Research review paperMicrobial melanin: Recent advances in biosynthesis, extraction, characterization, and applications
Introduction
Natural pigments are considered safe, with pronounced multifarious benefits compared to synthetic pigments, among those, ‘Melanin’ forms a ubiquitous heterogeneous polymer group with a broad range of structural and functional diversity (Gosset, 2017; Stepien et al., 2013). On tracing back the Greek history, ‘Melanin’ came from melanos, meaning dark, but scientifically the term was coined in 1840 by Berzelius, a Swedish scientist for extraction of a dark-colored pigment from eye membranes. The polymeric pigments arise through the oxidation of phenolic or indolic substrates involving the enzyme catalysis. Solano (2014) defined melanin as a heterogeneous polymer derived by the oxidation of phenols and subsequent polymerization of intermediate phenols and their resulting quinones. Categorically melanin can be divided into three main types based on their structural monomers; eumelanin, pheomelanin, and allomelanin. Eumelanin and allomelanin impart black/brown color to the cells, whereas pheomelanin (animal kingdom) provides yellow/red pigmentation (Pralea et al., 2019; Nicolaus, 1968). Precursor units for the polymer of eumelanin consist primarily of indole-type units that arise from L-tyrosine or L-DOPA (L-3,4-dihydroxyphenylalanine) oxidation. Similarly, pheomelanins are the products of oxidative polymerization of cysteinyl conjugates of DOPA via benzothiazine intermediates (Prota, 1992; Wakamatsu and Ito, 2002; Ito et al., 2019). On the other hand, allomelanins are derived by the oxidation of nitrogen-free diphenols, such as catechol, 1,8-dihydroxynaphtalene, and γ-glutaminyl-3,4-dihydroxybenzene. Two more types of melanin also exist namely, pyomelanin and neuromelanin. Pyomelanin is a product of oxidation of homogentisic acid, whereas neuromelanin comprises of both benzothiazine and indole units (Pralea et al., 2019; Haining and Achat-Mendes, 2017). Apart from providing pigmentation to cells, melanin protects cells against UV radiations (Stepien et al., 2013; Coelho et al., 2009), performs quenching of free radicals (Meredith and Sarna, 2006), are responsible for varied functions in various phyla (Bonser, 1995; Trullas et al., 2007; Stuart-Fox and Moussalli, 2008), helps with defense mechanism in insects and mollusks (Palumbo, 2003; Vavricka et al., 2014), enhances virulence mechanism in various fungi and bacteria (Nosanchuk and Casadevall, 2003), provides the advantage of antibacterial and antioxidant activities. Furthermore, melanins have applications in semiconductors (Bothma et al., 2008), as metal chelators, as optical imagers (Abbas et al., 2009), in cosmeceuticals and pharmaceuticals, MRI probes, soil bioremediations, etc. (Martinez et al., 2019). Despite such promising and diverse attributes, it is quite taxing to elucidate specific conclusions regarding their properties and structures because of their physicochemical properties and heterogeneities. A major reason for heterogeneity is the lack of genetic makeup responsible for melanin biosynthesis and sequential metabolic pathways. Further, microbes have the proficiency in utilizing multiple precursors for melanin synthesis, making the polymerization process more haphazard amongst them (Cao et al., 2021). Difficulties in unscrambling the structural features and the insolubility of melanin in most solvents potentially challenges its extraction and purification techniques obstructing its cost-effective industrial production (Borovansky and Riley, 2011; Sun et al., 2016). Conclusively, the development of environment-friendly and cost-effective melanin production from eukaryotic resources is challenging; in such conditions, microbial melanin can pave the way (Sun et al., 2016; Pavan et al., 2020). Production of melanin from microbial sources is effective because of easy fermentation procedures where the yield can be accelerated by optimizing factors affecting melanin synthesis.
According to our knowledge, within the last five years, some exceptional reviews (Roy and Rhim, 2021; Tran-Ly et al., 2020; Vasanthabharathi and Jayalakshmi, 2020; Pavan et al., 2020; Pralea et al., 2019; Martinez et al., 2019) on microbial melanin have been reported focusing on specific attributes, either biosynthesis, characterization, production perspectives or biomaterial obtained from melanin; there lacks a comprehensive report of microbial melanin from biosynthesis to its application in several fields. Moreover, the present review targets the literature of melanin obtained from microbial sources, including bacteria, fungi, and actinobacteria, which so far is among the first reviews on microbial melanin. Herein, this review is focused on biosynthetic, extraction, and purification techniques, characteristics, and applicative attributes of microbial melanin. The review aimed to address how different functional properties of microbial melanin can be endorsed in industrial applications.
Section snippets
Melanin biosynthesis
Melanin synthesis requires polymeric oxidation of polyphenolic compounds involving enzymes such as tyrosinase or laccase. Tyrosinases have monophenol monooxygenase (EC 1.18.14.1) and o-diphenol:oxygen-oxidoreductase (EC 1.10.3.1) activities, and laccases have p-diphenol:oxygen-oxidoreductase (EC 1.10.3.2) activity. A study on Sinorhizobium melilotii reported that thioredoxin mutants of S. melilotii were defective in melanin production (Castro-Sowinski et al., 2007). Thioredoxin and tyrosinase
Extraction and purification
Distinct melanin sources such as fungi, bacteria, and its intracellular or extracellular localization form a basic platform to choose its extraction and purification methodology (Aghajanyan et al., 2005, Aghajanyan et al., 2017; Gomez-Marin and Sanchez, 2010). Melanin extraction employs different protocols pertaining to its amorphous nature and structural diversity (Aghajanyan et al., 2017; Tarangini and Mishra, 2014). Some processes require acid hydrolysis whereas others use sequential washing
Characterization of melanin
Melanin lacks a unique well-defined structure because of its heterogeneous nature. Hence, a pool of rigorous characterization techniques (Fig. 8) are required to patiently determine the structure of melanin and to identify between its two main types (D'Ischia et al., 2013).
Applications of microbial melanin
Microbial melanin have supremacy over melanin from other sources, such as no effect of seasonal variations, low-cost maintenance, easy operation, requires mild reaction conditions, and can be modified according to the medium and conditions of fermentation (Tarangini and Mishra, 2014; Liu et al., 2018) (Fig. 14).
Conclusions
Melanin upholds diverse applications as a result of its environmentally sustainable and multifarious biological properties. Microorganisms have emerged as a great source of melanin pertaining to their easier upscaling opportunities while maintaining large structural diversity. The complexity of these complex biopolymers lies in the dedicated biosynthetic pathways mostly altered due to enzymatic imbalances, wherein the pivotal role is played by precursor metabolites whose changing concentrations
Funding
This research was supported by Scientific and Engineering Research Board (SERB), Department of Science and Technology [ECRA/2016/000788 and EEQ/2016/000268]; and Council of Scientific and Industrial Research [MLP/0027].
Declaration of Competing Interest
None.
Acknowledgments
Sanju Singh, Doniya Elze Mathew, Asmita Dhimmar acknowledges CSIR-JRF fellowship from Council of Scientific and Industrial Research (CSIR), Pankaj Kumar and Apexa Gajjar acknowledges DBT-JRF fellowship from Department of Biotechnology (DBT), and Harshal Sahastrabudhe acknowledges GATE-JRF fellowship from Council of Scientific and Industrial Research (CSIR).
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These authors contributed equally.