Abstract
The effects of malachite green (MG) on the bacterial community in Antarctic soil were assessed. Culture-independent community analysis using 16S rRNA gene pyrosequencing showed that, in the presence of MG, the relative abundance of Pseudomonas dramatically increased from 2.2 % to 36.6 % (16.6-fold), and Pseudomonas became the predominant genus. The reduction in bacterial biodiversity was demonstrated by diversity indices and rarefaction curves. MG-degrading Pseudomonas sp. MGO was isolated from Antarctic soil. MG tolerance and decolorization activity were confirmed by growth, spectrophotometric, high-performance liquid chromatography, and thin-layer chromatography analyses in high MG concentrations. Our data showed that the decolorization process occurred via biodegradation, while biosorption also occurred after some time during the fed-batch decolorization process. Significant inductions in laccase, nicotinamide adenine dinucleotide–2,6 dichlorophenol indophenol reductase, and MG reductase activities suggested their involvement in the decolorization process. We also showed that the high tolerance of strain MGO to toxic MG might be mediated by upregulation of oxidative stress defense systems such as superoxide dismutase and protease. Collectively, these results demonstrated the response of the Antarctic soil bacterial community to MG and provided insight into the molecular mechanism of MG-tolerant Pseudomonas strains isolated from Antarctic soil.
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References
Alderman DJ (1985) Malachite green: review. J Fish Dis 8:289–298
Andersen SM, Johnsen K, Sørensen J, Nielsen P, Jacobsen CS (2000) Pseudomonas frederiksbergensis sp. nov., isolated from soil at a coal gasification site. Int J Syst Evol Microbiol 50:1957–1964
Bergwerff AA, Scherpenisse P (2003) Determination of residues of malachite green in aquatic animals. J Chromatogr B Analyt Technol Biomed Life Sci 788:351–359
Bianco MV, Blanco FC, Imperiale B, Forrellad MA, Rocha RV, Klepp LI, Cataldi AA, Morcillo N, Bigi F (2011) Role of P27-P55 operon from Mycobacterium tuberculosis in the resistance to toxic compounds. BMC Infec Dis 11:195
Chao (1987) Estimating the population size for capture-recapture data with unequal catchability. Biometrics 43:783–791
Chun J, Lee JH, Jung Y, Kim M, Kim S, Kim BK, Lim Y (2007) EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int J Syst Evol Microbiol 57:2259–2261
Clifton-Hadley RS, Alderman DJ (1987) The effects of malachite green upon proliferative kidney-disease. J Fish Dis 10:101–107
Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145
Corsolini S, Borghesi N, Ademollo N, Focardi S (2011) Chlorinated biphenyl and pesticides in migrating and resident seabirds from East and West Antarctica. Environ Int 37:1329–1335
Cowan DA, Chown SL, Convey P, Tuffin M, Hughes K, Pointing S, Vincent F (2011) Non-indigenous microorganisms in the Antarctic: assessing the risks. Trends Microbiol 19:540–548
Culp SJ, Beland FA (1996) Malachite green: a toxicological review. J Am Coll Toxicol 15:219–238
Deng D, Guo J, Zeng G, Sun G (2008) Decolorization of anthraquinone, triphenylmethane and azo dyes by a new isolated Bacillus cereus strain DC11. Int Biodeterior Biodegrad 62:263–269
DeSantis TZ, Hugenholtz P, Keller K, Brodie EL, Larsen N, Piceno YM, Phan R, Andersen GL (2006) NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes. Nucleic Acids Res 34:W394–W399
Dhamgaye S, Devaux F, Vandeputte R, Shah AH, Singh A, Blugeon C, Sanglard D, Prasad R (2012) In vitro effect of malachite green on Candida albicans involves multiple pathways and transcriptional regulators UPC2 and STP2. Antimicrob Agents Chemother 56:495–506
Ercolini D, Casaburi A, Nasi A, Ferrocino I, Di Monaco R, Ferranti P, Mauriello G, Villani F (2010) Different molecular types of Pseudomonas fragi have the same overall behavior as meat spoilers. Int J Food Microbiol 142:120–131
Felsenstein J (2002) PHYLIP (phylogeny inference package) version 3.6a. Department of Genetics, University of Washington, Seattle
Gao JF, Zhang Q, Wang JH, Wu XL, Wang SY, Peng YZ (2011) Contributions of functional groups and extracellular polymeric substances on the biosorption of dyes by aerobic granules. Bioresour Technol 102:805–813
Hale RC, Kim SL, Harvey E, La Guardia MJ, Mainor TM, Bush EO, Jacobs EM (2008) Antarctic research bases: local sources of polybrominated diphenyl ether (PBDE) flame retardants. Environ Sci Technol 42:1452–1457
Hatvani N, Mecs I (2001) Production of laccase and manganese peroxidase by Lentinus edodes on malt containing by product of the brewing process. Process Biochem 37:491–496
Hoffman GL, Meyer FP (1974) Parasites of freshwater fishes. TFH, New Jersey
Jadhav JP, Govindwar SP (2006) Biotransformation of malachite green by Saccharomyces cerevisiae MTCC 463. Yeast 23:315–323
Jadhav JP, Phugare SS, Dhanve RS, Jadhav SB (2010) Rapid biodegradation and decolorization of Direct Orange 39 (Orange TGLL) by an isolated bacterium Pseudomonas aeruginosa strain BCH. Biodegradation 21:453–463
Jang MS, Lee YM, Kim CH, Lee JH, Lee YC (2005) Triphenylmethane reductase from Citrobacter sp. strain KCTC18061P: purification, characterization, gene cloning, and overexpression of a functional protein in Escherichia coli. Appl Environ Microbiol 71:7955–7960
Jaraula CMB, Kenig F, Doran PT, Priscu JC, Welch KA (2009) Composition and biodegradation of a synthetic oil spilled on the perennial ice cover of Lake Fryxell, Antarctica. Environ Sci Technol 43:2708–2713
Jones JJ, Falkinham JO III (2003) Decolorization of malachite green and crystal violet by waterborne pathogenic mycobacteria. Antimicrob Agents Chemother 47:2323–2326
Kang YS, Kim YJ, Jeon CO, Park W (2006) Characterization of naphthalene-degrading Pseudomonas species isolated from pollutant-contaminated sites: oxidative stress during their growth on naphthalene. J Microbiol Biotechnol 16:1819–1825
Lee Y, Pena-Llopis S, Kang YS, Shin HD, Demple B, Madsen EL, Jeon CO, Park W (2006) Expression analysis of the fpr (ferredoxin-NADP + reductase) gene in Pseudomonas putida KT2440. Biochem Biophys Res Commun 339:1246–1254
Li LT, Hong Q, Yan X, Fang GH, Ali SW, Li SP (2009) Isolation of a malachite green-degrading Pseudomonas sp. MDB-1 strain and cloning of the tmr2 gene. Biodegradation 20:769–776
Liggett D, McIntosh A, Thomson A, Gilbert N, Storey B (2011) From frozen continent to tourism hotspot? Five decades of Antarctic tourism development and management, and a glimpse into the future. Tour Manage 32:357–366
Liu G, Zhou J, Wang J, Wang X, Jin R, Lv H (2011) Decolorization of azo dyes by Shewanella oneidensis MR-1 in the presence of humic acids. Appl Microbiol Biotechnol 97:417–424
Lopez NI, Pettinari MJ, Stackebrandt E, Tribelli PM, Põtter M, Steinbüchel A, Méndez BS (2009) Pseudomonas extremaustralis sp. nov., a poly(3-hydroxybutyrate) producer isolated from an Antarctic environment. Curr Microbiol 59:514–519
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275
Maalej-Kammoun M, Zouari-Mechichi H, Belbahri L, Woodward S, Mechichi T (2009) Malachite green decolourization and detoxification by the laccase from a newly isolated strain of Trametes sp. Int Biodet Biodeg 63:600–606
Michel VV, Labadie J, Hebraud M (1996) Effect of different temperature upshifts on protein synthesis by the psychrotrophic bacterium Pseudomonas fragi. Curr Microbiol 33:16–25
Murugesan K, Yang IH, Kim YM, Jeon JR, Chang YS (2009) Enhanced transformation of malachite green by laccase of Ganoderma lucidum in the presence of natural phenolic compounds. Appl Microbiol Biotechnol 82:341–350
Nawrocki EP, Eddy ER (2007) Query-dependent banding (QDB) for faster RNA similarity searches. PLoS Comput Biol 3:e56
Okere UV, Cabrerizo A, Dachs J, Jones KC, Semple KT (2012) Biodegradation of phenanthrene by indigenous microorganisms in soils from Livingstone Island, Antarctica. FEMS Microbiol Lett 329:69–77
Parsell DA, Lindquist S (1993) The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Ann Rev Genet 27:437–496
Parshetti G, Kalme S, Saratale G, Govindwar S (2006) Biodegradation of malachite green by Kocuria rosea MTCC 1532. Acta Chim Slov 53:492–498
Pearce CI, Christie R, Boothman C, von Canstein H, Guthrie JT, Lloyd JR (2006) Reactive azo dye reduction by Shewanella strain J18 143. Biotechnol Bioeng 95:692–703
Reddy GS, Matsumoto GI, Schumann P, Stackebrandt E, Shivaji S (2004) Psychrophilic pseudomonads from Antarctica: Pseudomonas antarctica sp. nov., Pseudomonas meridiana sp. nov. and Pseudomonas proteolytica sp. nov. Int J Syst Evol Microbiol 54:713–719
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Schnick RA (1988) The impetus to register new therapeutants for aquaculture. Prog Fish-Cult 50:190–196
Shannon CE, Weaver W (1963) The mathematical theory of communication. University of Illinois Press, Urbana
Srivastava S, Sinha R, Roy D (2004) Toxicological effects of malachite green. Aquat Toxicol 66:319–329
Stanier RY, Palleroni NJ, Doudoroff M (1966) The aerobic pseudomonads: a taxonomic study. J Gen Microbiol 43:159–271
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Telke AA, Kalyani DC, Dawkar VV, Govindwar SP (2009) Influence of organic and inorganic compounds on oxidoreductive decolorization of sulfonated azo dye C.I. Reactive Orange 16. J Hazard Mater 172:298–309
Telke AA, Joshi SM, Jadhav SU, Tamboli DP, Govindwar SP (2010) Decolorization and detoxification of Congo red and textile industry effluent by an isolated bacterium Pseudomonas sp. SU-EBT. Biodegradation 21:283–296
Thamban M, Thakur RC (2012) Trace metal concentrations of surface snow from Ingrid Christensen Coast, East Antarctica—spatial variability and possible anthropogenic contributions. Environ Monit Assess DOI:. doi:10.1007/s10661-012-2764-0
Yatome C, Ogawa T, Koga D, Idaka E (1981) Biodegradation of azo and triphenylmethane dye by Pseudomonas pseudomallei 13 NA. J Soc Dyers Colour 97:166–168
Yatome C, Yamada S, Ogawa T, Matsui M (1993) Degradation of crystal violet by Nocardia coralline. Appl Microbiol Biotechnol 38:565–569
Acknowledgment
This work was supported by a grant (2012-0005277) from the MEST/NRF program. Dr. W. Park was supported by the LG Yonam Foundation, Seoul, South Korea.
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Jung, J., Seo, H., Lee, S.H. et al. The effect of toxic malachite green on the bacterial community in Antarctic soil and the physiology of malachite green-degrading Pseudomonas sp. MGO. Appl Microbiol Biotechnol 97, 4511–4521 (2013). https://doi.org/10.1007/s00253-012-4669-9
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DOI: https://doi.org/10.1007/s00253-012-4669-9