Table of Contents    
REVIEW ARTICLE
Year : 2019  |  Volume : 10  |  Issue : 2  |  Page : 104-113  

Marine pigmented bacteria: A prospective source of antibacterial compounds


1 Andaman and Nicobar Centre for Ocean Science and Technology, ESSO-NIOT, Dollygunj, Port Blair, Andaman and Nicobar Islands, India
2 Marine Biotechnology Group, ESSO-National Institute of Ocean Technology (NIOT), Ministry of Earth Sciences (Govt. of India), Chennai, Tamil Nadu, India

Date of Web Publication18-Jul-2019

Correspondence Address:
Chatragadda Ramesh
Andaman and Nicobar Centre for Ocean Science and Technology, ESSO-National Institute of Ocean Technology, Dollygunj, Port Blair - 744 103
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jnsbm.JNSBM_201_18

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   Abstract 


Antimicrobial properties of several nonpigmented bacteria isolated from the marine environment have been well understood. However, marine bacteria with distinct asset of pigmentation have not been studied intensively and explored unlike nonpigmented bacteria. Recently, several studies have found multidrug-resistant microbes against various diseases. Therefore, search for alternative novel and natural bioactive compounds is in demand at current research. Furthermore, the application of synthetic colorants in the food industry has several harmful effects; thus, exploring pigments from natural environments is important to substitute synthetic colorants. This review emphasizes marine pigmented bacteria as a potential alternative source of natural compounds as well as natural colorants. The antibacterial potential of marine bacterial pigmented compounds reported from the year 2000 to hitherto is detailed cogitatively in this review, along with the best-known paradigms of pigments such as prodigiosin and violacein. In parenthesis, some other important applications of well-studied prodigiosin and violacein pigment molecules are highlighted briefly.

Keywords: Antibacterial activity, marine pigmented bacteria, pigment molecules, prodigiosin, violacein


How to cite this article:
Ramesh C, Vinithkumar NV, Kirubagaran R. Marine pigmented bacteria: A prospective source of antibacterial compounds. J Nat Sc Biol Med 2019;10:104-13

How to cite this URL:
Ramesh C, Vinithkumar NV, Kirubagaran R. Marine pigmented bacteria: A prospective source of antibacterial compounds. J Nat Sc Biol Med [serial online] 2019 [cited 2019 Oct 19];10:104-13. Available from: http://www.jnsbm.org/text.asp?2019/10/2/104/262948




   Introduction Top


Marine bacterial communities possess enormous potentiality to produce diverse bioactive molecules such as pigment molecules. On usual microbial culture media, several marine Gram-positive and Gram-negative bacteria appear to produce an array of pigments. Production of these pigments by microbes appears to mediated by the quorum-sensing mechanism.[1] Apparently, several marine bacterial pigments have demonstrated various biological activities such as antimicrobial, anticancer, and immunosuppressive activities.[2] Recently, studies on natural products and microbial autecology science have increased the demand for novel resources of eco-friendly natural products such as bacterial pigments for different biomedical and industrial applications.

Carotenes are polyunsaturated hydrocarbons that may contain 30, 40, or 50 carbon atoms in one molecule. Melanins are polyphenolic pigments that derived from phenolic compounds by the hydroxylation, oxidation, and polymerization reactions. Phenazines are tricyclic, redox-active, and small nitrogen-containing heterocyclic aromatic compounds. Prodiginines are aromatic chemical compounds with pyrrolyl dipyrromethene core structure. Quinones are aromatic ring-structure containing compounds with yellow-to-red color hues. Tambjamines are alkaloid compounds that show yellow color. Violacein compounds are indole-pigmented compounds derived from tryptophan metabolism. Pigment molecules of these families of compounds originated from marine bacteria demonstrated potential biomedical applications such as cytotoxic activities, antioxidant, antimicrobial, antimalarial, anticancer, antitumor, and antifouling properties.[3]

Such natural pigment molecules of microbial origin have a great demand in the industry due to their functional attributes such as nontoxic nature, easier gene manipulation, large volume of biomass production, and environmental acceptability. Therefore, exploration, exploitation, and identification of novel or rare types of pigment compounds from marine-pigmented bacteria (MPB) are necessary for wide range of biomedical and industrial applications.[4] Currently, cognitive scientists and food industries are seeking for such natural pigments from marine bacteria due to their functional attributes. These pigment molecules have not been fully explored from marine microbes and are still untouched when compared to microbes of terrestrial origin. Several carotenoids with potent antioxidant activity have been frequently observed from marine bacteria.[4] However, there are scarcely few reports on marine antimicrobial pigments. Therefore, in this review, we have detailed the antibacterial potential of various pigment molecules originated from marine bacteria isolated from different milieus. This review will be a beginner's guide and benefit the researchers greatly to work on MPB.


   Antibacterial Potential of Marine-Pigmented Bacteria Top


In the last decade, several marine bacterial species have been found to produce potential antimicrobial compounds against several pathogenic and nonpathogenic bacteria [Figure 1] and [Table 1], [Table 2]. The yellow color of Cytophaga/Flexibaterium cluster strain AM13 is due to tryptanthrin; a rare bacterial compound possesses antibiotic activity. In most other cases, yellow cultures owe their color to the carotenoid zeaxanthin (Hel21) or one of the many Vitamin K derivatives (e.g., menaquinone MK6 in Hel21).[35] The antibacterial activity of violet pigment, a mixture of violacein and deoxyviolacein, produced by the psychrotrophic bacterium Janthinobacterium lividum RT102 have resulted in complete inhibition of several pathogenic and putrefactive bacteria at minimum inhibitory concentration value of >15 mg/L.[18] It was revealed that marine heterotrophic-pigmented bacteria count for 1.4% of the total microbial community.[36] Evidently, marine heterotrophic-pigmented bacteria isolated from South China and the East China Sea and Pacific Ocean waters have displayed area-specific distribution and diversity with genus or species-specific color variation.[36]
Figure 1: Chemical structures of antibacterial pigment compounds of marine-pigmented bacteria

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Table 1: Antimicrobial pigment compounds from marine-pigmented bacteria

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Table 2: Antibacterial activities of marine pigmented bacteria against different pathogenic and nonpathogenic bacteria

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A red-pigmented marine bacterium Pseudovibrio denitrificans Z143-1 isolated from an unidentified tunicate exhibited anti-Staphylococcus aureus activity.[12] Fabrics such as wool and nylon samples dyed with the bright red pigment prodiginines extracted from a marine sediment isolate of Vibrio sp. killed 50% of the S. aureus and Escherichia coli.[8] A study also reported the strong growth inhibition activity by xanthophyll, a yellow pigment-producing Pseudoalteromonas piscicida, against S. aureus DSM 6672.[37] Collimonas fungivorans CTE227 a blue-black indole-derived pigment (violacein)-producing bacteria that isolated from the sea surface microlayer off the coast of Trøndelag, Norway, displayed the antibacterial activity against Micrococcus luteus.[17] Similarly, a deep blue pigment “glaukothalin” extracted from Rheinheimera strains (isolated from diatom aggregates and organic particles) showed >5 or <5 mm inhibition zone against two marine bacterial groups (Bacillus/Clostridium group and Cytophaga–Flavobacter–Bacteroides group).[1]

Significantly, purple-, red-, or yellow-pigmented Pseudoalteromonas were predominantly isolated from swabs of live or inert surfaces of different marine organisms in warmer waters.[23] The inhibitory activities caused by brown-pigmented Phaeobacter and Ruegeria bacterial species are due to the production of tropodithietic acid which is a species-specific metabolite likely essential for species survival.[23] The production of a diffusible brownish orange pigment by a marine luminous bacterium Vibrio campbellii has been related to either due to proteorhodopsin [38] or pyomelanin.[39] Prodigiosin, a red pigment compound has been extracted from a marine sponge Xestospongia testudinaria associated bacteria Serratia marcescens. Intracellular extract of this S. marcescens showed a wide range of antibacterial activity against Gram-positive and Gram-negative bacteria, and the highest zone of inhibition was found against methicillin-resistant S. aureus.[6]

Janthinobacterium sp. a violacein-producing bacterium isolated from Antarctic soil sample demonstrated potential inhibitory activity against different human Gram-negative bacterial pathogens, with varying concentrations of 0.5 and 16 μg/ml.[40] Pyocyanin a blue-green pigment produced by a hot spring isolate Pseudomonas aeruginosa possessed potential antimycobacterial activity against Mycobacterium smegmatis and other pathogenic bacteria.[34] Significantly, the production of indigoidine, a dark blue pigment by Leisingera sp., appeared to vary in pigment intensity in the presence of co-culture experiment, where higher pigment intensity was observed with the co-culture of Vibrio fischeri.[16] This Leisingera sp. is reported to display the antibacterial activity against different marine heterotrophic bacteria. Investigation by Leiva group found the association of a diverse community of Gram-positive yellow-, orange-, and amber-pigmented bacteria on Antarctic macroalgae (Adenocystis utricularis, Iridaea cordata, Monostroma hariotii, Plocamium cartilagineum, Phycodrys antarctica, and Pyropia endiviifolia) with potential antimicrobial activity against a set of macroalgae-associated bacteria.[41]

P. aeruginosa isolated from mangrove sediment samples of Vellar estuary produced blue-green pyocyanin and brownish pyorubin pigment compounds. These two compounds displayed maximum antibacterial activity at a concentration of 25 mg/mL with inhibition zones of 17 and 13 mm, respectively against Citrobacter sp.[25] Red pigment-producing vibrios (related to Vibrio rhizosphaerae and Vibrio ruber) isolated from different mangrove rhizospheres (Avicennia marina, Porteresia coarctata, and Rhizophora mucronata) have displayed antagonistic activity against both bacterial (Xanthomonas oryzae) and fungal (Fusarium oxysporum and Magnaporthe grisea) phytopathogens.[42]

A yellow-pigmented marine bacterium, M. luteus, isolated from seawater revealed the potential antibacterial activity against Staphylococcus sp., Klebsiella sp., and Pseudomonas sp.[43] Conversely, a strain of M. luteus BWCY16 isolated from seawater did not show inhibitory activity against Staphylococcus but showed the activity against Klebsiella and Pseudomonas.[44] These reports indicating that geographically different strains demonstrate species-specific antagonistic activity. S. marcescens CMST07, a red-pigmented estuarine bacterium exhibited antibacterial activity against different fouling bacteria Alteromonas, Bacillus, Gllionella, and Pseudomonas.[30] Streptomyces parvulus isolated from marine sediment sample produced a diffusible yellow pigment on YEME medium and also produced orange-red color antibiotic Actinomycin D that resulted potent antibacterial activity against different Gram-positive and Gram-negative bacterial pathogens and streptomycin-resistant strains such as Bacillus cereus and Pseudomonas putida.[24] Different textile fabrics treated with red pigment from a Vibrio species isolated from sweater sample has revealed distinctive inhibition activity against E. coli and S. aureus.[45] The yellow compounds fridamycin D and himalomycin A and B produced by Streptomyces sp. isolate B6921 have exhibited strong inhibition activity against E. coli, S. aureus, Streptomyces viridochromogenes, and Bacillus subtilis [Table 1] and [Table 2]. Biological activities of several other novel pigment bacterial species being reported in the International Journal of Systematic and Evolutionary Microbiology are still remained to be investigated for biomedical applications.


   Horizontal Gene Transfer/gene Acquisition Top


Pigment production in most of the known marine bacteria is due to the innate characteristic. However, the recent findings have suggested that bacteria-like Collimonas CT produce pigments due to gene acquisition (acquiring genes responsible for pigment production), probably acquired from J. lividum and/or Duganella sp.[17]


   Other Applications of Pigments Top


Reputedly prodigiosins and violacein pigment molecules have been widely used in several other applications regardless of biomedical applications. Prodigiosins are reported to have high color staining capability and thus they are used to stain candles, soap, papers, as ink in ballpoint and highlighter pens, and have potential dye application as colorants to different fabrics such as acrylic fiber, cotton, polyester, and silk.[46],[47] Application of virtual screening and prediction of bioactive nature of compounds in silico using various databases and docking programs would help to narrow down the range of such molecules to be tested in vitro and in vivo, which in turn can greatly reduce the economical investment in chemical synthesis and/or preliminary testing.[48]


   Conclusion Top


Although synthetic medicines appear to fight against human pathogenic bacteria, a variety of side effects have reported due to these medicines. While synthetic food colorants also found to cause several side effects such as cancer. Therefore, search and demand for natural pigments from marine bacteria is required to replace synthetic compounds. Microbial pigments could certainly replace such synthetic compounds. Since marine microbes tolerate a wide range of environmental factors, they can be cultured in vitro and desired level of pigment production can be achieved for various applications such as dyes, textiles, food colorants, and medicines. Pigmented bacteria are indeed displayed multifunctional compounds over other nonpigmented bacteria. Although bioactive nature of several nonpigmented bacteria has been reported from the sea, the vast marine environment has not been explored for pigmented bacteria. Therefore, studies on isolation, maintenance, and pigment production by pigmented bacteria are required in vitro to explore and standardize and to develop novel pigments.

Acknowledgments

Ramesh is grateful to the Science and Engineering Research Board, New Delhi, for funding under the National Postdoctoral Research Fellowship, grant number: SERB/N-PDF/2016/000354. We also thank the anonymous reviewers for their valuable comments and suggestions on this manuscript.

Financial support and sponsorship

This work has been funded by Science and Research Engineering Board, New Delhi, under National Postdoctoral Research Fellowship awarded to Ramesh.

Conflicts of interest

There are no conflicts of interest.



 
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