Biotechnol Lett DOI 10.1007/s10529-014-1726-8

ORIGINAL RESEARCH PAPER

Melanin: a photoprotection for Bacillus thuringiensis based biopesticides Estibaliz Sansinenea • Aurelio Ortiz

Received: 26 September 2014 / Accepted: 30 October 2014 Ó Springer Science+Business Media Dordrecht 2014

Abstract Melanins are negatively-charged, hydrophobic, dark high molecular weight irregular biopolymers, composed of polymerized phenolic and/or indolic compounds. They are produced by most organisms. Bacillus thuringiensis is a Gram-positive, spore-forming, soil bacterium and the most successful biological control agent that produces distinctly shaped crystals during sporulation that have insecticidal activity. However, one of the main disadvantages is that the insecticidal activity of B. thuringiensis formulation is unstable and rapidly loses its activity under field conditions due to UV radiation. Melanin absorbs radiation; therefore photoprotection of B. thuringiensis based on melanin has been studied and is herewith reviewed. Keywords Bacillus thuringiensis  Biopesticides  Melanin  Photoprotection

Introduction: Bacillus thuringiensis use versus sunlight degradation Bacillus thuringiensis is a Gram-positive, sporeforming, soil bacterium and the most successful

E. Sansinenea (&)  A. Ortiz Facultad de Ciencias Quı´micas de la Beneme´rita Universidad Auto´noma de Puebla, 72570 Puebla, Pue, Mexico e-mail: [email protected]

biological control agent. It produces distinctly shaped crystals during sporulation. These crystals are composed of proteins known as insecticidal crystal proteins (ICPs or Cry proteins), which are selectively toxic to different species of several invertebrate phyla. Numerous Cry protein genes (called cry genes) have been classified into groups (http://epunix.biols.susx. ac.uk/Home/Neil_Crickmore/Bt/). During sporulation, Cry proteins accumulate as crystalline inclusions within the cell. These crystals, when ingested by susceptible insects, are dissolved releasing monomers of the Cry proteins, followed by the proteolytic processing of the protoxin by midgut proteases, releasing the Cry toxin in its active form. The active toxin binds to specific receptors on the apical brush border of the midgut microvilli of susceptible insects causing lysis of midgut epithelial cells and death of insect larvae. It affects a selective range of insect orders, namely, lepidoptera, diptera and coleoptera (George and Crickmore 2012). Bacillus thuringiensis, therefore, has been used as a biopesticide in agriculture, forestry and mosquito control and today it is the most widely used biopesticide in the world (Sansinenea 2012). Because of their mode of action with a high specificity, microbial pesticides derived from B. thuringiensis present many advantages such as safety for non-target organisms, high specificity, low development of pest resistance and low environmental pollution. However, one of its main disadvantages is that the insecticidal activity of B. thuringiensis formulation is relatively unstable and

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rapidly loses its biological activity under field conditions due to the ultraviolet (UV) radiation in sunlight (Sansinenea 2012). Therefore, its use is expensive because repeated spraying is necessary. Ever since the entry of first commercial product of B. thuringiensis named ‘‘Sporeine’’ in France in 1938, there has been continuous rise in development of advanced products (Aronson et al. 1986). The problems of stability of biopesticides both during storage and after application have stalled biopesticide development (Brar et al. 2006). For this purpose, formulation development can play a key role addressing four major objectives which can serve as benchmarks for success: (1) stabilize microbial agents during distribution and storage; (2) aid handling and application of the product; (3) protect agent from adverse environmental factors; (4) enhance activity of microbial agents in field. Commercial biopesticides must be economical to produce, have persistent storage stability, high residual activity, be easy to handle, mix, and apply, and provide consistently effective control of the target pest (Brar et al. 2006). Attempts to protect B. thuringiensis toxicity from damaging UV radiation, under field conditions, have had limited success. Different formulations were developed with addition of variety of screens (Cohen et al. 2001; Brar et al. 2006). However, some of these screens have a negative impact on the environment. The spores of B. thuringiensis are susceptible to solar radiation. This phenomenon can be attributed to the fact that sunlight is composed of UV-B (between 290 and 320 nm), UV-A (320–390 nm), visible (between 390 and 780 nm), and infrared radiation ([780 nm). Natural sunlight, especially the UV radiation portion of the spectrum, UV-B and UV-A, is mainly responsible for inactivation of insect pathogens by directly damaging DNA (e.g. pyrimidine dimers, cross-linking with proteins) or by producing reactive oxygenderived free radicals. Chromophores (exogenous, possibly endogenous too) derived from fermentation media which, after cell lysis, may be adsorbed onto B. thuringiensis crystal proteins (Pusztai et al. 1991; Cohen et al. 1991; Ignoffo 1992). These chromophores, absorbing at 300–380 nm, so far uncharacterized, pass excited, electronic-state energy to O2 and, in turn, convert it to the highly-reactive singlet or free radical state. In this state, the singlet oxygen attacks indole side chains of tryptophan residues on the toxin protein resulting in loss of insecticidal activity. Cohen

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et al. (1991) suggested the use of cationic moieties, such as acriflavin and rhodamine B, to transfer energy from excited tryptophan and act as a UV radiation blocker. Resistance to UV of Bacillus spores (Nicholson et al. 2000) is caused by altered conformation of DNA, high concentrations of small acid-soluble proteins (Cucchi and Sanchez de Rivas 1998) and low concentrations of dipicolinic acid (Nicholson et al. 2000). In addition, abundance of plasmids, surfacelocalized Cry protoxins, and UV-induction of bacteriophage may increase susceptibility to UV of B. thuringiensis spores (Benoit et al. 1990; Du and Nickerson 1996; Inal et al. 1990). In this sense, we have reviewed a number of topics about melanin, focusing primarily on melanin as a photoprotector in B. thuringiensis-based biopesticides.

General features of melanin Melanins are dark brown-black pigments that are widespread in a variety of organisms ranging from humans to bacteria, including Escherichia coli W3110 (Lagunas-Mun˜oz et al. 2006), Bacillus cereus (Zhang et al. 2007) and Klebsiella sp. GSK (Sajjan et al. 2010), Pseudomonas aeruginosa (Rodriguez-Rojas et al. 2009), Pseudomonas stutzeri (Kumar et al. 2013), B. thuringiensis (Aghajanyan et al. 2005), Aeromonas media (Wan et al. 2007) and Vibrio cholerae (Ivins and Holmes 1980). Fungal species that synthesize melanin include Cryptococcus neoformans, Aspergillus fumigatus, and Pneumocystis carinii (Plonka and Grabacka 2006). Melanins can be obtained by chemical (Pawelek et al. 1993) and microbiological synthesis (Plonka and Grabacka 2006) or by extraction from animal or plant tissues (Prota 1992). One of the major problems in studying melanins is the lack of adequate methods for the isolation of pure melanin pigments. Remarkably little is known about the structures of melanins despite their abundance in the global biomass. This is due to the inability of current biochemical and biophysical techniques to provide a definitive chemical structure, because these complex polymers are amorphous, insoluble, and not amenable to either solution or crystallographic structural studies. Characteristically, melanins are insoluble in aqueous or organic solvents, resistant to concentrated acid

Biotechnol Lett Fig. 1 Chemical structures of pheomelanin, eumelanin neuromelanin and pyomelanin oligomers

OH

H N

O

OH N

S HO O

NH2 HO

O

O OH

S N

N O

OH

S

O

O HO

N H

HO

N H

O

O O H2N Pheomelanin

O

OH

OH

OH O

N H

OH

OH Eumelanin CO2H

OH O N OH H 5,6-dihydroxyindole, monomer of neuromelanin polymers

and susceptible to bleaching by oxidizing agents (Prota 1992; Butler and Day 1998). Methods for partial chemical degradation of melanin followed by HPLC analysis have been developed and are useful for the characterization of specific types of melanin (Wakamatsu and Ito 2002; Wakamatsu et al. 2002). Melanins (see Fig. 1) are classified as: allomelanin (allo) present in plants and fungi; neuromelanin (neu) present in neural cells; pheomelanin (pheo) and eumelanin (eu) that are found in the skin, hair and iris. Melanins generated from L-3,4-dihydroxyphenylalanine (L-DOPA) by phenoloxidases are referred to as eumelanins. They are generally black or brown. Yellow or reddish melanins are called pheomelanins and incorporate cysteine within the L-DOPA. Brownish melanins are derived from homogentisic acid by tyrosinases and are called pyomelanins. Melanins formed from acetate, via the polyketide synthase pathway, are typically black or brown and are referred to as dihydroxynaphthalene melanins (Plonka and Grabacka 2006). The synthesis of melanin in microorganisms has functions other than UV protection. Melanin production in micro-organisms is often associated with numerous survival mechanisms and can serve as energy transducers and affect cellular integrity.

O Benzoquinoacetate monomer of pyomelanin

Melanin is also used for sexual display and camouflage. Melanin plays a major role in the innate immune system of insects, which synthesize the polymer to damage microbial intruders (Nappi and Christensen 2005). Bacterial melanin accelerates motor recovery after lesions in the central nervous system (Manvelyan et al. 2008; Petrosyan 2013). But the major role of the melanin is that to confer resistance to UV by absorbing a broad range of the electromagnetic spectrum and preventing photoinduced damage. Melanin has, therefore, been commercially used in photoprotective creams and eye glasses and at the same time protects several bacterial species from UV radiation (Nosanchuk and Casadevall 2003), such as B. thuringiensis (Salazar et al. 2014).

Melanin synthesis In mammals, melanin synthesis is catalyzed by a tyrosinase. Melanin synthesis begins in the liver where phenylalanine is converted to tyrosine by the action of phenylalanine hydroxylase. The oxidation of L-tyrosine to 3,4-dihydroxyphenylalanine (L-DOPA) is then catalyzed by the action of tyrosinase enzymes within the melanocyte’s melanosome. In the next step, L-DOPA is

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CO2H

Tyrosinase HO

NH2

HO

CO2H Tyrosinase NH2

HO

Tyrosine

O

CO2H NH2

O

L-DOPAquinone

L-DOPA HO

Cystein Gluthatione

CO2H N H LeucoDOPAchrome HO

HO

CO2H NH2

HO S HO

O CO2H

N H 5,6-Dihydroxyindole HO

HO

Tyrosine related protein 2(TRP2)

Tyrosinase O

N H DOPAchrome

N H Indole-5,6-quinone

HO

CO2H NH2

S CO2H N 1,4-benzothiazinyl-alanine HO H 5,6-Dihydroxyindole2-carboxylic acid (DHICA) Tyrosine related protein 1(TRP1)

HO

O

HO O

CO2H N O H Indole-5,6-quinonecarboxylic acid

NH NH

CO2H

CysteinylDOPA

N

HO

O

H2N

OH N

O

NH2 CO2H CO2H

S S

NH2

N OH

Eumelanin

Pheomelanin

Fig. 2 Melanin synthesis pathway

oxidized to DOPAquinone. From DOPAquinone, the melanin synthesis pathways diverge to produce either eumelanin or pheomelanin (Fig. 2).

Finally, the oxidation of 5,6-dihydroxyindole to indole5,6-quinone by tyrosinase leads to the formation of eumelanin (brown-black pigment).

Eumelanin

Pheomelanin

Firstly, DOPAquinone is converted to leucoDOPAchrome and then to DOPAchrome through auto-oxidation, and subsequently, in the presence of DOPAchrome tautomerase and dihydroxyindole-2-carboxylic acid oxidase, DOPAchrome is converted to 5,6-dihydroxyindole.

In the presence of cysteine or glutathione, dopaquinone is converted to cysteinyl DOPA Subsequently, pheomelanin, a yellow–red pigment, is formed through the oxidative polymerization of cysteinyldopa via 1,4benzothiazinylalanine intermediates.

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Oxidative polymerization of phenolic compounds, such as catechol and 1,8-dihydroxynaphthalene (allomelanins), DOPA (eumelanins) and cysteinyl-DOPA (pheomelanins), leads to the formation of brown-black pigments called melanins (Butler and Day 1998). In contrast, microbes generally synthesize melanin via various phenoloxidases (such as tyrosinases, laccases, or catacholases) and/or the polyketide synthase pathway (Wheeler and Bell 1988). The amino acids, L-tyrosine, L-phenylalanine and Lcysteine, are precursors of melanins. L-Tyrosine is the precursor of L-DOPA in the B. thuringiensis mutant MB24 as it enhanced the level of melanin production whereas arginine:HCl blocked the formation of melanin, indicating the involvement of a similar kind of enzyme in its production (Hoti and Balaraman 1993). Melanin synthesis in bacteria is mainly catalyzed by tyrosinase or laccase (Kong et al. 2000; CastroSowinski et al. 2002). Tyrosinase (monophenol monooxygenase EC 1.14.18.1) catalyzes the ohydroxylation of L-tyrosine to L-dihydroxy phenylalanine (hydroxy activity), as well as, oxidation of Ldihydroxy phenylalanine to L-dopaquinone (oxidase activity) (Fairhead and Tho¨ny-Meyer 2012). The Ldopaquinone is oxidized to form melanin, which has antioxidant, antiviral activity and protective effect against the damage caused by ultraviolet radiation (Fairhead and Tho¨ny-Meyer 2012). A number of tyrosinase inhibitors from both natural and synthetic sources have been identified. A tyrosinase inhibitor, such as a melanogenesis inhibitor, whose action mainly resides in some interference in melanin formation, may act regardless of any direct inhibitor/enzyme interaction. Many putative inhibitors have been examined in the presence of tyrosine or LDOPA as the enzyme substrate, and activity is assessed in terms of dopachrome formation. There are six compounds which are classified as tyrosinase inhibitors; however, there is a controversy about this classification as revised by Chang (2009). Tyrosinase, a copper-containing enzyme, is widely distributed in mammals, plants and micro-organisms. In microorganisms, the tyrosinase from two fungi, Agaricus bisporus and Neurospora crassa, have been investigated most extensively from both structural and functional points of view. The activities of tyrosinase from various organisms (most studies use the commercially available mushroom tyrosinase) have been used in several different biotechnological applications (Halaouli et al. 2006).

One potentially important use for tyrosinase is the production of the drug L-DOPA. L-DOPA is a useful drug in the treatment of Parkinson’s disease but the production of it directly from L-tyrosine by using tyrosinase is not necessarily straightforward (Fairhead and Tho¨ny-Meyer 2012). As was mentioned above, tyrosinase is active towards a wide range of phenols. Thus, it is perhaps not surprising that it has been proposed for removing such toxic compounds from the environment. The activation of such a wide range of substrates by tyrosinase could be advantageous in a biosensor setting as the enzyme is capable of oxidizing many different molecules. Melanin is an unusual compound that absorbs a broad spectrum of electromagnetic radiation from visible light to ionizing radiation. In addition, metal ions, sound and free radicals have also been proposed to have a role in bacterial electron transfer. Thus, melanin has several interesting properties that may make it of use in biotechnology. However, melanin is also important in the pathogenicity of several bacterial species and inhibitors towards tyrosinase that prevent melanin production are therefore also of interest. Melanin formation by tyrosinase can also be used as a convenient proxy marker for various bacterial activities. Such activity has been used to develop a highthroughput screen for high L-tyrosine producing strains of E. coli. Conversely, melanin production and tyrosinase activity of some species of soil bacteria, (e.g. Azospirillum and Rhizobium sp.) play a role in their symbiotic relationship with plants. Another interesting application of the ability of tyrosinase to produce melanin is in the development of the biopesticide B. thuringiensis (Fairhead and Tho¨ny-Meyer 2012).

Melanin: the solution for preparation of lightstable biopesticides Melanin absorbs radiation; consequently, photoprotection of B. thuringiensis based on melanin has been studied. Various organic compounds, such as benzaldehyde, cinnamaldehyde, salicylaldehyde, Methylene Blue and yeast extract, when employed as sunscreens for Lysinibacillus sphaericus showed elimination of larvicidal activity after 12 h of UV irradiation (C¸o¨kmu¨s et al. 2002). However, some of these UV screens have

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negative impacts on the environment. Spores of B. subtilis are susceptible to solar radiation as well as to UV at 254 nm (major peak of UV-C). When the efficacy of melanin for the protection of mosquito larvicidal activity of B. thuringiensis against UV radiation was studied, the bioassays confirmed an important role of melanin as a photoprotective agent (Liu et al. 1993). Liu et al. (1993) succeeded in protecting mosquitocidal activity of B. thuringiensis subsp. israelensis from UV radiation by melanin isolated from Streptomycetes lividans. This method eliminated the use of an external UV protectant and resulted in stable and safe formulations. Wan et al. (2007) reported the isolation of a novel A. media strain from large-scale screening for melanin producers that produces high levels of melanin. The pigment produced by this bacterium efficiently protected the insecticidal activity of B. thuringiensis subsp. israelensis, a commercial bioinsecticide, against both UV and natural solar radiation. Several research groups have obtained Bt mutants producing melanin. Jones et al. (1991) reported efficient isolation of mutants of B. thuringiensis by successive rounds of UV irradiation. These mutants had increased resistance to UV as well as, increased toxicity. Patel et al. (1996) isolated a mutant, B. thuringiensis M-8, by UV irradiation, which produced a dark-brown pigment, characterized as melanin, the natural UV photoprotector. This mutant had an increased UV resistance. Saxena et al. (2002) described another B. thuringiensis mutant producing melanin following successive rounds of UV irradiation. Although, these mutants were more resistant to UV irradiation, some of them lost their toxin-encoding genes. Hoti and Balaraman (1993) obtained a mutant of B. thuringiensis producing a dark-brown pigment, identified as melanin, by chemical mutagenesis. VilasBoˆas et al. (2005) described a pigment-producing mutant of B. thuringiensis subsp. thuringiensis 407 utilizing the mutagenic agent ethyl methane-sulfonate. They characterized the pigment as melanin. Ruan et al. (2004) found that most B. thuringiensis strains have the potential to produce melanin in the presence of L-tyrosine at an elevated temperature. However, at this temperature insecticidal Cry proteins could not be synthesized so genetic engineering was needed to produce insecticidal proteins in

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acrystalliferous Bt mutant producing melanin strains (Liu et al. 2013). Expression of the mel gene from P. maltophilia in B. thuringiensis confers UV protection to the host strain (Ruan et al. 2002). Another strategy is the obtaining of wild type of B. thuringiensis strains that naturally produce melanin. Chen et al. (2004) reported a wild strain of B. thuringiensis subsp. dendrolimus L-7601 producing melanin without the addition of tyrosine or an analogue. This had UV resistance and low toxicity to insects. Salazar et al. (2014) reported a wild type strain of B. thuringiensis naturally producing melanin and Cry proteins with UV resistance and antagonistic effect over some common bacteria of the environment such as Micrococcus luteus, Staphylococcus aureus, Klebsiella pneumoniae and Serratia marcescens.

Conclusions and perspectives Melanins are enigmatic pigments that are widespread in organisms ranging from bacteria to humans. The most noteworthy function of melanins is to act as a photoprotector against radiation, especially in the UV region of the spectrum (Nosanchuk and Casadevall 2003). Melanin is thought to filter out UV radiation and scavenges reactive oxygen species and, consequently, reduces UV damage in vivo (Wan et al. 2007). Bioinsecticides that control the growth of insect larvae are generally made by B. thuringiensis (Sansinenea 2012). Although temperature, humidity and air composition have some influence on the usage of bioinsecticides, the major loss of toxicity in the fields is because of exposure to UV radiation (Pusztai et al. 1991). Numerous attempts have been made to develop protection for bioinsecticides against damaging UV radiation under field conditions, such as chemical UV screens. The environmental consequences of these approaches remain to be evaluated. Being environmentally friendly, melanin has been considered as an effective photoprotective agent for bioinsecticides. Several research groups have obtained B. thuringiensis mutants producing melanin by successive rounds of UV radiation or by after treatment with the mutagenic agent. Although, these mutants were more resistant to UV radiation, some had lost their toxinencoding genes. Some researchers have obtained B.

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thuringiensis mutants producing melanin following high temperature induction in the presence of Ltyrosine. However, at this temperature insecticidal Cry proteins were not be synthesized so genetic engineering is needed to produce insecticidal proteins in acrystalliferous B. thuringiensis mutant producing melanin strains. The wild strains with melanin producing capacity are another alternative. We hope that this review will be useful for the search of new strategies to protect the biopesticides for the use of them in the field. Acknowledgments support.

We thank VIEP (project) for financial

References Aghajanyan A, Hambardzumyan A, Hovsepyan A, Asaturian R, Vardanyan A, Saghiyan A (2005) Isolation, purification and physicochemical characterization of water-soluble Bacillus thuringiensis melanin. Pigment Cell Res 18:130–135 Aronson A, Beckman W, Dunn P (1986) Bacillus thuringiensis and related insect pathogens. Microbiol Rev 50:1–24 Benoit TG, Wilson GR, Bull DL, Aronson AI (1990) Plasmid associated sensitivity of Bacillus thuringiensis to UV light. Appl Environ Microbiol 56:2282–2286 Brar SK, Verma M, Tyagi RD, Vale´ro JR (2006) Recent advances in downstream processing and formulations of Bacillus thuringiensis based biopesticides. Process Biochem 41:323–342 Butler MJ, Day AW (1998) Fungal melanins: a review. Can J Microbiol 44:1115–1136 Castro-Sowinski S, Martinez-Drets G, Okon Y (2002) Laccase activity in melanin-producing strains of Sinorhizobium meliloti. FEMS Microbiol Lett 209:119–125 Chang T-S (2009) An updated review of tyrosinase inhibitors. Int J Mol Sci 10:2440–2475 Chen Y, Deng Y, Wang J, Cai J, Ren G (2004) Characterization of melanin produced by a wild-type strain of Bacillus thuringiensis. J Gen Appl Microbiol 50:183–188 Cohen E, Rozen H, Joseph T, Braun S, Margulies L (1991) Photoprotection of Bacillus thuringiensis var. kurstaki from ultraviolet irradiation. J Invertebr Pathol 57:343–351 Cohen E, Joseph T, Wassermann-Golan M (2001) Photostabilization of biocontrol agents by berberine. Int J Pest Manage 47:63–67 ¨ , Berber ´I C¸o¨kmu¨s C, Sayar AH, Sac¸ilik SC, Osmanagaoglu O (2002) Effects of UV-light on Bacillus sphaericus and its protection by chemicals. J Basic Microbiol 40:215–221 Cucchi A, Sanchez de Rivas C (1998) SASP (small, acid-soluble spore proteins) and spore properties in Bacillus thuringiensis israelensis and Bacillus sphaericus. Curr Microbiol 36:220–225 Du C, Nickerson KW (1996) Bacillus thuringiensis HD-73 spores have surface-localized Cry1Ac toxin: physiological

and pathogenic consequences. Appl Environ Microbiol 62:3722–3726 Fairhead M, Tho¨ny-Meyer L (2012) Bacterial tyrosinases: old enzymes with new relevance to biotechnology. New Biotechnol 29:183–191 George Z, Crickmore N (2012) Bacillus thuringiensis applications in agriculture. In: Sansinenea E (ed) Bacillus thuringiensis biotechnology. Springer, Netherlands, pp 19–39 Halaouli S, Asther M, Sigoillot JC, Hamdi M, Lomascolo A (2006) Fungal tyrosinases: new prospects in molecular characteristics, bioengineering and biotechnological applications. J Appl Microbiol 100:219–232 Hoti SL, Balaraman K (1993) Formation of melanin pigment by a mutant of Bacillus thuringiensis H14. J Gen Microbiol 139:2365–2369 Ignoffo CM (1992) Environmental factors affecting persistence of entomopathogens. Fla Entomol 75:516–525 Inal JR, Karunakaran V, Burges HD (1990) Isolation and propagation of phages naturally associated with the |variety of Bacillus thuringiensis. J Appl Bacteriol 68:17–21 Ivins BE, Holmes RK (1980) Isolation and characterization of melanin-producing (mel) mutants of Vibrio cholera. Infect Immun 27:721–729 Jones DR, Karunakaran V, Burges HD, Hacking AJ (1991) Ultra-violet resistant mutations of Bacillus thuringiensis. J Appl Bacteriol 70:460–463 Kong K-H, Hong M-P, Choi S-S, Kim Y-T, Cho S-H (2000) Purification and characterization of a highly stable tyrosinase from Thermomicrobium roseum. Biotechnol Appl Biochem 31:113–118 Kumar CG, Sahu N, Reddy GN, Prasad RBN, Nagesh N, Kamal A (2013) Production of melanin pigment from Pseudomonas stutzeri isolated from red seaweed Hypnea musciformis. Lett Appl Microbiol 57:295–302 Lagunas-Mun˜oz VH, Cabrera-Valladares N, Bolı´var F, Gosset G, Martı´nez A (2006) Optimum melanin production using recombinant Escherichia coli. J Appl Microbiol 101: 1002–1008 Liu YT, Sui MJ, Ji DD, Wu IH, Chou CC, Chen CC (1993) Protection from ultraviolet irradiation by melanin of mosquitocidal activity of Bacillus thuringiensis var. israelensis. J Invertebr Pathol 62:131–136 Liu F, Yang W, Ruan L, Sun M (2013) A Bacillus thuringiensis host strain with high melanin production for preparation of light-stable biopesticides. Ann Microbiol 63:1131–1135 Manvelyan LR, Gevorkyan OV, Petrosyan TP (2008) Recovery of instrumental conditioned reflexes in rats after pyramidotomy and action of bacterial melanin. J Evol Biochem Physiol 44:316–321 Nappi AJ, Christensen BM (2005) Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity. Insect Biochem Mol Biol 35:443–459 Nicholson WL, Munakata N, Horneck G, Melosh HJ, Setlow P (2000) Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol Mol Biol Rev 64:548–572 Nosanchuk JD, Casadevall A (2003) The contribution of melanin to microbial pathogenesis. Cell Microbiol 5:203–223 Patel KR, Wyman JA, Patel KA, Burden BJ (1996) A mutant Bacillus thuringiensis producing a dark-brown pigment

123

Biotechnol Lett with increased UV resistance and insecticidal activity. J Invertebr Pathol 67:120–124 Pawelek J, Osber MP, Orlow SJ (1993) Synthetic melanin. US Patent 5 227 459 A Petrosyan TR (2013) Bacterial melanin favors regeneration after motor tract and peripheral nerve damage. Open Access J Sci Technol 1:1–6 Plonka PM, Grabacka M (2006) Melanin synthesis in microorganisms-biotechnological and medical aspects. Acta Biochim Pol 53:429–443 Prota G (1992) Melanins and melanogenesis. Academic Press, New York Pusztai M, Fast P, Gringorten L, Kaplan H, Lessard T, Carey PR (1991) The mechanism of sunlight mediated inactivation of Bacillus thuringiensis crystals. Biochem J 273:43–47 Rodriguez-Rojas A, Mena A, Martı´ın S, Borrell N, Oliver A, Blazquez J (2009) Inactivation of the hmgA gene of Pseudomonas aeruginosa leads to pyomelanin hyperproduction, stress resistance and increased persistence in chronic lung infection. Microbiology 155:1050–1057 Ruan L, Huang Y, Zhang G, Yu D, Ping S (2002) Expression of the mel gene from Pseudomonas maltophilia in Bacillus thuringiensis. Lett Appl Microbiol 34:244–248 Ruan L, Yu Z, Fang B, He W, Wang Y, Shen P (2004) Melanin pigment formation and increased UV resistance in Bacillus thuringiensis following high temperature induction. Syst Appl Microbiol 27:286–289 Sajjan S, Kulkarni G, Yaligara V, Kyoung L, Karegoudar T (2010) Purification and physiochemical characterization of melanin pigment from Klebsiella sp. GSK. J Microbiol Biotechnol 20:1513–1520

123

Salazar F, Ramı´rez M, Ortiz A, Sansinenea E (2014) A UV tolerant wild-type strain of Bacillus thuringiensis producing melanin. Jundishapur J Microbiol In press Sansinenea E (2012) Bacillus thuringiensis biotechnology. Springer, Netherlands Saxena D, Ben-Dov E, Manasherob R, Barak Z, Boussiba S, Zaritsky A (2002) A UV tolerant mutant of Bacillus thuringiensis subsp. kurstaki producing melanin. Curr Microbiol 44:25–30 Vilas-Boˆas GT, Vilas-Boˆas LA, Braz VT, Saridakis HO, Santos CA, Arantes OMN (2005) Isolation and partial characterization of a mutant of Bacillus thuringiensis producing melanin. Braz J Microbiol 36:271–274 Wakamatsu K, Ito S (2002) Advanced chemical methods in melanin determination. Pigment Cell Res 15:174–183 Wakamatsu K, Ito S, Rees JL (2002) The usefulness of 4-amino3-hydroxyphenylalanine as a specific marker of pheomelanin. Pigment Cell Res 15:225–232 Wan X, Liu HM, Liao Y, Su Y, Geng J, Yang MY, Chen XD, Shen P (2007) Isolation of a novel strain of Aeromonas media producing high levels of DOPA-melanin and assessment of the photoprotective role of the melanin in bioinsecticide applications. J Appl Microbiol 103: 2533–2541 Wheeler MH, Bell AA (1988) Melanins and their importance in pathogenic fungi. Curr Top Med Mycol 2:338–387 Zhang J, Cai J, Deng Y, Chen Y, Ren G (2007) Characterization of melanin produced by a wild-type strain of Bacillus cereus. Front Biol 2:26–29

Melanin: a photoprotection for Bacillus thuringiensis based biopesticides.

Melanins are negatively-charged, hydrophobic, dark high molecular weight irregular biopolymers, composed of polymerized phenolic and/or indolic compou...
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