Abstract
In our previous research, we constructed a Bacillus thuringiensis (Berliner) (Bacillales: Bacillaceae; Bt) strain (BMB171ΔhmgA), in which the loss of homogentisate 1, 2-dioxygenase (HmgA) activity promoted the melanin accumulation in the culture medium. However, further improvement in melanin yield by Bt strains has not been considered. Herein, based on the melanin synthesis pathway, we attempted to increase the melanin yield in Bt by adding a suitable concentration of L-tyrosine and increasing the expression levels of tyrosine aminotransferase (PhhC) and 4-hydroxyphenylpyruvate dioxygenase (HppD) using strong promoters. The results showed that the melanin yield of the engineered strain (Bt-2P) grown in medium supplemented with L-tyrosine was approximately 5.7 times higher than that of the original strain without L-tyrosine, suggesting that L-tyrosine addition and phhC or hppD overexpression were effective to improve the melanin yield in Bt. In addition, we tested the photoprotective effect of melanin on Autographa californica (Speyer) (Lepidoptera: Noctuidae) multiple nucleopolyhedrovirus (Lefavirales: Baculoviridae; AcMNPV) and Ralstonia solanacearum (Smith) Yabuuchi et al. (Burkholderiales: Burkholderiaceae) bacteriophage ФNK-7 against ultraviolet (UV) irradiation. The results implied that the titers of AcMNPV and bacteriophage ФNK-7 in the presence of melanin were approximately ten and four times higher than those without melanin under UV radiation, respectively. This indicated that the addition of melanin could effectively maintain the activities of the viruses. In conclusion, we reported strategies to increase the melanin yield in Bt and expanded the potential applications of melanin.
Similar content being viewed by others
References
Akhanaev Y, Pavlushin S, Polenogova O, Klementeva T, Lebedeva D, Okhlopkova O, Kolosov A, Martemyanov V (2022) The effect of mixtures of Bacillus thuringiensis-based insecticide and multiple nucleopolyhedrovirus of Lymantria dispar L. in combination with an optical brightener on L. dispar larvae. BioControl 67:331–343
Bridelli MG, Crippa PR (2010) Infrared and water sorption studies of the hydration structure and mechanism in natural and synthetic melanin. J Phys Chem B 114:9381–9390
Cao Z, Tan T, Jiang K, Mei S, Hou X, Cai J (2018) Complete genome sequence of Bacillus thuringiensis L-7601, a wild strain with high production of melanin. J Biotechnol 275:40–43
Chen Y, Deng Y, Wang J, Cai J, Ren G (2004) Characterization of melanin produced by a wild-type strain of Bacillus cereus. J Gen Appl Microbiol 50:183–188
Crickmore N, Zeigler DR, Feitelson J, Schnepf E, van Rie J, Lereclus D, Baum J, Dean DH (1998) Revision of the nomenclature for the Bacillus thuringiensis pesticidal crystal proteins. Microbiol Mol Biol Rev 62:807–813
Duarte Neto JM, Wanderley MC, da Silva TA, Marques DA, da Silva GR, Gurgel JF, Oliveira JD, Porto AL (2020) Bacillus thuringiensis endotoxin production: a systematic review of the past 10 years. World J Microbiol Biotechnol 36:128
Fu W, Wu Z, Zheng R, Yin N, Han F, Zhao Z, Dai M, Han D, Wang W, Niu L (2022) Inhibition mechanism of melanin formation based on antioxidant scavenging of reactive oxygen species. Analyst 147:2703–2711
Glass K, Ito S, Wilby PR, Sota T, Nakamura A, Bowers CR, Vinther J, Dutta S, Summons R, Briggs DEG, Wakamatsu K, Simon JD (2012) Direct chemical evidence for eumelanin pigment from the Jurassic period. Proc Natl Acad Sci 109:10218–10223
Gobatto V, Giani SG, Camassola M, Dillon AJP, Specht A, Barros NM (1998) Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol Mol Biol Rev 62:775–806
Guo J, Rao Z, Yang T, Man Z, Xu M, Zhang X (2014) High-level production of melanin by a novel isolate of Streptomyces kathirae. FEMS Microbiol Lett 357:85–91
Gupta M, Kumar H, Kaur S (2021) Vegetative insecticidal protein (Vip): a potential contender from Bacillus thuringiensis for efficient management of various detrimental agricultural pests. Front Microbiol 12:659736
Hodgson JJ, Buchon N, Blissard GW (2019) Identification of insect genes involved in baculovirus AcMNPV entry into insect cells. Virology 527:1–11
Kim YJ, Wu W, Chun SE, Whitacre JF, Bettinger CJ (2013) Biologically derived melanin electrodes in aqueous sodium-ion energy storage devices. Proc Natl Acad Sci 110:20912–20917
Kiran GS, Dhasayan A, Lipton AN, Selvin J, Arasu MV, Al-Dhabi NA (2014) Melanin-templated rapid synthesis of silver nanostructures. J Nanobiotechnol 12:18
Li X, Zhang Y, Zhan Y, Tian H, Yan B, Cai J (2023) Utilization of a strong promoter combined with the knockout of protease genes to improve the yield of Vip3Aa in Bacillus thuringiensis BMB171. Pest Manag Sci 79:1713–1720
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
Liu Y, Ai K, Lu L (2014) Polydopamine and its derivative materials: Synthesis and promising applications in energy, environmental, and biomedical fields. Chem Rev 114:5057–5115
Martínez LM, Martinez A, Gosset G (2019) Production of melanins with recombinant microorganisms. Front Bioeng Biotechnol 7:285
Meng XQ, Zheng GL, Zhao CD, Wan FH, Li CY (2017) A cell clone strain from Mythimna separata (Lepidoptera: Noctuidae) highly susceptible to Autographa californica multiple nucleopolyhedrovirus (AcMNPV) and M. separata NPV (MsNPV). Vitr Cell Dev Biol—Anim 53:646–650
Nion YA, Toyota K (2015) Recent trends in control methods for bacterial wilt diseases caused by Ralstonia solanacearum. Microbes Environ 30:1–11
Palma L, Muñoz D, Berry C, Murillo J, Caballero P (2014) Bacillus thuringiensis toxins: An overview of their biocidal activity. Toxins 6:3296–3325
Plonka PM, Grabacka M (2006) Melanin synthesis in microorganisms - Biotechnological and medical aspects. Acta Biochim Pol 53:429–443
Pralea IE, Moldovan RC, Petrache AM, Ilieș M, Hegheș SC, Ielciu I, Nicoară R, Moldovan M, Ene M, Radu M, Uifălean A, Iuga CA (2019) From extraction to advanced analytical methods: The challenges of melanin analysis. Int J Mol Sci 20:3943
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
Ribera J, Panzarasa G, Stobbe A, Osypova A, Rupper P, Klose D, Schwarze FWMR (2019) Scalable biosynthesis of melanin by the basidiomycete Armillaria cepistipes. J Agric Food Chem 67:132–139
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
Sansinenea E, Ortiz A (2015) Melanin: a photoprotection for Bacillus thuringiensis based biopesticides. Biotechnol Lett 37:483–490
Sansinenea E, Salazar F, Ramirez M, Ortiz A (2015) An ultra-violet tolerant wild-type strain of melanin-producing Bacillus thuringiensis. Jundishapur J Microbiol 8:e20910
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
Singh S, Nimse SB, Mathew DE, Dhimmar A, Sahastrabudhe H, Gajjar A, Ghadge VA, Kumar P, Shinde PB (2021) Microbial melanin: Recent advances in biosynthesis, extraction, characterization, and applications. BioTechnol Adv 53:107773
Smagghe F, Spooner-Hart R, Chen ZH, Donovan-Mak M (2023) Biological control of arthropod pests in protected cropping by employing entomopathogens: Efficiency, production and safety. Biol Control 186:105337
Sono K, Lye D, Moore CA, Boyd WC, Gorlin TA, Belitsky JM (2012) Melanin-based coatings as lead-binding agents. Bioinorg Chem Appl 2012:361803
Tan TT, Zhang XD, Miao Z, Yu Y, Du SL, Hou XY, Cai J (2019) A single point mutation in hmgA leads to melanin accumulation in Bacillus thuringiensis BMB181. Enzyme Microb Technol 120:91–97
Tarangini K, Mishra S (2014) Production of melanin by soil microbial isolate on fruit waste extract: two step optimization of key parameters. Biotechnol Reports 4:139–146
Tran-Ly AN, Reyes C, Schwarze FWMR, Ribera J (2020) Microbial production of melanin and its various applications. World J Microbiol Biotechnol 36:170
Xue QY, Yin YN, Yang W, Heuer H, Prior P, Guo JH, Smalla K (2011) Genetic diversity of Ralstonia solanacearum strains from China assessed by PCR-based fingerprints to unravel host plant- and site-dependent distribution patterns. FEMS Microbiol Ecol 75:507–519
Yang W, Ruan L, Tao J, Peng D, Zheng J, Sun M (2018) Single amino acid substitution in homogentisate dioxygenase affects melanin production in Bacillus thuringiensis. Front Microbiol 9:2242
Zhang JT, Yan JP, Zheng DS, Sun YJ, Yuan ZM (2008) Expression of mel gene improves the UV resistance of Bacillus thuringiensis. J Appl Microbiol 105:151–157
Zhang B, Liang A, Fu Y (2019) Ac34 protein of AcMNPV promoted progeny virus production and induced the apoptosis in host Sf9 cells. Biotechnol Lett 41:147–158
Zhu L, Chu Y, Zhang B, Yuan X, Wang K, Liu Z, Sun M (2022) Creation of an industrial Bacillus thuringiensis strain with high melanin production and UV tolerance by gene editing. Front Microbiol 13:913715
Acknowledgements
This work was supported by the Science and Technology Plan Project of Yunnan Tobacco Company Kunming Branch (No. KMYC202201) and the National Natural Science Foundation of China (No. 32272610).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing financial interest.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. No human participants were involved.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
An, B., Zhan, Y., Cheng, Q. et al. Production improvement and photoprotection of melanin produced by Bacillus thuringiensis. BioControl (2024). https://doi.org/10.1007/s10526-024-10250-9
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10526-024-10250-9