Towards an understanding of bacterial metabolites prodigiosin and violacein and their potential for use in commercial sunscreens

International Journal of Cosmetic Science

Volumn 37, Issue 1, 2015, Pages 98-107

  Suryawanshi, R K ^a   Patil, C D ^a   Borase, H P ^a   Narkhede, C P ^a   Stevenson, A ^b   Hallsworth, J E ^b   Patil, S V ^a  

^a NORTH MAHARASHTRA UNIVERSITY   (India)

^b QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

bacterial pigments; Escherichia coli; natural skin care products; Staphylococcus aureus; UV protection

Indexed keywords

ALOE VERA EXTRACT; ANTIOXIDANT; ASCORBIC ACID; CUCUMIS SATIVUS EXTRACT; PIGMENT; PLANT EXTRACT; PRODIGIOSIN; REACTIVE OXYGEN METABOLITE; SKIN PROTECTIVE AGENT; STREPTOMYCIN; SUNSCREEN; UNCLASSIFIED DRUG; VIOLACEIN; INDOLE DERIVATIVE;

ALOE VERA; ANTIBACTERIAL ACTIVITY; ANTIMICROBIAL ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; CHROMOBACTERIUM VIOLACEUM; CONTROLLED STUDY; CUCUMBER; ESCHERICHIA COLI; GROWTH INHIBITION; HUMAN; IC50; INFRARED SPECTROSCOPY; MACROMOLECULE; MICROBIAL DIVERSITY; NONHUMAN; OXIDATIVE STRESS; PLANT LEAF; SERRATIA MARCESCENS; SKIN PROTECTION; STAPHYLOCOCCUS AUREUS; ULTRAVIOLET SPECTROPHOTOMETRY; BACTERIUM; METABOLISM;

BACTERIA; INDOLES; PRODIGIOSIN; SUNSCREENING AGENTS;

EID: 84921286816     PISSN: 01425463     EISSN: 14682494     Source Type: Journal    
DOI: 10.1111/ics.12175     Document Type: Article

References (81)

1. Randazzo, C.L., Pitino, I., Ribbera, A., and, Caggia, C., Pecorino Crotonese cheese: study of bacterial population and flavour compounds. Food Microbiol. 27, 363-374 (2009).
2. Cray, J.A., Bell, A.N.W., Bhaganna, P., Mswaka, A.Y., Timson, D.J., and, Hallsworth, J.E., The biology of habitat dominance; can microbes behave as weeds? Microb. Biotechnol. 6, 453-492 (2013).
3. Lievens, B., Hallsworth, J.E., Belgacem, Z.B., Pozo, M.I., Stevenson, A., Willems, K.A., and, Jacquemyn, H., Microbiology of sugar-rich environments, diversity, ecology, and system constraints. Environ. Microbiol. (2014). In press doi: 10.1111/1462-2920.12570.
4. Lee, H.K., Chun, J., Moon, E.Y., Ko, S.H., Lee, D.S., Lee, H.S., and, Bae, K.S., Hahella chejuensis gen. nov, sp. nov., an extracellular-polysaccharide-producing marine bacterium. Int. J. Syst. Evol. Microbiol. 51, 661-666 (2001).
5. Nobutaka, S., Masami, N., Kazuyuki, H., Tadaaki, H., and, Katsumi, A., Synergistic antifungal activity of chitinolytic enzymes and prodigiosin produced by biocontrol bacterium, Serratia marcescens strain B2 against gray mold pathogen, Botrytis cinerea. J. Gen. Plant Pathol. 67, 312-319 (2001).
6. Kim, S.J., Lee, H.K., Lee, Y.K., and, Yim, J.H., Mutant selection of Hahella chejuensis KCTC 2396 and statistical optimization of medium components for prodigiosin yield-up. J. Microbiol. 46, 183-188 (2008).
7. Starič, N., Danevčič, T., and, Stopar, D., Vibrio sp. DSM 14379 pigment production-a competitive advantage in the environment? Microb. Ecol. 60, 592-598 (2010).
8. Gulani, C., Bhattacharya, S., and, Das, A., Assessment of process parameters influencing the enhanced production of prodigiosin from Serratia marcescens and evaluation of its antimicrobial, antioxidant and dyeing potentials. Malays. J. Microbiol. 18, 116-122 (2012).
9. Maverakis, E., Miyamura, Y., Bowen, M.P., Correa, G., Ono, Y., and, Goodarzi, H., Light, including ultraviolet. J. Autoimmun. 34, J247-J257 (2010).
10. Nichols, J.A., and, Katiyar, S.K., Skin photoprotection by natural polyphenols, anti-inflammatory antioxidant and DNA repair mechanisms. Arch. Dermatol. Res. 302, 71-83 (2010).
11. Galvez, M.V., Antioxidants in photoprotection: do they really work? Actas Dermosifiliogr 101, 197-200 (2010).
12. Balogh, T.S., Velasco, M.V., Pedriali, C.A., Kaneko, T.M., and, Baby, A.R., Ultraviolet radiation protection, current available resources in photoprotection. An. Bras. Dermatol. 86, 732-742 (2011).
13. Jiang, R., Roberts, M.S., Collins, D.M., and, Benson, H.A., Absorption of sunscreens across human skin, an evaluation of commercial products for children and adults. Br. J. Clin. Pharmacol. 48, 635-637 (1999).
14. Kutting, B., Baumeister, T., Weistenhöfer, W., Pfahlberg, A., Uter, W., and, Drexler, H., Effectiveness of skin protection measures in prevention of occupational hand eczema: results of a prospective randomized controlled trial over a follow-up period of 1 year. Br. J. Dermatol. 162, 362-370 (2010).
15. Sharma, V., Shukla, R.K., Saxena, N., Parmar, D., Das, M., and, Dhawan, A., DNA damaging potential of zinc oxide nanoparticles in human epidermal cells. Toxicol. Lett. 185, 211-218 (2009).
16. Suryawanshi, R.K., Patil, C.D., Borase, H.P., Salunke, B.K., and, Patil, S.V., Studies on production and biological potential of prodigiosin by Serratia marcescens. Appl. Biochem. Biotechnol. 173, 1209-1221 (2014).
17. Mansur, J.S., Breder, M.N., Mansur, M.C., and, Azulay, R.D., Determination of Sun protection factor by spectrophotometry. An. Bras. Dermatol. 61, 121-124 (1986).
18. Sayre, R.M., Agin, P.P., Levee, G.J., and, Marlowe, E., A comparison of in vivo and in vitro testing of sunscreen formulas. Photochem. Photobiol. 29, 559-566 (1979).
19. Borase, H.P., Patil, C.D., Suryawanshi, R.K., and, Patil, S.V., Ficus carica latex-mediated synthesis of silver nanoparticles and its application as a chemophotoprotective agent. Appl. Biochem. Biotechnol. 171, 676-688 (2013).
20. Yim, J.H., Kim, S.J., Aan, S.H., and, Lee, H.K., Physiochemical and rheological properties of a novel emulsifier, EPS-R, produced by the marine bacterium Hahella chejuensis. Biotechnol. Bioprocess Eng. 9, 405-413 (2004).
21. Jeong, H., Yim, J.H., Lee, C., et al,. Genomic blueprint of Hahella chejuensis, a marine microbe producing an algicidal agent. Nucleic Acids Res. 33, 7066-7073 (2005).
22. Kim, D., Lee, J.S., Park, Y.K., et al,. Biosynthesis of antibiotic prodiginines in the marine bacterium Hahella chejuensis KCTC 2396. J. Appl. Microbiol. 102, 937-944 (2007).
23. Hejazi, A., and, Falkiner, F.R., Serratia marcescens. J. Med. Microbiol. 46, 903-912 (1997).
24. Williams, R.P., Gott, C.L., Quadri, S.M.H., and, Scott, R.H., Influence of temperature of incubation and type of growth media on pigmentation in Serratia marcescens. J. Bacteriol. 106, 438-443 (1971).
25. Hardjito, L., Huq, A., and, Colwell, R.R., The influence of environmental conditions on the production of pigment by Serratia marcescens. Biotechnol. Bioprocess Eng. 7, 100-104 (2002).
26. Giri, A.V., Anandkumar, N., Muthukumaran, G., and, Pennathur, G., A novel medium for the enhanced cell growth and production of prodigiosin from Serratia marcescens isolated from soil. BMC Microbiol. 4, 11 (2004).
27. Salisbury, W.A., and, Likos, J.J., Hydrolysis of casein: a differential aid for the identification of Serratia marcescens. J. Clin. Pathol. 25, 1083-1085 (1972).
28. Cray, J.A., Houghton, J.D.R., Cooke, L.R., and, Hallsworth, J.E., A simple inhibition coefficient for quantifying potency of biocontrol agents against plant-pathogenic fungi. Biol. Control. In press
29. Aucken, H.M., and, Pitt, T.L., Antibiotic resistance and putative virulence factors of Serratia arcescens with respect to O and K serotypes. J. Med. Microbiol. 47, 1105-1113 (1998).
30. Thomson, N.R., Crow, M.A., McGowan, S.J., Cox, A., and, Salmond, G.P., Biosynthesis of carbapenem antibiotic and prodigiosin pigment in Serratia is under quorum sensing control. Mol. Microbiol. 36, 539-556 (2000).
31. Heineman, A.J., Howard, H.Y., and, Palocz, H.J., Influence of dissolved oxygen levels on production of L-asparaginase and prodiogiosin by Serratia marcescens. Appl. Microbiol. 19, 800-804 (1970).
32. Cang, S., Sanada, M., Johdo, O., Ohta, S., Nagamatsu, Y., and, Yoshimoto, A., High production of prodigiosin by Serratia marcescens grown on ethanol. Biotechnol. Lett. 22, 1761-1765 (2000).
33. Haddix, P.L., Jones, S., Patel, P., Burnham, S., Knights, K., Powell, J.N., and, LaForm, A., Kinetic analysis of growth rate, ATP, and pigmentation suggests an energy-spilling function for the pigment prodigiosin of Serratia marcescens. J. Bacteriol. 190, 7453-7463 (2008).
34. Stevenson, A., and, Hallsworth, J.E., Water and temperature relations of soil Actinobacteria. Environ. Microbiol. Rep. (2014). In press doi: 10.1111/1758-2229.12199
35. Oren, A., and, Hallsworth, J.E., Microbial weeds in saline habitats: the enigma of the weed-like Haloferax mediterranei. FEMS Microbiol. Lett. 359, 134-142 (2014). doi: 10.1111/1574-6968.12571.
36. Sevcikova, B., and, Kormanec, J., Differential production of two antibiotics of Streptomyces coelicolor A3 (2), actinorhodin and undecylprodigiosin, upon salt stress conditions. Arch. Microbiol. 181, 384-389 (2004).
37. Yamazaki, G., Nishimura, S., Ishida, A., et al,. Effect of salt stress on pigment production of Serratia rubidaea N-1: a potential indicator strain for screening quorum sensing inhibitors from marine microbes. J. Gen. Appl. Microbiol. 52, 113-117 (2006).
38. Burger, S.R., and, Bennet, J.W., Droplet enrichment factors of pigmented and non pigmented Serratia marcescens, Possible selective function for prodigiosin. Appl. Environ. Microbiol. 50, 487-490 (1985).
39. Boric, M., Danevčič, T., and, Stopar, D., Prodigiosin from Vibrio sp. DSM 14379; a new UV-protective pigment. Microb. Ecol. 62, 528-536 (2011).
40. D'Aoust, J.Y., and, Kushner, D.J., Vibrio psychroerythrus sp. n.: classification of the psychrophilic marine bacterium, NRC 1004. J. Bacteriol. 111, 340-342 (1972).
41. Chin, J.P., Megaw, J., Magill, C.L., et al,. Solutes determine the temperature windows for microbial survival and growth. Proc. Natl Acad. Sci. USA 107, 7835-7840 (2010).
42. Methé, B.A., Nelson, K.E., Deming, J.W., et al,. The psychrophilic lifestyle as revealed by the genome sequence of Colwellia psychrerythraea 34H through genomic and proteomic analyses. Proc. Natl Acad. Sci. USA 102, 10913-10918 (2005).
43. Farmer, J.J. 3rd, Hickman-Brenner, F.W., Fanning, G.R., Gordon, C.M., and, Brenner, D.J., Characterization of Vibrio metschnikovii and Vibrio gazogenes by DNA-DNA hybridization and phenotype. J. Clin. Microbiol. 26, 1993-2000 (1988).
44. Shieh, W.Y., Chen, Y.W., Chaw, S.M., and, Chiu, H.H., Vibrio ruber sp. nov., a red, facultatively anaerobic, marine bacterium isolated from sea water. Int. J. Syst. Evol. Microbiol. 53, 479-484 (2003).
45. Kumar, N.R., and, Nair, S., Vibrio rhizosphaerae sp. nov., a red-pigmented bacterium that antagonizes phytopathogenic bacteria. Int. J. Syst. Evol. Microbiol. 57, 2241-2246 (2007).
46. Koburger, J.A., and, May, S.O., Isolation of Chromobacterium spp. from foods, soil and water. Appl. Environ. Microbiol. 44, 1463-1465 (1982).
47. Duran, N., and, Menck, C.F., Chromobacterium violaceum, a review of pharmaceutical and industrial perspectives. Crit. Rev. Microbiol. 27, 201-222 (2001).
48. Sneath, P.H.A., Cultural and biochemical characteristics of the genus Chromobacterium. J. Gen. Microbiol. 15, 70-98 (1956).
49. Streichsbier, F., Utilization of chitin as sole carbon and nitrogen source by Chromobacterium violaceum. FEMS Microbiol. Lett. 19, 129-132 (1983).
50. Chernin, L.S., Winson, M.K., Thompson, J.M., et al,. Chitinolytic activity in Chromobacterium violaceum: substrate analysis and regulation by quorum sensing. J. Bacteriol. 180, 4435-4441 (1998).
51. Konzen, M., De Marco, D., Cordova, C.A., Vieira, T.O., Antônio, R.V., and, Creczynski-Pasa, T.B., Antioxidant properties of violacein: possible relation on its biological function. Bioorg. Med. Chem. 14, 8307-8313 (2006).
52. Matz, C., Deines, P., Boenigk, J., Ardnt, H., Eberl, L., Kjelleberg, S., and, Jürgens, K., Impact of violacein-producing bacteria on survival and feeding of bacterivorous nanoflagellates. Appl. Environ. Microbiol. 70, 1593-1599 (2004).
53. Deines, P., Matz, C., and, Jürgens, K., Toxicity of violacein-producing bacteria fed to bacterivorous freshwater plankton. Limnol. Oceanogr. 54, 1343-1352 (2009).
54. Lichstein, H.C., and, Van De Sand, V.F., Violacein, an antibiotic pigment produced by Chromobacterium violaceum. J. Infect. Dis. 76, 47-51 (1945).
55. Eneroth, A., Ahrnè, S., and, Molin, G., Contamination routes of Gram-negative spoilage bacteria in the production of pasteurised milk, evaluated by randomly amplified polymorphic DNA (RAPD). Int. Dairy J. 10, 325-331 (2000).
56. Pantanella, F., Berlutti, F., Passariello, C., Sarli, S., Morea, C., and, Schippa, S., Violacein and biofilm production in Janthinobacterium lividum. J. Appl. Microbiol. 102, 992-999 (2007).
57. Brucker, R.M., Harris, R.N., Schwantes, C.R., Gallaher, T.N., Flaherty, D.C., Lam, B.A., and, Minbiole, K.P., Amphibian chemical defense, antifungal metabolites of the microsymbiont Janthinobacterium lividum on the salamander Plethodon cinereus. J. Chem. Ecol. 34, 1422-1429 (2008).
58. Da Silva, N., Taniwaki, M.H., Junqueira, V.C.A., Silveira, N.F.A., do Nascimento, M.S., and, Gomes, R.A.R., Pseudomonas. In: Microbiological Examination Methods of Food and Water-A Laboratory Manual, Ch. 17 (, Da Silva, N., Taniwaki, M.H., Junqueira, V.C.A., Silveira, N.F.A., do Nascimento, M.S., and, Gomes, R.A.R., eds.), pp. 181-196. Taylor and Francis Group, London (2013).
59. Patijanasoontorn, B., Boonma, P., Wilailackana, C., et al,. Hospital acquired Janthinobacterium lividum septicemia in Srinagarind Hospital. J. Med. Assoc. Thai. 12, 6-10 (2000).
60. Antonio, R.V., and, Creczynski-Pasa, T.B., Genetics analysis of violacein biosynthesis by Chromobacterium violaceum. Genet. Mol. Res. 3, 85-91 (2004).
61. Stevenson, A., Cray, J.A., Williams, J.P., et al,. Is there a common water activity for the three Domains of life? ISME J. (2014). In press.
62. Stevenson, A., Burkhardt, J., Cockell, C.S., et al,. Multiplication of microbes below 0.690 water activity: implications for terrestrial and extraterrestrial life. Environ. Microbiol. (2014) doi: 10.1111/1462-2920.12598.
63. Hallsworth, J.E., Nomura, Y., and, Iwahara, M., Ethanol-induced water stress and fungal growth. J. Ferment. Bioeng. 86, 451-456 (1998).
64. Bhaganna, P., Volkers, R.J.M., Bell, A.N.W., Kluge, K., Timson, D.J., McGrath, J.W., and, Hallsworth, J.E., Hydrophobic substances induce water stress in microbial cells. Microb. Biotechnol. 3, 701-716 (2010).
65. McCammick, E.M., Gomase, V.S., Timson, D.J., McGenity, T.J., and, Hallsworth, J.E., Water-hydrophobic compound interactions with the microbial cell. In: Handbook of Hydrocarbon and Lipid Microbiology-Hydrocarbons, Oils and Lipids, Diversity, Properties and Formation (, Timmis, K.N., ed.), Vol. 2, pp. 1451-1466. Springer, New York (2010).
66. Hallsworth, J.E., Heim, S., and, Timmis, K.N., Chaotropic solutes cause water stress in Pseudomonas putida. Environ. Microbiol. 12, 1270-1280 (2003).
67. 2-containing environments: chaotropicity defines the window. Environ. Microbiol. 9, 803-813 (2007).
68. Yakimov, M.M., La Cono, V., La Spada, G., et al,. Microbial community of seawater-brine interface of the deep-sea brine Lake Kryos as revealed by recovery of mRNA are active below the chaotropicity limit of life. Environ. Microbiol. (2014). DOI: 10.1111/1462-2920.12587.
69. Cray, J.A., Russell, J.T., Timson, D.J., Singhal, R.S., and, Hallsworth, J.E., A universal measure of chaotropicity and kosmotropicity. Environ. Microbiol. 15, 287-296 (2013).
70. Rummel, J.D., Beaty, D.W., Jones, M.A., et al,. A new analysis of Mars 'Special Regions', findings of the second MEPAG Special Regions Science Analysis Group (SR-SAG2). Astrobiology (2014). In press.
71. Song, M.J., Bae, J., Lee, D.S., Kim, C.H., Kim, J.S., Kim, S.W., and, Hong, S.I., Purification and characterization of prodigiosin produced by integrated bioreactor from Serratia sp. KH-95. J. Biosci. Bioeng. 101, 157-161 (2006).
72. Yen, G.C., Duh, P.D., and, Tsai, H.L., Antioxidant and pro-oxidant properties of ascorbic acid and gallic acid. Food Chem. 79, 307-313 (2002).
73. +)-ATPase by prodigiosins. Biochem. Pharmacol. 60, 1855-1863 (2000).
74. - symporters that uncouple proton translocators. J. Biol. Chem. 273, 21455-21462 (1998).
75. Bromberg, N., Justo, G.Z., Haun, M., Durán, N., and, Ferreira, C.V., Violacein cytotoxicity on human blood lymphocytes and effect on phosphatases. J. Enzym. Inhib. Med. Chem. 20, 449-454 (2005).
76. De Carvalho, D.D., Costa, F.T., Duran, N., and, Haun, M., Cytotoxic activity of violacein in human colon cancer cells. Toxicol. In Vitro 20, 1514-1521 (2006).
77. Hallsworth, J.E., Ethanol-induced water stress in yeast. J. Ferment. Bioeng. 85, 125-137 (1998).
78. Murali, N.S., and, Teramura, A.H., Intraspecific difference in Cucumis sativus sensitivity to ultraviolet-B radiation. Physiol. Plant. 68, 673-677 (1986).
79. Ray, A., Gupta, S.D., and, Ghosh, S., Evaluation of anti-oxidative activity and UV absorption potential of the extracts of Aloe vera L. gel from different growth periods of plants. Ind. Crops Prod. 49, 712-719 (2013).
80. Schalka, S., and, Reis, V.M., Sun protection factor, meaning and controversies. An. Bras. Dermatol. 86, 507-515 (2011).
81. Latha, M.S., Martis, J., Shobha, V., et al,. Sunscreening agents, a review. J. Clin. Aesthet. Dermatol. 6, 16-26 (2013).