Abstract
The production of black pigments in bacteria was discovered more than a century ago and related to tyrosine metabolism. However, their diverse biological roles and the control of melanin synthesis in different bacteria have only recently been investigated. The broad distribution of these pigments suggests that they have an important role in a variety of organisms. Melanins protect microorganisms from many environmental stress conditions, ranging from ultraviolet radiation and toxic heavy metals to oxidative stress. Melanins can also affect bacterial interactions with other organisms and are important in pathogenesis and survival in many environments. Bacteria produce several types of melanin through dedicated pathways or as a result of enzymatic imbalances in altered metabolic routes. The control of the melanin synthesis in bacteria involves metabolic and transcriptional regulation, but many aspects remain still largely unknown. The diverse properties of melanins have spurred a large number of applications, and recent efforts have been done to produce the pigment at biotechnologically relevant scales.
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Change history
07 January 2020
The original version of this article contains error for some of the authors corrections were not included during correction stage especially for Table 1.
Notes
Bartolomeo Bizio was an Italian scientist, one of the precursors of modern microbiology though little is known about him at present. He chemically analyzed the ink of Sepia that he considered of a unique and admirable black color. In words of Bizio “having obtained a black matter so pure and so special that it cannot be compared with any of the known substances, I felt compelled to call it with a name that belonged only to it, naming her melaina” (Bizio 1825).
References
Ahmad S, Lee SY, Kong HG, Jo EJ, Choi HK, Khan R, Lee SW (2016) Genetic determinants for pyomelanin production and its protective effect against oxidative stress in Ralstonia solanacearum. PLoS One 11:e0160845. https://doi.org/10.1371/journal.pone.0160845
Ahmad S, Lee SY, Khan R, Kong HG, Son GJ, Roy N, Choi K, Lee SW (2017) Identification of a gene involved in the negative regulation of pyomelanin production in Ralstonia solanacearum. J Microbiol Biotechnol 27:1692–1700. https://doi.org/10.4014/jmb.1705.05049
Arias-Barrau E, Olivera ER, Luengo JM, Fernández C, Galán B, García JL, Díaz E, Miñambres B (2004) The homogentisate pathway: a central catabolic pathway involved in the degradation of L-phenylalanine, L-tyrosine, and 3-hydroxyphenylacetate in Pseudomonas putida. J Bacteriol 186:5062–5077. https://doi.org/10.1128/JB.186.15.5062-5077.2004
Banerjee A, Supakar S, Banerjee R (2014) Melanin from the nitrogen-fixing bacterium Azotobacter chroococcum: a spectroscopic characterization. PLoS One 9:e84574. https://doi.org/10.1371/journal.pone.0084574
Beijerinck MW (1900) Sur la production de quinone par le Streptothrix chromogena, et la biologie de ce microbe. In: Archives Néerlandaises des Sciences Exactes et Naturelles, Serie II, Tome III. Société hollandaise des sciences à Harlem, La Haye, pp 327–340. https://biodiversitylibrary.org/page/44932656
Beijerinck MW (1911) Pigments as products of oxidation by bacterial action. In: Proceedings of the Royal Netherlands Academy of Arts and Sciences (KNAW) 13 II, 1910-1911. Amsterdam, pp. 1066-1077
Ben-David Y, Zlotnik E, Zander I, Yerushalmi G, Shoshani S, Banin E (2018) SawR a new regulator controlling pyomelanin synthesis in Pseudomonas aeruginosa. Microbiol Res 206:91–98. https://doi.org/10.1016/j.micres.2017.10.004
Berzelius JJ (1840) Dinte vom Dintenfisch. In: Lehrbuch der Chemie, Vol 9. Arnoldischen Buchhandlung, Dresden-Leipzig, pp 776–778. https://books.google.com.ar/books?id=zp45AAAAcAAJ&printsec=frontcover#v=onepage&q&f=false
Bizio B (1825) Ricerche chimiche sovra l’inchiostro della Seppia. Giornale di fisica, chimica, storia naturale, medicina, ed Arti. Decade II, Tomo VIII: 88-108
Bolognese F, Scanferla C, Caruso E, Orlandi VT (2019) Bacterial melanin production by heterologous expression of 4-hydroxyphenylpyruvate dioxygenase from Pseudomonas aeruginosa. Int J Biol Macromol 133:1072–1080. https://doi.org/10.1016/j.ijbiomac.2019.04.061
Borthakur D, Lamb JW, Johnston AW (1987) Identification of two classes of Rhizobium phaseoli genes required for melanin synthesis, one of which is required for nitrogen fixation and activates the transcription of the other. Mol Gen Genet 207:155–160. https://doi.org/10.1007/bf00331503
Castro-Sowinski S, Martinez-Drets G, Okon Y (2002) Laccase activity in melanin-producing strains of Sinorhizobium meliloti. FEMS Microbiol Lett 209:119–125. https://doi.org/10.1111/j.1574-6968.2002.tb11119.x
Castro-Sowinski S, Matan O, Bonafede P, Okon Y (2007) A thioredoxin of Sinorhizobium meliloti CE52G is required for melanin production and symbiotic nitrogen fixation. Mol Plant-Microbe Interact 20:986–993. https://doi.org/10.1094/MPMI-20-8-0986
Chauhan PS, Goradia B, Saxena A (2017) Bacterial laccase: recent update on production, properties and industrial applications. 3 Biotech 7:323. https://doi.org/10.1007/s13205-017-0955-7
Chávez-Béjar MI, Balderas-Hernandez VE, Gutiérrez-Alejandre A, Martinez A, Bolívar F, Gosset G (2013) Metabolic engineering of Escherichia coli to optimize melanin synthesis from glucose. Microb Cell Factories 12:108. https://doi.org/10.1186/1475-2859-12-108
Chen LY, Leu WM, Wang KT, Lee YH (1992) Copper transfer and activation of the Streptomyces apotyrosinase are mediated through a complex formation between apotyrosinase and its trans-activator MelC1. J Biol Chem 267:20100–20107
Claus H, Decker H (2006) Bacterial tyrosinases. Syst Appl Microbiol 29:3–14. https://doi.org/10.1016/j.syapm.2005.07.012
Coyne VE, Al-Harthi L (1992) Induction of melanin biosynthesis in Vibrio cholerae. Appl Environ Microbiol 58:2861–2865
Crameri R, Ettlinger L, Hütter R, Lerch K, Suter MA, Vetterli JA (1982) Secretion of tyrosinase in Streptomyces glaucescens. J Gen Microbiol 128:371–379. https://doi.org/10.1099/00221287-128-2-371
Croxatto A, Chalker VJ, Lauritz J, Jass J, Hardman A, Williams P, Cámara M, Milton DL (2002) VanT, a homologue of Vibrio harveyi LuxR, regulates serine, metalloprotease, pigment, and biofilm production in Vibrio anguillarum. J Bacteriol 184:1617–1629. https://doi.org/10.1128/jb.184.6.1617-1629.2002
Dalfard AB, Khajeh K, Soudi MR, Naderi-Manesh H, Ranjbar B, Sajedi RH (2006) Isolation and biochemical characterization of laccase and tyrosinase activities in a novel melanogenic soil bacterium. Enzym Microb Technol 39:1409–1416
Denoya CD, Skinner DD, Morgenstern MR (1994) A Streptomyces avermitilis gene encoding a 4-hydroxyphenylpyruvic acid dioxygenase-like protein that directs the production of homogentisic acid and an ochronotic pigment in Escherichia coli. J Bacteriol 176:5312–5319. https://doi.org/10.1128/jb.176.17.5312-5319.1994
Diamantidis G, Effosse A, Potier P, Bally R (2000) Purification and characterization of the first bacterial laccase in the rhizospheric bacterium Azospirillum lipoferum. Soil Biol Biochem 32:919–927. https://doi.org/10.1016/S0038-0717(99)00221-7
Drewnowska JM, Zambrzycka M, Kalska-Szostko B, Fiedoruk K, Swiecicka I (2015) Melanin-like pigment synthesis by soil Bacillus weihenstephanensis isolates from northeastern Poland. PLoS One 10:e0125428. https://doi.org/10.1371/journal.pone.0125428
Ekborg NA, Gonzalez JM, Howard MB, Taylor LE, Hutcheson SW, Weiner RM (2005) Saccharophagus degradans gen. nov., sp. nov., a versatile marine degrader of complex polysaccharides. Int J Syst Evol Microbiol 55:1545–1549. https://doi.org/10.1099/ijs.0.63627-0
El-Naggar NE, El-Ewasy SM (2017) Bioproduction, characterization, anticancer and antioxidant activities of extracellular melanin pigment produced by newly isolated microbial cell factories Streptomyces glaucescens NEAE-H. Sci Rep 7:42129. https://doi.org/10.1038/srep42129
Faccio G, Kruus K, Saloheimo M, Thöny-Meyer L (2012) Bacterial tyrosinases and their applications. Process Biochem 47:1749–1760. https://doi.org/10.1016/j.procbio.2012.08.018
Fairhead M, Thöny-Meyer L (2012) Bacterial tyrosinases: old enzymes with new relevance to biotechnology. New Biotechnol 29:183–191. https://doi.org/10.1016/j.nbt.2011.05.007
Funa N, Ohnishi Y, Fujii I, Shibuya M, Ebizuka Y, Horinouchi S (1999) A new pathway for polyketide synthesis in microorganisms. Nature 400:897–899. https://doi.org/10.1038/23748
Funa N, Funabashi M, Ohnishi Y, Horinouchi S (2005) Biosynthesis of hexahydroxyperylenequinone melanin via oxidative aryl coupling by cytochrome P-450 in Streptomyces griseus. J Bacteriol 187:8149–8155. https://doi.org/10.1128/JB.187.23.8149-8155.2005
Gamal Shalaby AS, Ragab TIM, Helal MMI, Esawy MA (2019) Optimization of Bacillus licheniformis MAL tyrosinase: in vitro anticancer activity for brown and black eumelanin. Heliyon 5:e01657. https://doi.org/10.1016/j.heliyon.2019.e01657
Ganesh Kumar C, Sahu N, Narender Reddy G, Prasad RB, Nagesh N, Kamal A (2013) Production of melanin pigment from Pseudomonas stutzeri isolated from red seaweed Hypnea musciformis. Lett Appl Microbiol 57:295–302. https://doi.org/10.1111/lam.12111
Garrod AE (1996) The incidence of alkaptonuria: a study in chemical individuality. 1902. Mol Med 2:274–282
Gibello A, Ferrer E, Sanz J, Martin M (1995) Polymer production by Klebsiella pneumoniae 4-hydroxyphenylacetic acid hydroxylase genes cloned in Escherichia coli. Appl Environ Microbiol 61:4167–4171
Gibello A, Suárez M, Allende JL, Martín M (1997) Molecular cloning and analysis of the genes encoding the 4-hydroxyphenylacetate hydroxylase from Klebsiella pneumoniae. Arch Microbiol 167:160–166
Givaudan A, Effosse A, Faure D, Potier P, Bouillant ML, Bally R (1993) Polyphenol oxidase in Azospirillum lipoferum isolated from rice rhizosphere: evidence for laccase activity in non-motile strains of Azospirillum lipoferum. FEMS Microbiol Lett 108:205–210. https://doi.org/10.1111/j.1574-6968.1993.tb06100.x
Gómez-Marín AM, Sánchez CI (2010) Thermal and mass spectroscopic characterization of a sulphur-containing bacterial melanin from Bacillus subtilis. J Non-Cryst Solids 356:1576–1580. https://doi.org/10.1016/j.jnoncrysol.2010.05.054
Gonyar LA, Fankhauser SC, Goldberg JB (2015) Single amino acid substitution in homogentisate 1,2-dioxygenase is responsible for pigmentation in a subset of Burkholderia cepacia complex isolates. Environ Microbiol Rep 7:180–187. https://doi.org/10.1111/1758-2229.12217
Goodwin PH, Sopher CR (1994) Brown pigmentation of Xanthomonas campestris pv. phaseoli associated with homogentisic acid. Can J Microbiol 40:28–34
Goudenège D, Labreuche Y, Krin E, Ansquer D, Mangenot S, Calteau A, Médigue C, Mazel D, Polz MF, Le Roux F (2013) Comparative genomics of pathogenic lineages of Vibrio nigripulchritudo identifies virulence-associated traits. ISME J 7:1985–1996. https://doi.org/10.1038/ismej.2013.90
Gowri PM, Srivastava S (1996) Encapsulation as a response of Azospirillum brasilense sp7 to zinc stress. World J Microbiol Biotechnol 12:319–322. https://doi.org/10.1007/BF00340207
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. https://doi.org/10.1111/1574-6968.12497
Guo J, Rao Z, Yang T, Man Z, Xu M, Zhang X, Yang ST (2015) Cloning and identification of a novel tyrosinase and its overexpression in Streptomyces kathirae SC-1 for enhancing melanin production. FEMS Microbiol Lett 362:fnv041. https://doi.org/10.1093/femsle/fnv041
Gustavsson M, Hörnström D, Lundh S, Belotserkovsky J, Larsson G (2016) Biocatalysis on the surface of Escherichia coli: melanin pigmentation of the cell exterior. Sci Rep 6:36117. https://doi.org/10.1038/srep36117
Han H, Iakovenko L, Wilson AC (2015) Loss of homogentisate 1,2-dioxygenase activity in Bacillus anthracis results in accumulation of protective pigment. PLoS One 10:e0128967. https://doi.org/10.1371/journal.pone.0128967
Harir M, Bellahcene M, Baratto MC, Pollini S, Rossolini GM, Trabalzini L, Fatarella E, Pogni R (2018) Isolation and characterization of a novel tyrosinase produced by Sahara soil actinobacteria and immobilization on nylon nanofiber membranes. J Biotechnol 265:54–64. https://doi.org/10.1016/j.jbiotec.2017.11.004
Hawkins FK, Johnston AW (1988) Transcription of a Rhizobium leguminosarum biovar phaseoli gene needed for melanin synthesis is activated by nifA of Rhizobium and Klebsiella pneumoniae. Mol Microbiol 2:331–337. https://doi.org/10.1111/j.1365-2958.1988.tb00036.x
He P, Moran GR (2009) We two alone will sing: the two-substrate alpha-keto acid-dependent oxygenases. Curr Opin Chem Biol 13:443–450. https://doi.org/10.1016/j.cbpa.2009.06.012
Held T, Kutzner HJ (1990) Transcription of the tyrosinase gene in Streptomyces michiganensis DSM 40015 is induced by copper and repressed by ammonium. J Gen Microbiol 136:2413–2419
Hernández-Romero D, Solano F, Sanchez-Amat A (2005) Polyphenol oxidase activity expression in Ralstonia solanacearum. Appl Environ Microbiol 71:6808–6815. https://doi.org/10.1128/AEM.71.11.6808-6815.2005
Herrera MC, Krell T, Zhang X, Ramos JL (2009) PhhR binds to target sequences at different distances with respect to RNA polymerase in order to activate transcription. J Mol Biol 394:576–586. https://doi.org/10.1016/j.jmb.2009.09.045
Herter S, Schmidt M, Thompson ML, Mikolasch A, Schauer F (2011) A new phenol oxidase produced during melanogenesis and encystment stage in the nitrogen-fixing soil bacterium Azotobacter chroococcum. Appl Microbiol Biotechnol 90:1037–1049. https://doi.org/10.1007/s00253-011-3093-x
Hocquet D, Petitjean M, Rohmer L, Valot B, Kulasekara HD, Bedel E, Bertrand X, Plésiat P, Köhler T, Pantel A, Jacobs MA, Hoffman LR, Miller SI (2016) Pyomelanin-producing Pseudomonas aeruginosa selected during chronic infections have a large chromosomal deletion which confers resistance to pyocins. Environ Microbiol 18:3482–3493. https://doi.org/10.1111/1462-2920.13336
Hullo MF, Moszer I, Danchin A, Martin-Verstraete I (2001) CotA of Bacillus subtilis is a copper-dependent laccase. J Bacteriol 183:5426–5430. https://doi.org/10.1128/jb.183.18.5426-5430.2001
Hunter RC, Newman DK (2010) A putative ABC transporter, HatABCDE, is among molecular determinants of pyomelanin production in Pseudomonas aeruginosa. J Bacteriol 192:5962–5971. https://doi.org/10.1128/JB.01021-10
Ikeda K, Masujima T, Sugiyama M (1996) Effects of methionine and Cu2+ on the expression of tyrosinase activity in Streptomyces castaneoglobisporus. J Biochem 120:1141–1145. https://doi.org/10.1093/oxfordjournals.jbchem.a021533
Katz E, Betancourt A (1988) Induction of tyrosinase by L-methionine in Streptomyces antibioticus. Can J Microbiol 34:1297–1303. https://doi.org/10.1139/m88-227
Keith KE, Killip L, He P, Moran GR, Valvano MA (2007) Burkholderia cenocepacia C5424 produces a pigment with antioxidant properties using a homogentisate intermediate. J Bacteriol 189:9057–9065. https://doi.org/10.1128/JB.00436-07
Kelley SK, Coyne VE, Sledjeski DD, Claiborne Fuqua W, Weiner RM (1990) Identification of a tyrosinasse from a periphytic marine bacterium. FEMS Microbiol Lett 67:275–279. https://doi.org/10.1016/0378-1097(90)90008-E
Kimura T, Fukuda W, Sanada T, Imanaka T (2015) Characterization of water-soluble dark-brown pigment from Antarctic bacterium, Lysobacter oligotrophicus. J Biosci Bioeng 120:58–61. https://doi.org/10.1016/j.jbiosc.2014.11.020
Kiran GS, Dhasayan A, Lipton AN, Selvin J, Arasu MV, Al-Dhabi NA (2014) Melanin-templated rapid synthesis of silver nanostructures. J Nanobiotechnology 12:18. https://doi.org/10.1186/1477-3155-12-18
Kiran GS, Jackson SA, Priyadharsini S, Dobson ADW, Selvin J (2017) Synthesis of Nm-PHB (nanomelanin-polyhydroxy butyrate) nanocomposite film and its protective effect against biofilm-forming multi drug resistant Staphylococcus aureus. Sci Rep 7:9167. https://doi.org/10.1038/s41598-017-08816-y
Kotob SI, Coon SL, Quintero EJ, Weiner RM (1995) Homogentisic acid is the primary precursor of melanin synthesis in Vibrio cholerae, a Hyphomonas strain, and Shewanella colwelliana. Appl Environ Microbiol 61:1620–1622
Kurian NK, Bhat SG (2018) Data on the characterization of non-cytotoxic pyomelanin produced by marine Pseudomonas stutzeri BTCZ10 with cosmetological importance. Data Brief 18:1889–1894. https://doi.org/10.1016/j.dib.2018.04.123
Lagunas-Muñoz VH, Cabrera-Valladares N, Bolívar F, Gosset G, Martínez A (2006) Optimum melanin production using recombinant Escherichia coli. J Appl Microbiol 101:1002–1008. https://doi.org/10.1111/j.1365-2672.2006.03013.x
Lerch K, Ettinger L (1972) Purification and characterization of a tyrosinase from Streptomyces glaucescens. Eur J Biochem 31:427–437
Leu WM, Chen LY, Liaw LL, Lee YH (1992) Secretion of the Streptomyces tyrosinase is mediated through its trans-activator protein, MelC1. J Biol Chem 267:20108–20113
Li C, Ji C, Tang B (2018) Purification, characterisation and biological activity of melanin from Streptomyces sp. FEMS Microbiol Lett 365(19). https://doi.org/10.1093/femsle/fny077
Liu N, Zhang T, Wang YJ, Huang YP, Ou JH, Shen P (2004) A heat inducible tyrosinase with distinct properties from Bacillus thuringiensis. Lett Appl Microbiol 39:407–412. https://doi.org/10.1111/j.1472-765X.2004.01599.x
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. https://doi.org/10.1007/s13213-012-0570-0
López-Serrano D, Solano F, Sanchez-Amat A (2004) Identification of an operon involved in tyrosinase activity and melanin synthesis in Marinomonas mediterranea. Gene 342:179–187. https://doi.org/10.1016/j.gene.2004.08.003
Loprasert S, Whangsuk W, Dubbs JM, Sallabhan R, Somsongkul K, Mongkolsuk S (2007) HpdR is a transcriptional activator of Sinorhizobium meliloti hpdA, which encodes a herbicide-targeted 4-hydroxyphenylpyruvate dioxygenase. J Bacteriol 189:3660–3664. https://doi.org/10.1128/JB.01662-06
Lucas-Elío P, Solano F, Sanchez-Amat A (2002) Regulation of polyphenol oxidase activities and melanin synthesis in Marinomonas mediterranea: identification of ppoS, a gene encoding a sensor histidine kinase. Microbiology 148:2457–2466. https://doi.org/10.1099/00221287-148-8-2457
Madhusudhan DN, Mazhari BB, Dastager SG, Agsar D (2014) Production and cytotoxicity of extracellular insoluble and droplets of soluble melanin by Streptomyces lusitanus DMZ-3. Biomed Res Int 2014:306895. https://doi.org/10.1155/2014/306895
Manirethan V, Raval K, Rajan R, Thaira H, Balakrishnan RM (2018) Data on the removal of heavy metals from aqueous solution by adsorption using melanin nanopigment obtained from marine source: Pseudomonas stutzeri. Data in brief 20:178–189. https://doi.org/10.1016/j.dib.2018.07.065
Manivasagan P, Venkatesan J, Senthilkumar K, Sivakumar K, Kim SK (2013) Isolation and characterization of biologically active melanin from Actinoalloteichus sp. MA-32. Int J Biol Macromol 58:263–274. https://doi.org/10.1016/j.ijbiomac.2013.04.041
Matoba Y, Kumagai T, Yamamoto A, Yoshitsu H, Sugiyama M (2006) Crystallographic evidence that the dinuclear copper center of tyrosinase is flexible during catalysis. J Biol Chem 281:8981–8990. https://doi.org/10.1074/jbc.M509785200
McFall E, Newman EB (1996) Amino acids as carbon sources. In: Neidhardt FC, Curtiss R III, Ingraham JL, Lin EC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (eds) Escherichia coli and Salmonella: cellular and molecular biology, 2nd edn. ASM Press, Washington, DC, pp 358–379
McMahon AM, Doyle EM, Brooks S, O’Connor KE (2007) Biochemical characterisation of the coexisting tyrosinase and laccase in the soil bacterium Pseudomonas putida F6. Enzym Microb Technol 40:1435–1441. https://doi.org/10.1016/j.enzmictec.2006.10.020
Mekala LP, Mohammed M, Chinthalapati S, Chinthalapati VR (2019) Pyomelanin production: insights into the incomplete aerobic l-phenylalanine catabolism of a photosynthetic bacterium, Rubrivivax benzoatilyticus JA2. Int J Biol Macromol 126:755–764. https://doi.org/10.1016/j.ijbiomac.2018.12.142
Mercado-Blanco J, García F, Fernández-López M, Olivares J (1993) Melanin production by Rhizobium meliloti GR4 is linked to nonsymbiotic plasmid pRmeGR4b: cloning, sequencing, and expression of the tyrosinase gene mepA. J Bacteriol 175:5403–5410. https://doi.org/10.1128/jb.175.17.5403-5410.1993
Mistry JB, Bukhari M, Taylor AM (2013) Alkaptonuria. Rare Dis 1:e27475. https://doi.org/10.4161/rdis.27475
Noorian P, Hu J, Chen Z, Kjelleberg S, Wilkins MR, Sun S, McDougald D (2017) Pyomelanin produced by Vibrio cholerae confers resistance to predation by Acanthamoeba castellanii. FEMS Microbiol Ecol 93(12). https://doi.org/10.1093/femsec/fix147
Nosanchuk JD, Casadevall A (2003) The contribution of melanin to microbial pathogenesis. Cell Microbiol 5:203–223. https://doi.org/10.1046/j.1462-5814.2003.00268.x
Nosanchuk JD, Casadevall A (2006) Impact of melanin on microbial virulence and clinical resistance to antimicrobial compounds. Antimicrob Agents Chemother 50:3519–3528. https://doi.org/10.1128/AAC.00545-06
Orlandi VT, Bolognese F, Chiodaroli L, Tolker-Nielsen T, Barbieri P (2015) Pigments influence the tolerance of Pseudomonas aeruginosa PAO1 to photodynamically induced oxidative stress. Microbiology 161:2298–2309. https://doi.org/10.1099/mic.0.000193
Palmer GC, Palmer KL, Jorth PA, Whiteley M (2010) Characterization of the Pseudomonas aeruginosa transcriptional response to phenylalanine and tyrosine. J Bacteriol 192:2722–2728. https://doi.org/10.1128/JB.00112-10
Pavan ME, Abbott SL, Zorzópulos J, Janda JM (2000) Aeromonas salmonicida subsp. pectinolytica subsp. nov., a new pectinase-positive subspecies isolated from a heavily polluted river. Int J Syst Evol Microbiol 50(Pt 3):1119–1124. https://doi.org/10.1099/00207713-50-3-1119
Pavan ME, Pavan EE, López NI, Levin L, Pettinari MJ (2015) Living in an extremely polluted environment: clues from the genome of melanin-producing Aeromonas salmonicida subsp. pectinolytica 34melT. Appl Environ Microbiol 81:5235–5248. https://doi.org/10.1128/AEM.00903-15
Pavan ME, Solar Venero E, Egoburo DE, Pavan EE, López NI, Julia Pettinari M (2019) Glycerol inhibition of melanin biosynthesis in the environmental Aeromonas salmonicida 34melT. Appl Microbiol Biotechnol 103:1865–1876. https://doi.org/10.1007/s00253-018-9545-9
Piñero S, Rivera J, Romero D, Cevallos MA, Martínez A, Bolívar F, Gosset G (2007) Tyrosinase from Rhizobium etli is involved in nodulation efficiency and symbiosis-associated stress resistance. J Mol Microbiol Biotechnol 13:35–44. https://doi.org/10.1159/000103595
Plonka PM, Grabacka M (2006) Melanin synthesis in microorganisms - biotechnological and medical aspects. Acta Biochim Pol 53:429–443
Pomerantz SH, Murthy VV (1974) Purification and properties of tyrosinases from Vibrio tyrosinaticus. Arch Biochem Biophys 160:73–82
Reiss R, Ihssen J, Thöny-Meyer L (2011) Bacillus pumilus laccase: a heat stable enzyme with a wide substrate spectrum. BMC Biotechnol 11:9. https://doi.org/10.1186/1472-6750-11-9
Rizvi A, Ahmed B, Zaidi A, Khan MS (2019) Bioreduction of toxicity influenced by bioactive molecules secreted under metal stress by Azotobacter chroococcum. Ecotoxicology 28:302–322. https://doi.org/10.1007/s10646-019-02023-3
Rodríguez-Rojas A, Mena A, Martín S, Borrell N, Oliver A, Blázquez 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. https://doi.org/10.1099/mic.0.024745-0
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. System Appl Microbiol 27:286–289. https://doi.org/10.1078/0723-2020-00265
Sajjan S, Kulkarni G, Yaligara V, Kyoung L, Karegoudar TB (2010) Purification and physiochemical characterization of melanin pigment from Klebsiella sp. GSK J Microbiol Biotechnol 20:1513–1520. https://doi.org/10.4014/jmb.1002.02006
Sanchez-Amat A, Solano F (1997) A pluripotent polyphenol oxidase from the melanogenic marine Alteromonas sp shares catalytic capabilities of tyrosinases and laccases. Biochem Biophys Res Commun 240:787–792
Sanchez-Amat A, Ruzafa C, Solano F (1998) Comparative tyrosine degradation in Vibrio cholerae strains. The strain ATCC 14035 as a prokaryotic melanogenic model of homogentisate-releasing cell. Comp Biochem Physiol B Biochem Mol Biol 119:557–562. https://doi.org/10.1016/S0305-0491(98)00028-5
Sanchez-Amat A, Solano F, Lucas-Elío P (2010) Finding new enzymes from bacterial physiology: a successful approach illustrated by the detection of novel oxidases in Marinomonas mediterranea. Mar Drugs 8:519–541. https://doi.org/10.3390/md8030519
Schaerlaekens K, Schierová M, Lammertyn E, Geukens N, Anné J, Van Mellaert L (2001) Twin-arginine translocation pathway in Streptomyces lividans. J Bacteriol 183:6727–6732. https://doi.org/10.1128/JB.183.23.6727-6732.2001
Shivprasad S, Page WJ (1989) Catechol formation and melanization by Na+-dependent Azotobacter chroococcum: a protective mechanism for aeroadaptation? Appl Environ Microbiol 55:1811–1817
Shuster V, Fishman A (2009) Isolation, cloning and characterization of a tyrosinase with improved activity in organic solvents from Bacillus megaterium. J Mol Microbiol Biotechnol 17:188–200. https://doi.org/10.1159/000233506
Silva C, Santos A, Salazar R, Lamilla C, Pavez B, Meza P, Hunter R, Barrientos L (2019) Evaluation of dye sensitized solar cells based on a pigment obtained from Antarctic Streptomyces fildesensis. Sol Energy 181:379–385. https://doi.org/10.1016/j.solener.2019.01.035
Singh G, Bhalla A, Kaur P, Capalash N, Sharma P (2011) Laccase from prokaryotes: a new source for an old enzyme. Rev Environ Sci Biotechnol 10:309–326. https://doi.org/10.1007/s11157-011-9257-4
Singh S, Malhotra AG, Pandey A, Pandey KM (2013) Computational model for pathway reconstruction to unravel the evolutionary significance of melanin synthesis. Bioinformation 9:94–100. https://doi.org/10.6026/97320630009094
Singh D, Kumar J, Kumar A (2018) Isolation of pyomelanin from bacteria and evidences showing its synthesis by 4-hydroxyphenylpyruvate dioxygenase enzyme encoded by hppD gene. Int J Biol Macromol 119:864–873. https://doi.org/10.1016/j.ijbiomac.2018.08.003
Skinner CE (1938) The “tyrosinase reaction” of the actinomycetes. J Bacteriol 35:415–424
Solano F (2014) Melanins: skin pigments and much more - types, structural models, biological functions, and formation routes. New Journal of Science 2014:Article ID 498276. https://doi.org/10.1155/2014/498276
Solano F, Lucas-Elío P, Fernández E, Sanchez-Amat A (2000) Marinomonas mediterranea MMB-1 transposon mutagenesis: isolation of a multipotent polyphenol oxidase mutant. J Bacteriol 182:3754–3760. https://doi.org/10.1128/jb.182.13.3754-3760.2000
Stepanova V, Rodionov DA (2011) Genomic analysis of transcriptional regulation of aromatic amino acid metabolism in gammaproteobacteria. Department of Bioengineering and Bioinformatics of MV Lomonosov Moscow State University 352:186–188
Surwase SN, Jadhav SB, Phugare SS, Jadhav JP (2013) Optimization of melanin production by Brevundimonas sp. SGJ using response surface methodology. 3. Biotech 3:187–194. https://doi.org/10.1007/s13205-012-0082-4
Takano H, Asano K, Beppu T, Ueda K (2007) Role of σH paralogs in intracellular melanin formation and spore development in Streptomyces griseus. Gene 393:43–52. https://doi.org/10.1016/j.gene.2007.01.026
Tarangini K, Mishra S (2013) Production, characterization and analysis of melanin from isolated marine Pseudomonas sp. using vegetable waste. Res J Engineering Sci 2:40–46
Tarangini K, Mishra S (2014) Production of melanin by soil microbial isolate on fruit waste extract: two step optimization of key parameters. Biotechnol Rep 4:139–146. https://doi.org/10.1016/j.btre.2014.10.001
Thaira H, Raval K, Manirethan V, Balakrishnan RM (2019) Melanin nano-pigments for heavy metal remediation from water. Sep Sci Technol 54:265–274. https://doi.org/10.1080/01496395.2018.1443132
Toledo AV, Franco MEE, López SMY, Troncozo MI, Saparrat MCN, Balatti PA (2017) Melanins in fungi: types, localization and putative biological roles. Physiol Mol Plant Path 99:2–6. https://doi.org/10.1016/j.pmpp.2017.04.004
Trias J, Viñas M, Guinea J, Lorèn JG (1989) Brown pigmentation in Serratia marcescens cultures associated with tyrosine metabolism. Can J Microbiol 35:1037–1042
Tsai TY, Lee YH (1998) Roles of copper ligands in the activation and secretion of Streptomyces tyrosinase. J Biol Chem 273:19243–19250. https://doi.org/10.1074/jbc.273.30.19243
Tsai YJ, Ouyang CY, Ma SY, Tsai DY, Tseng HW, Yeh YC (2014) Biosynthesis and display of diverse metal nanoparticles by recombinant Escherichia coli. RSC Adv 4:58717–58719. https://doi.org/10.1039/c4ra12805b
Turick CE, Tisa LS, Caccavo F Jr (2002) Melanin production and use as a soluble electron shuttle for Fe(III) oxide reduction and as a terminal electron acceptor by Shewanella algae BrY. Appl Environ Microbiol 68:2436–2444. https://doi.org/10.1128/AEM.68.5.2436-2444.2002
Turick CE, Knox AS, Leverette CL, Kritzas YG (2008) In situ uranium stabilization by microbial metabolites. J Environ Radioact 99:890–899. https://doi.org/10.1016/j.jenvrad.2007.11.020
Turick CE, Beliaev AS, Zakrajsek BA, Reardon CL, Lowy DA, Poppy TE, Maloney A, Ekechukwu AA (2009) The role of 4-hydroxyphenylpyruvate dioxygenase in enhancement of solid-phase electron transfer by Shewanella oneidensis MR-1. FEMS Microbiol Ecol 68:223–235. https://doi.org/10.1111/j.1574-6941.2009.00670.x
Turick CE, Knox AS, Becnel JM, Ekechukwu AA, Milliken CE (2010) Properties and function of pyomelanin. In: Elnashar M (ed) Biopolymers, 1st edn. Sciyo, Rijeka, pp 449–472. https://doi.org/10.5772/10273
Unuofin JO, Okoh AI, Nwodo UU (2019) Aptitude of oxidative enzymes for treatment of wastewater pollutants: a laccase perspective. Molecules 24:2064. https://doi.org/10.3390/molecules24112064
Valeru SP, Rompikuntal PK, Ishikawa T, Vaitkevicius K, Sjöling A, Dolganov N, Zhu J, Schoolnik G, Wai SN (2009) Role of melanin pigment in expression of Vibrio cholerae virulence factors. Infect Immun 77:935–942. https://doi.org/10.1128/IAI.00929-08
Vijayan V, Jasmin C, Anas A, Kuttan SP, Vinothkumar S, Subrayan PP, Nair S (2017) Sponge-associated bacteria produce non-cytotoxic melanin which protects animal cells from photo-toxicity. Appl Biochem Biotechnol 183:396–411. https://doi.org/10.1007/s12010-017-2453-0
Wang R, Wang H, Zhou H, Wang Y, Yue J, Diao B, Kan B (2011) Characters of homogentisate oxygenase gene mutation and high clonality of the natural pigment-producing Vibrio cholerae strains. BMC Microbiol 11:109. https://doi.org/10.1186/1471-2180-11-109
Wang H, Qiao Y, Chai B, Qiu C, Chen X (2015) Identification and molecular characterization of the homogentisate pathway responsible for pyomelanin production, the major melanin constituents in Aeromonas media WS. PLoS One 10:e0120923. https://doi.org/10.1371/journal.pone.0120923
Wang L, Li Y, Li Y (2019) Metal ions driven production, characterization and bioactivity of extracellular melanin from Streptomyces sp. ZL-24. Int J Biol Macromol 123:521–530. https://doi.org/10.1016/j.ijbiomac.2018.11.061
Yabuuchi E, Ohyama A (1972) Characterization of “pyomelanin”-producing strains of Pseudomonas aeruginosa. Int J Syst Bacteriol 22:53–64. https://doi.org/10.1099/00207713-22-2-53
Zaidi KU, Ali AS, Ali SA, Naaz I (2014, 2014) Microbial tyrosinases: promising enzymes for pharmaceutical, food bioprocessing, and environmental industry. Biochem Res Int. https://doi.org/10.1155/2014/854687
Zeng Z, Cai X, Wang P, Guo Y, Liu X, Li B, Wang X (2017a) Biofilm formation and heat stress induce pyomelanin production in deep-sea Pseudoalteromonas sp. SM9913. Front Microbiol 8:1822. https://doi.org/10.3389/fmicb.2017.01822
Zeng Z, Guo XP, Cai X, Wang P, Li B, Yang JL, Wang X (2017b) Pyomelanin from Pseudoalteromonas lipolytica reduces biofouling. Microb Biotechnol 10:1718–1731. https://doi.org/10.1111/1751-7915.12773
Zerrad A, Anissi J, Ghanam J, Sendide K, El Hassouni M (2014) Antioxidant and antimicrobial activities of melanin produced by a Pseudomonas balearica strain. J Biotechnol Lett 5:87–94
Zheng H, Chatfield CH, Liles MR, Cianciotto NP (2013) Secreted pyomelanin of Legionella pneumophila promotes bacterial iron uptake and growth under iron-limiting conditions. Infect Immun 81:4182–4191. https://doi.org/10.1128/IAI.00858-13
Zhu D, He X, Zhou X, Deng Z (2005) Expression of the melC operon in several Streptomyces strains is positively regulated by AdpA, an AraC family transcriptional regulator involved in morphological development in Streptomyces coelicolor. J Bacteriol 187:3180–3187. https://doi.org/10.1128/JB.187.9.3180-3187.2005
Acknowledgments
The authors thank Esteban Pavan for helpful comments. N.I.L. and M.J.P. are career investigators from CONICET.
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This work was partially supported by the University of Buenos Aires, CONICET, and Agencia Nacional de Promoción Científica y Tecnológica.
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Pavan, M.E., López, N.I. & Pettinari, M.J. Melanin biosynthesis in bacteria, regulation and production perspectives. Appl Microbiol Biotechnol 104, 1357–1370 (2020). https://doi.org/10.1007/s00253-019-10245-y
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DOI: https://doi.org/10.1007/s00253-019-10245-y