|Year : 2019 | Volume
| Issue : 2 | Page : 104-113
Marine pigmented bacteria: A prospective source of antibacterial compounds
Chatragadda Ramesh1, Nambali Valsalan Vinithkumar1, Ramalingam Kirubagaran2
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 Publication||18-Jul-2019|
Andaman and Nicobar Centre for Ocean Science and Technology, ESSO-National Institute of Ocean Technology, Dollygunj, Port Blair - 744 103
Source of Support: None, Conflict of Interest: None
| 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 2020 Apr 7];10:104-13. Available from: http://www.jnsbm.org/text.asp?2019/10/2/104/262948
| Introduction|| |
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. Apparently, several marine bacterial pigments have demonstrated various biological activities such as antimicrobial, anticancer, and immunosuppressive activities. 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.
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. 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. 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|| |
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). 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. It was revealed that marine heterotrophic-pigmented bacteria count for 1.4% of the total microbial community. 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.
|Figure 1: Chemical structures of antibacterial pigment compounds of marine-pigmented bacteria|
Click here to view
|Table 2: Antibacterial activities of marine pigmented bacteria against different pathogenic and nonpathogenic bacteria|
Click here to view
A red-pigmented marine bacterium Pseudovibrio denitrificans Z143-1 isolated from an unidentified tunicate exhibited anti-Staphylococcus aureus activity. 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. A study also reported the strong growth inhibition activity by xanthophyll, a yellow pigment-producing Pseudoalteromonas piscicida, against S. aureus DSM 6672. 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. 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).
Significantly, purple-, red-, or yellow-pigmented Pseudoalteromonas were predominantly isolated from swabs of live or inert surfaces of different marine organisms in warmer waters. 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. The production of a diffusible brownish orange pigment by a marine luminous bacterium Vibrio campbellii has been related to either due to proteorhodopsin  or pyomelanin. 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.
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. Pyocyanin a blue-green pigment produced by a hot spring isolate Pseudomonas aeruginosa possessed potential antimycobacterial activity against Mycobacterium smegmatis and other pathogenic bacteria. 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. 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.
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. 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.
A yellow-pigmented marine bacterium, M. luteus, isolated from seawater revealed the potential antibacterial activity against Staphylococcus sp., Klebsiella sp., and Pseudomonas sp. 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. 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. 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. 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. 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|| |
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.
| Other Applications of Pigments|| |
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., 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.
| Conclusion|| |
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.
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.
| References|| |
Grossart HP, Thorwest M, Plitzko I, Brinkhoff T, Simon M, Zeeck A, et al.
Production of a blue pigment (Glaukothalin) by marine Rheinheimera
spp. Int J Microbiol 2009;2009:701735.
Soliev AB, Hosokawa K, Enomoto K. Bioactive pigments from marine bacteria: Applications and physiological roles. Evid Based Complement Alternat Med 2011;2011:670349.
Venil CK, Zakaria ZA, Ahmad WA. Bacterial pigments and their applications. Process Biochem 2013;48:1065-79.
Shindo K, Misawa N. New and rare carotenoids isolated from marine bacteria and their antioxidant activities. Mar Drugs 2014;12:1690-8.
Jafarzade M, Yahya NA, Shayesteh F, Usup G, Ahmad A. Influence of culture conditions and medium composition on the production of antibacterial compounds by marine Serratia
sp. WPRA3. J Microbiol 2013;51:373-9.
Ibrahim D, Nazari TF, Kassim J, Lim S. Prodigiosin – An antibacterial red pigment produced by Serratia marcescens
IBRL USM 84 associated with a marine sponge Xestospongia testudinaria
. J Appl Pharm Sci 2014;4:1-6.
Kim D, Lee JS, Park YK, Kim JF, Jeong H, Oh TK, et al.
Biosynthesis of antibiotic prodiginines in the marine bacterium Hahella chejuensis
KCTC 2396. J Appl Microbiol 2007;102:937-44.
Alihosseini F, Ju KS, Lango J, Hammock BD, Sun G. Antibacterial colorants: Characterization of prodiginines and their applications on textile materials. Biotechnol Prog 2008;24:742-7.
Lee JS, Kim YS, Park S, Kim J, Kang SJ, Lee MH, et al.
Exceptional production of both prodigiosin and cycloprodigiosin as major metabolic constituents by a novel marine bacterium, Zooshikella rubidus
S1-1. Appl Environ Microbiol 2011;77:4967-73.
Kawasaki T, Sakurai F, Hayakawa Y. A prodigiosin from the roseophilin producer Streptomyces griseoviridis
. J Nat Prod 2008;71:1265-7.
Bowman JP. Bioactive compound synthetic capacity and ecological significance of marine bacterial genus Pseudoalteromonas
. Mar Drugs 2007;5:220-41.
Sertan-de Guzman AA, Predicala RZ, Bernardo EB, Neilan BA, Elardo SP, Mangalindan GC, et al. Pseudovibrio denitrificans
strain Z143-1, a heptylprodigiosin-producing bacterium isolated from a Philippine tunicate. FEMS Microbiol Lett 2007;277:188-96.
Liang Y, Chen L, Ye X, Anjum K, Lian XY, Zhang Z, et al.
New streptophenazines from marine Streptomyces
sp. 182SMLY. Nat Prod Res 2017;31:411-7.
Liang Y, Xie X, Chen L, Yan S, Ye X, Anjum K, et al.
Bioactive polycyclic quinones from marine Streptomyces
sp. 182SMLY. Mar Drugs 2016;14:10.
Schneemann I, Kajahn I, Ohlendorf B, Zinecker H, Erhard A, Nagel K, et al.
Mayamycin, a cytotoxic polyketide from a Streptomyces
strain isolated from the marine sponge Halichondria panicea
. J Nat Prod 2010;73:1309-12.
Gromek SM, Suria AM, Fullmer MS, Garcia JL, Gogarten JP, Nyholm SV, et al. Leisingera
sp. JC1, a bacterial isolate from Hawaiian Bobtail Squid eggs, produces indigoidine and differentially inhibits vibrios. Front Microbiol 2016;7:1342.
Hakvåg S, Fjaervik E, Klinkenberg G, Borgos SE, Josefsen KD, Ellingsen TE, et al.
sp. from the sea surface microlayer of costal waters in Trøndelag, Norway. Mar Drugs 2009;7:576-88.
Nakamura Y, Asada C, Sawada T. Production of antibacterial violet pigment by psychrotropic bacterium RT102 strain. Biotechnol Bioprocess Eng 2003;8:37-40.
Yang LH, Xiong H, Lee OO, Qi SH, Qian PY. Effect of agitation on violacein production in Pseudoalteromonas luteoviolacea
isolated from a marine sponge. Lett Appl Microbiol 2007;44:625-30.
Yada S, Wang Y, Zou Y, Nagasaki K, Hosokawa K, Osaka I, et al.
Isolation and characterization of two groups of novel marine bacteria producing violacein. Mar Biotechnol (NY) 2008;10:128-32.
Vynne NG, Mansson M, Gram L. Gene sequence based clustering assists in dereplication of Pseudoalteromonas luteoviolacea
strains with identical inhibitory activity and antibiotic production. Mar Drugs 2012;10:1729-40.
Ambrožič Avguštin J, Žgur Bertok D, Kostanjšek R, Avguštin G. Isolation and characterization of a novel violacein-like pigment producing psychrotrophic bacterial species Janthinobacterium svalbardensis
sp. nov. Antonie Van Leeuwenhoek 2013;103:763-9.
Gram L, Melchiorsen J, Bruhn JB. Antibacterial activity of marine culturable bacteria collected from a global sampling of ocean surface waters and surface swabs of marine organisms. Mar Biotechnol (NY) 2010;12:439-51.
Shetty PR, Buddana SK, Tatipamula VB, Naga YV, Ahmad J. Production of polypeptide antibiotic from Streptomyces parvulus
and its antibacterial activity. Braz J Microbiol 2014;45:303-12.
Saha S, Thavasi R, Jayalakshmi S. Phenazine pigments from Pseudomonas aeruginosa
and their application as antibacterial agent and food colourants. Res J Microbiol 2008;3:122-8.
Vasanthabharathi V, Lakshminarayanan R, Jayalakshmi S. Melanin production from marine Streptomyces
. Afr J Biotechnol 2011;10:11224-34.
Isnansetyo A, Kamei Y. MC21-A, a bactericidal antibiotic produced by a new marine bacterium, Pseudoalteromonas phenolica
sp. nov. O-BC30(T), against methicillin-resistant Staphylococcus aureus
. Antimicrob Agents Chemother 2003;47:480-8.
Stafsnes M, Bruheim P. Pigmented marine heterotrophic bacteria. In: Kim SK, editor. Marine Biomaterials. Boca Raton: CRC Press; 2013. p. 117-48.
Maskey RP, Helmke E, Laatsch H. Himalomycin A and B: Isolation and structure elucidation of new fridamycin type antibiotics from a marine Streptomyces
isolate. J Antibiot (Tokyo) 2003;56:942-9.
Priya KA, Satheesh S, Ashokkumar B, Varalakshmi P, Selvakumar G, Sivakumar N. Antifouling activity of prodigiosin from estuarine isolate of Serratia marcescens
CMST 07. In: Velu RK, editor. Microbiological Research in Agroecosystem Management. Vol. 16. New Delhi: Springer; 2013. p. 11-21.
Porsby CH, Nielsen KF, Gram L. Phaeobacter
species of the roseobacter clade colonize separate niches in a Danish turbot (Scophthalmus maximus
)-rearing farm and antagonize Vibrio anguillarum
under different growth conditions. Appl Environ Microbiol 2008;74:7356-64.
Brinkhoff T, Bach G, Heidorn T, Liang L, Schlingloff A, Simon M, et al.
Antibiotic production by a Roseobacter
clade-affiliated species from the German Wadden sea and its antagonistic effects on indigenous isolates. Appl Environ Microbiol 2004;70:2560-5.
Bruhn JB, Nielsen KF, Hjelm M, Hansen M, Bresciani J, Schulz S, et al.
Ecology, inhibitory activity, and morphogenesis of a marine antagonistic bacterium belonging to the Roseobacter
clade. Appl Environ Microbiol 2005;71:7263-70.
Zahir I, Houari A, Ibnsouda S. Antibacterial effect of Pseudomonas aeruginosa
isolated from a Moroccan hot spring discharge and partial purification of its extract. Br Biotech J 2014;4:1123-40.
Wagner-Döbler I, Beil W, Lang S, Meiners M, Laatsch H. Integrated approach to explore the potential of marine microorganisms for the production of bioactive metabolites. Adv Biochem Eng Biotechnol 2002;74:207-38.
Du H, Jiao N, Hu Y, Zeng Y. Diversity and distribution of pigmented heterotrophic bacteria in marine environments. FEMS Microbiol Ecol 2006;57:92-105.
Radjasa OK, Limantara L, Sabdono A. Antibacterial activity of a pigment producing bacterium associated with Halimeda
sp. from land-locked marine lake Kakaban, Indonesia. J Coast Dev 2009;12:100-4.
Wang Z, O'Shaughnessy TJ, Soto CM, Rahbar AM, Robertson KL, Lebedev N, et al.
Function and regulation of Vibrio campbellii
proteorhodopsin: Acquired phototrophy in a classical organoheterotroph. PLoS One 2012;7:e38749.
Wang Z, Lin B, Mostaghim A, Rubin RA, Glaser ER, Mittraparp-Arthorn P, et al. Vibrio campbellii
HmgA-mediated pyomelanization impairs quorum sensing, virulence, and cellular fitness. Front Microbiol 2013;4:379.
Asencio G, Lavin P, Alegría K, Domínguez M, Bello H, González-Rocha G, et al
. Antibacterial activity of the Antarctic bacterium Janthinobacterium
sp. SMN 33.6 against multi-resistant gram-negative bacteria. Electron J Biotechnol 2014;17:1-5.
Leiva S, Alvarado P, Huang Y, Wang J, Garrido I. Diversity of pigmented gram-positive bacteria associated with marine macroalgae from Antarctica. FEMS Microbiol Lett 2015;362:fnv206.
Rameshkumar N, Nair S. Isolation and molecular characterization of genetically diverse antagonistic, diazotrophic red-pigmented vibrios from different mangrove rhizospheres. FEMS Microbiol Ecol 2009;67:455-67.
Umadevi K, Krishnaveni M. Antibacterial activity of pigment produced from Micrococcus luteus
KF532949. Int J Chem Anal Sci 2013;4:149-52.
Ramesh CH, Mohanraju R, Murthy KN, Karthick P. Molecular characterization of marine pigmented bacteria showing antibacterial activity. Indian J Mar Sci 2017;46:2081-7.
Pabba SK, Krishna G, Prakasham RS, Charya MA. Antibacterial activity of textile fabrics treated with red pigments from marine bacteria. J Mar Biosci 2015;1:11-9.
Ahmad WA, Ahmad WY, Zakaria Z, Yusof NZ. Application of Bacterial Pigments as Colorant: The Malaysian Perspective. Heidelberg: Springer; 2012. p. 57-74.
Venil CK, Aruldass CA, Dufossé L, Zakaria ZA, Ahmad WA. Current perspective on bacterial pigments: Emerging sustainable compounds with coloring and biological properties for the industry – An incisive evaluation. RSC Adv 2014;4:39523.
Akhoon BA, Singh KP, Karmakar M, Smita S, Pandey R, Gupta SK. Virtual screening and prediction of the molecular mechanism of bioactive compounds in silico
. In: Gupta VK, Tuohy MG, editors. Biotechnology of Bioactive Compounds. West Sussex: John Wiley & Sons, Ltd.; 2015. p. 371-94.
[Table 1], [Table 2]