Górak, M.; Żymańczyk-Duda, E. Application of cyanobacteria for chiral phosphonate synthesis. Green Chem 2015, 17, 4570–4578.
Wang, Z.; Cui, X.; Wang, C.; Huang, J.; Geng, D. Biotransformation of 6-deoxypseudoanisatin by Synechocystis sp. PCC6803. J. Tradit. Chin. Med. Sci. 2014, 1, 135–139.

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Subjects: Biotechnology & Applied Microbiology

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Agnieszka Śliżewska

Ewa Żymańczyk-Duda

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Update Date: 23 Nov 2021

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1. Cyanobacteria- short introduction

2. Cyanobacteria as Biocatalysts

References