Cyanobacteria as bio-factories for production of UV ... · Cyanobacteria as bio-factories for production of UV-screening compounds N Browne1, F Donovan1, P Murray1, SK Saha2* Cyanobacteria

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* Corresponding authorEmail: [email protected] Department of Applied Sciences, CHIMERA

Research Group, Limerick Institute of Tech-nology, Moylish Park, Limerick, Ireland (ROI)

2 Shannon Applied Biotechnology Centre, Limerick Institute of Technology, Moylish Park, Limerick, Ireland (ROI)

Cyanobacteria as bio-factories for production of UV-screening compounds

N Browne1, F Donovan1, P Murray1, SK Saha2*

Cyanobacteria are mostly autotrophic in their mode of nutrition, but there are some heterotrophic forms also. They grow as free-floating, colonial as well as endosymbionts with higher plants. Cyanobacteria inhabit diverse ecological condi-tions from psychrophilic to thermo-philic, acidophilic to alkylophilic, epilithic to endolithic and freshwa-ter to halophilic . Cyanobacteria are found in a wide variety of habitats ranging from freshwater to oceans, soil to bare rocks, deserts to ice shelves and hot springs to Arctic and Antarctic lakes. They thrive in harsh environmental conditions, namely ultraviolet (UV) irradiance, photo-oxidation, drought and desicca-tion, nitrogen starvation , heat–cold shocks, anaerobiosis, osmotic and salinity stresses due to their unique survival strategies1,2.

Ultraviolet irradiation and bio-sunscreenCyanobacteria are naturally exposed to copious amounts of UV irradiation from the sun, their primary source of energy. A stratospheric ozone layer shields the Earth from penetration of UV irradiation (UV-A, 315–400 nm; UV-B, 280–315 nm; UV-C, 100–280 nm) and their harmful effects on cel-lular damaging. Ozone layer is con-tinuously depleting due to increasing use of anthropogenically released environmental hazards such as chlorofluorocarbons, chlorocarbons and organobromides. This is lead-ing to an increase in UV-A and UV-B exposure on the Earth3. UV-A is the most commonly penetrating type of UV light, while UV-B’s penetration is increasing due to reduction of ozone layers. UV-C cannot reach the Earth’s

AbstractIntroductionThere is a growing demand for the replacement of chemical sunscreens with bio-sunscreens. Production of bio-sunscreen alone requires an alternative source of ultraviolet-screening compounds than the exist ing wild source. At present, bio-sunscreen compounds are sourced from marine macroalgae containing mycosporine-like amino acids such as, palythine , porphyra-334 and shinorine . Importantly , cyanobacteria being the most successful prokaryotic photosynthetic organisms in various extreme environments can produce palythine, porphyra-334, shinorine and other types of mycosporine-like amino acids with multiple bio-functions . Some cyanobacteria additionally produce special type of pigments embedded within their extracellular sheaths for their cellular protection from ultraviolet light damage. Cyanobacteria can be cul-tivated in a sustainable manner for the production of desired ultraviolet-screening compounds using their photosynthetic machinery , meagre amounts of nutrients , sunlight or artificial lights; atmospheric or industrial waste CO2 and marine water . This alternative bio-facto-ry neither depends on the local weather nor supports un-sustainable harvesting of bio-materials from the wild. The tools required for

cyanobacterial genetic manipulations are well developed, and more than 50 cyanobacterial genome sequences are available in the public domain, which allows further genetic improvement of cyanobacteria through comparative gene distribution and synteny analysis . Therefore, cyanobacteria can be considered as novel alternative bio-factories for the production of ul-traviolet-screening compounds.

This review briefly discusses the types of ultraviolet-screening compounds of cyanobacteria and their usefulness as bio-factories for the production of alternative source of ultraviolet-screening compounds.ConclusionThe fact that the ability to cultivate cyanobacteria in a controlled in vitro environment with specific growth and induction requirements makes them ideal bio-factory for the production of ultraviolet-screening compounds. The extent of cyanobacterial potential must yet be manipulated by conventional and genetic manipulations, which require further scrutiny at a molecular level for efficient bio-synthesis of ultravio-let-screening compounds.

IntroductionCyanobacteria and their habitatsCyanobacteria are photosynthetic , ox-ygen-evolving prokaryotic organisms present on the Earth for approximatel 3.5 billion years. They are the origi-nal oxygenic photosynthetic organ-isms and are morphologically di-verse ranging from unicellular to multicellular (Figure 1) , coccoid to branched filaments , almost colour-less to variously pigmented. There are more than 150 genera and over 2000 species described so far.

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For citation purposes: Browne N, Donovan F, Murray P, Saha SK. Cyanobacteria as bio-factories for production of UV-screening compounds. OA Biotechnology 2014 Mar 12;3(1):6. Co

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absorption maxima from 310 to 365 nm. They are colourless, water soluble and composed of a cyclohex-enone or cyclohexenimine chromo-phore conjugated with a nitrogen substituent of an amino acid or its imino alcohol7. The differences be-tween absorption spectra of MAAs are due to variations in the attached side groups and their nitrogen sub-stituents. MAAs share a 5-hydroxy-5-hydroxymethyl-cyclohex-1,2-ene ring and have a methoxy substituent at the second carbon atom. They are always substituted at the third car-bon atom with an amino compound and at the first carbon atom with ei-ther an oxo or an imino moiety. Thus, the ring system of MAAs contains a glycine subunit at the third carbon atom. Certain MAAs may also contain sulphate esters or glycosidic linkages through the imine substituents (Fig-ure 2). A simple UV-visible spectra analysis of methanolic extracts can be adopted to screen cyanobacteria capable of producing UV-screening compounds and their possible chem-ical diversity (Figure 1). However, the most suitable methods for identifica-tion of MAAs require high-perfor-mance liquid chromatography- based characterisation of specific retention time, absorption maxima and their molecular masses8–10.

MAAs bio-synthesis is induced when cyanobacteria are exposed to UV-B irradiation9. Basic chromo-phores in MAAs responsible for the UV absorbance are possibly synthesised during the prelimi-nary stages of cyanobacterial shi-kimate pathway11. This pathway connects the carbohydrates me-tabolism to the bio-synthesis of aro-matic compounds 9. However, both the complete enzymatic pathway of MAAs bio-synthesis and their regu-lation by environmental conditions are not fully understood. The genes involved in MAA bio-synthesis in cyanobacterium Anabaena variabilis PCC 7937 are YP_324358 (pretdict-ed 3-dehydroquinate synthase) and

and/or UV-B region of the spectrum. These compounds play an impor-tant role supporting cyanobacterial growth and survival in habitats ex-posed to strong irradiation. MAAs and scytonemin are able to protect cyanobacterial cells through absorb-ing the harmful UV irradiation and dissipating the energy in a harmless form of heat radiation6.

Mycosporine-like amino acidsTo date, approximately 21 MAAs have been discovered in marine and freshwater organisms7, some of these MAAs were also identified in cyanobacteria (Table 1). MAAs are low-molecular-weight compounds (<400 Da) of an amino alcohol with

surface as of yet as it is absorbed completely in the atmosphere. Of the types of UV lights, UV-B is the most detrimental because it has enough energy to cause photochemi-cal damage to cellular nucleic acids and proteins. Cyanobacteria evolved on Earth when the ozone shield was absent . They presumably faced co-pious exposure to UV irradiation while surviving due to their screen-ing mechanisms4. To counteract UV exposure, cyanobacteria have de-veloped evolutionary mechanisms, such as the synthesis of UV-screening compounds namely mycosporine-like amino acids (MAAs) and scy-tonemin5. These bio-sunscreen com-pounds strongly absorb in the UV-A

Figure 1: Morphological and bio-chemical variations of Irish cyanobacteria. Right panel shows corresponding absorption spectra of methanolic extracts of (a) Chlorogloea microcystoides, (b) Calothrix crustacea, (c) Lyngbya majuscula (d) and Nostoc commune.

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For citation purposes: Browne N, Donovan F, Murray P, Saha SK. Cyanobacteria as bio-factories for production of UV-screening compounds. OA Biotechnology 2014 Mar 12;3(1):6. Co

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YP_324357 (o-methyltransferase). The products of the above two genes are involved in the bio-synthesis of the common core (deoxygadusol) of all MAAs12. Another study with the gene NpF5557 of Nostoc punctiforme suggested that cyanobacteria pos-sess at least two distinct pathways for the bio-synthesis of bi-substitut-ed mycosporines5.

ScytoneminScytonemin represents a yellow-brown, low-molecular-weight (544 Da), lipid-soluble pigment of the cy-anobacterial sheath with an absorp-tion maximum of 384 nm. Production of scytonemin in certain cyanobacte-ria is believed to be the earliest de-veloped mechanism of UV protection, more ancient than the flavonoids or melanins13. Purified scytonemin has a maximum UV absorption at 384 ± 2 nm, although it can also absorb at 252, 278 and 300 nm14. Scytonemin was first reported by Nägeli in 1849 in some terrestrial cyanobacteria and later termed scytonemin15. Its structure constituting indolic and

Table 1 List of cyanobacterial MAAs with their specific absorption maximaCyanobacteria Type of MAAs l-max (nm) Specific growth conditions References

Synechocystis sp. PCC 6803

Mycosporine—taurine 309 UV-A and B26M-343 343 UV-A

Dehydroxylusujirene 356 UV-A

Anabaena doliolum

Mycosporine—glycine 310 PAR

27Porphyra-334334 UV-B

Shinorine

Anabaena variabilis PCC 7937Palythine—serine 320 Sulphur depletion

28Shinorine 334 PAR + UV-A and B

Nostoc communePalythine—threonine 322

Sunlight 10Porphyra-334 334

Euhalothece sp.Mycosporine-2-glycine 331 UV-A

29Euhalothece-362 362 UV-A

Trichodesmium sp.Asterina-330 332 UV-A

30Palythene 360 UV-A

MAA, mycosporine like-amino acids; PAR, photosynthetically active radiation; UV, ultraviolet.

phenolic subunits was determined in 199316. Scytonemin is redox sensitive by changing from a greenish brown (when oxidised) to a red (reduced) form16. It duced) form16. It is usually found in duced) form16. It is usually found in the oxidised form; however, the redox form depends on the acid–base conditions during the process of extraction17. Scytonemin is thought to be synthesised from the metabolites of aromatic amino acid bio-synthesis and can be induced by high photon fluence rate17. Scytonemin bio-syn-thesis was also reported to induce in response to UV-A irradiation; high temperature; photo-oxidative stress; deficiency of specific elements such as Fe, Mg or N2; high light intensity and periodic desiccation stress17–21. This pigment is excreted and depos-ited in the extracellular sheaths of some cyanobacteria. Scytonemin is thought to carry out screening ac-tivity without any further metabolic investment even after prolonged physiological inactivity (e.g. desicca-tion). Scytonemin-producing cyano-bacteria are typically found in the

upper layers of microbial mat com-munities, which are exposed to high levels of solar irradiance22,23. Thus, the extracellular pigment scytone-min is thought to have a protective role against harmful UV irradiation, allowing organisms to adapt to harsh habitats. Scytonemin also possesses anti-inflammatory and anti-prolifer-ative properties in addition to its UV-screening properties (see review)13.

A milestone study with cyanobac-terium N. punctiforme ATCC 29133 (PCC 73102) led to the understand-ing of scytonemin bio-synthesis at a molecular level. In this study, a trans-poson mutagenesis using Tn5-1063a (transposon with antibiotic resist-ance marker) yielded a scytonemin-less Nostoc mutant strain that did not produce scytonemin under UV irradiation. This was the only pheno-typic difference of this mutant strain compared with the wild type. The above mutation was traced to open reading frame (ORF) NpR1273 (now known as scyD), which is a part of a gene cluster of 18 contiguous ORFs (NpR1276 to NpR1259)21. These

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For citation purposes: Browne N, Donovan F, Murray P, Saha SK. Cyanobacteria as bio-factories for production of UV-screening compounds. OA Biotechnology 2014 Mar 12;3(1):6. Co

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cyanobacteria have higher growth rates compared with macroalgae and can be cultivated photoautotrophi-cally in outdoor raceway or circular ponds and in in-door photobioreac-tors under an optimised controlled environment. The cyanobacterial production system can be based on non-arable land because of their abil-ity to thrive in areas that cannot sup-port agriculture; moreover, cyano-bacteria can be cultivated throughout the year without depending on local weather adopting in-door cultivation systems. Photoautotrophic cultiva-tion of cyanobacteria requires only marginal amounts of nutrients sup-plied as inorganic chemicals, organic matters or wastewater; sunlight or artificial lights; atmospheric or in-dustrial waste CO2 and non-potable water (brackish or marine water). Further, the genetic tools for cyano-bacterial strain improvement are well established and more than 50 cyano-bacteria genome sequences are avail-able online. The available genome sequences allow comparisons of gene distribution and synteny among vari-ous cyanobacteria strains as well as close relatives for their genetic opti-misations. Therefore, selected cyano-bacteria can be further optimised to produce commercially important UV-screening compounds at industrial scales by developing cheaper and sustainable cultivation systems using available raw materials.

Approaches for exploration of cyanobacteriaCyanobacterial cultivation can be based on utilisation of free solar en-ergy (open cultivation systems) or utilisation of artificial (photosynthet-ically active radiation) lights (closed photobioreactors) for sustainable production of UV-screening com-pounds. Minimal nutrients require-ment for their growth can be sup-plied as chemical or organic nutrients and to enhance their dense bio-mass yield, use of industrial waste CO2 within the bio-refinery concept is an

of sunscreen for the protection from sun-burn injuries. The aim of this review was to discuss cyanobacteria as bio-factories for production of UV-screening compounds.

DiscussionThe authors have referenced some of their own studies in this review. The protocols of these studies have been approved by the relevant ethics com-mittees related to the institution in which they were performed.

Why cyanobacteria for ultraviolet-screening compoundsAt present, bio-sunscreens are mainly sourced from marine macroalgae that are harvested from the wild, and their bio-mass with specific bio-active con-tent may vary seasonally. However,

gene clusters are co-transcribed as a single transcriptional unit and their expressions are induced by UV-A exposure. These gene products are associated with the bio-synthesis of scytonemin: (i) as assembly of scy-tonemin, (ii) production of first two enzymes of shikimic acid pathway (AroG and AroB), (iii) production of first enzyme of tyrosine bio-synthe-sis (TyrA) and (iv) production of all five enzymes of tryptophan bio-syn-thetic pathway (TrpECABD)24. Thus, it was thought that the entire down-stream region scyD of the N. puncti-forme is dedicated to the delivery of monomeric blocks for scytonemin synthesis. Exposure to sun is a pri-mary factor for skin cancer and pho-toageing25. There is a growing con-cern and dramatic increase in the use

Figure 2: Chemical structures of various mycosporine like–amino acids found in cyanobacteria.

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Thus, their complete potential is not explored, which needs integrated re-search and development projects to reduce production cost. Cyanobac-teria cultivation in open race-way ponds is effective for free solar en-ergy harvest, but there are several biological threats of contamination with other algae, algae grazers, fungi and amoeba, rotifers, etc. Further, lo-cal weather fluctuations including light, temperature and rain may in-fluence cultivation efficiency. There-fore, cultivation in closed photobio-reactors could be the best alternative for nutritional quality bio-mass or value-added bio-molecule produc-tion throughout the year irrespective of local weather. Large-scale cultiva-tion in tubular, flat plate or other de-signs of closed photobioreactors are expensive. Overheating and fouling in closed photobioreactors are also ma-jor challenges. The present harvest-ing technologies such as filtration, centrifugation or rolling belt are ex-pensive for large-scale cyanobacteri-al bio-mass harvesting, which needs optimisation and cheaper technology. Bio-flocculation is the process used for several-folds concentration of cul-tured bio-mass prior to downstream processing. This process could be the simplest and cost-effective method. However, bio-flocculation for all cy-anobacteria is not universal and needs optimisation possibly by mini-mum use of chemical flocculants.

ConclusionSunscreen use has noticeably in-creased due to growing concern that sun exposure is a primary fac-tor of skin cancer and photoageing. Cyanobacteria can step up the mark to fulfil the global demand for bio-sunscreens by replacing the use of chemical-based sunscreens. Cyano-bacteria bio-synthesise UV-screen-ing compounds such as MAAs and scytonemin, which protect them in harsh habitats. Cyanobacteria of-fer several advantages over the cur-rent macroalgae (alternative source

The spent bio-mass thus obtained can have applications as bio-fertiliser or in bio-energy generation within the bio-refinery concept (Figure 3).

Challenges for exploration of cyanobacteriaFew cyanobacteria namely Spirulina platensis, Arthrospira maxima and Aphanizomenon flos-aquae have been cultivating photoautotrophically as outdoor cultures for health supple-ment products, however mostly not based on the bio-refinery concept.

ideal situation. Once, active growth is obtained at desired cell density, cyanobacterial cells can be starved for specific nutrients and/or UV ir-radiation for induction of specific UV-screening compounds. Then, the bio-mass would be ready for harvesting and extraction of UV-screening com-pounds. Depending on the nature of compounds, specific extraction pro-tocol has to be adopted, for example, MAAs can be extracted by aqueous methanol and scytonemin with or-ganic solvent or supercritical CO2.

Figure 3: Schematic diagram showing cyanobacterial bio-factory for ultra-violet-screening compounds production within bio-refinery concept. UV, ultraviolet; MAAs, mycosporine-like amino acids.

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For citation purposes: Browne N, Donovan F, Murray P, Saha SK. Cyanobacteria as bio-factories for production of UV-screening compounds. OA Biotechnology 2014 Mar 12;3(1):6. Co

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17. Garcia-Pichel F, Castenholz RW. Char-acterisation and biological implications of scytonemin, a cyanobacterial sheath pigment. J Phycol. 1991 Jun;27(3):395–409.18. Dillon JG, Tatsumi CM, Tandingan PG, Castenholz RW. Effect of environmental factors on the synthesis of scytonemin, a UV-screening pigment, in a cyanobac-terium (Chroococcidiopsis sp.). Arch Mi-crobiol. 2002 Apr;177(4):322–31.19. Fleming ED, Castenholz RW. Effects of periodic desiccation on the synthesis of the UV-screening compound, scytone-min in cyanobacteria. Environ Microbiol. 2007 Jun;9(6):1448–55.20. Fleming ED, Castenholz RW. Effects of nitrogen source on the synthesis of the UV-screening compound, scytonemin, in the cyanobacterium Nostoc punctiforme PCC 73102. FEMS Microbiol Ecol. 2008 Mar; 63(3):301–8.21. Soule T, Stout V, Swingley WD, Meeks JC, Garcia-Pichel F. Molecular genet-ics and genomic analysis of scytonemin biosynthesis in Nostoc punctiforme ATCC 29133. J Bacteriol. 2007 Jun;189(12):4465–72.22. Balskus EP, Case RJ, Walsh CT. The biosynthesis of cyanobacterial sunscreen scytonemin in intertidal microbial mat communities. FEMS Microbiol Ecol. 2011 Aug;77(2):322–32.23. Büdel B, Karsten U, Garcia-Pichel F. Ultraviolet-absorbing scytonemin and mycosporine-like amino acid derivatives in exposed, rock-inhabiting cyanobacte-rial lichens. Oecologia. 1997 Oct;112(2): 165–72.24. Soule T, Garcia-Pichel F, Stout V. Gene expression patterns associated with the biosynthesis of the sunscreen scytone-min in Nostoc punctiforme ATCC 29133 in response to UVA radiation. J Bacteriol. 2009 Jul;191(14):4639–46.25. Maier T, Korting HC. Sunscreens–which and what for? Skin Pharmacol Physiol. 2005 Nov–Dec;18(6):253–62.26. Zhang L, Li L, Wu Q. Protective effects of mycosporine-like amino acids of Syn-echocystis sp. PCC 6803 and their partial characterization. J Photochem Photobiol B: Biology. 2007 Mar;86(3):240–5.27. Singh SP, Sinha RP, Kilsch M, Häder DP. Mycosporine-like amino acids (MAAs) profile of a rice-field cyanobacterium Anabaena doliolum as influenced by PAR and UVR. Planta. 2008 Dec;229(1): 225–33.

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for bio-sunscreen compounds) such as eliminating the need to harvest from the wild and their ability to be cultivated sustainably. The fact that the ability to cultivate cyanobacteria in a controlled in vitro environment with specific growth and induction requirements makes them ideal bio-factory for the production of UV-screening compounds. The extent of cyanobacterial potential must yet be manipulated by conventional and genetic manipulations, which re-quire further scrutiny at a molecular level for efficient bio-synthesis of UV-screening compounds.

Abbreviations listMAAs, mycosporine-like amino ac-ids; ORF, open reading frame; UV, ultraviolet.

AcknowledgementNorma Browne thanks the Irish Re-search Council, Government of Ire-land for the postgraduate scholarship (Project ID GOIPG/2013/32). Fiona Donovan acknowledges the receipt of GRO Masters Bursary 2012 from Limerick Institute of Technology.

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Licensee OA Publishing London 2014. Creative Commons Attribution License (CC-BY)

For citation purposes: Browne N, Donovan F, Murray P, Saha SK. Cyanobacteria as bio-factories for production of UV-screening compounds. OA Biotechnology 2014 Mar 12;3(1):6. Co

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30. Subramaniam A, Carpenter EJ, Karentz D, Falkowski PG. Biooptical properties of the marine diazotrophic cyanobacteria Trichodesmium spp. I. Ab-sorption and photosynthetic action spec-tra. Limnol Oceanogr. 1999 Jan;44(3): 608–17.

29. Kedar L, Kashman Y, Oren A. My-cosporine-2-glycine is the major my-cosporine-like amino acid in a unicellular cyanobacterium (Euhalothece sp.) isolat-ed from a gypsum crust in a hypersaline saltern pond. FEMS Microbiol Lett. 2002 Mar;208(2):233–7.

28. Singh SP, Kilsch M, Sinha RP, Häder DP. Sulfur deficiency changes mycosporine-like amino acid (MAA) composition of Anabaena variabilis PCC 7937: a pos-sible role of sulphur in MAA bioconver-sion. Photochem Photobiol. 2010 Jul–Aug;86(4):862–70.