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A Salt Lake Extremophile, Paracoccus Bogoriensis Sp. Nov., Efficiently Produces Xanthophyll Carotenoids

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A Salt Lake Extremophile, Paracoccus Bogoriensis Sp. Nov., Efficiently Produces Xanthophyll Carotenoids African Journal of Microbiology Research Vol. 3(8) pp. 426-433 August, 2009 Available online http://www.academicjournals.org/ajmr ISSN 1996-0808 ©2009 Academic Journals Full Length Research Paper A salt lake extremophile, Paracoccus bogoriensis sp. nov., efficiently produces xanthophyll carotenoids George O. Osanjo1*, Elizabeth W. Muthike2, Leah Tsuma3, Michael W. Okoth2, Wallace D. Bulimo3, Heinrich Lünsdorf4, Wolf-Rainer Abraham4, Michel Dion5, Kenneth N. Timmis4 , Peter N. Golyshin4 and Francis J. Mulaa3 1School of Pharmacy, University of Nairobi, P. O. Box 30197-00100, Nairobi, Kenya. 2Department of Food Science, Technology and Nutrition, University of Nairobi, P.O. Box 30197-00100, Nairobi, Kenya. 3Department of Biochemistry, University of Nairobi, P. O. Box 30197-00100, Nairobi, Kenya. 4Division of Microbiology, Helmholtz Centre for Infection Research, Inhoffenstrasse 7, D-38124 Braunschweig, Germany. 5Université de Nantes, UMR CNRS 6204, Biotechnologie, Biocatalyse, Biorégulation, Faculté des Sciences et des Techniques, 2, rue de la Houssinière, BP 92208, Nantes, F- 44322, France. Accepted 27 July, 2009 A Gram-negative obligate alkaliphilic bacterium (BOG6T) that secretes carotenoids was isolated from the outflow of Lake Bogoria hot spring located in the Kenyan Rift Valley. The bacterium is motile by means of a polar flagellum, and forms red colonies due to the production of xanthophyll carotenoid pigments. 16S rRNA gene sequence analysis showed this strain to cluster phylogenetically within the genus Paracoccus. Strain BOG6T is aerobic, positive for both catalase and oxidase, and non- methylotrophic. The major fatty acid of the isolate is C18: 1ω7c. It accumulated polyhydroxybutyrate granules. Strain BOG6T gave astaxanthin yield of 0.4 mg/g of wet cells indicating a potential for application in commercial production of carotenoids. On the basis of its genotypic characteristics, fatty acid composition and physiological reaction profiles, it is proposed that the isolate may be assigned to the genus Paracoccus as Paracoccus bogoriensis sp. nov. The type strain is BOG6T (=DSM16578 =LMG22798). The GenBank 16S rDNA nucleotide sequence accession number is AJ580352. Key words: Paracoccus bogoriensis, alpha-proteobacteria, alkaliphile, xanthophylls, astaxanthin, extremophile, carotenoids. INTRODUCTION Xanthophylls are C40 oxygenated carotenoid pigments used in fish aquaculture to impart pleasant colours to that are synthesised de novo by a wide variety of plants, salmon and trout (Jacobson et al., 2003; Lorenz and bacteria and archaea but not by animals (Johnson and Cysewski, 2000). It is also the natural pigment for some Schroeder, 1995; Ong and Tee, 1992). Xanthophylls varieties of tilapia. It is marketed as a nutritional supple- have considerable interest due to their widespread use in ment for humans (Guerin et al., 2003). Biological the food, nutraceutical and pharmaceutical industries activities of astaxanthin in humans include potentiation of (Borowitzka, 1988; Dufossé, 2006). The hydroxy ketoca- the immune system (Bendich, 1989; Jynouchi et al., rotenoid astaxanthin (3, 3‘- dihydroxy-, ‘-carotene-4, 4‘- 1995) and suppression of certain cancers (Palozza et al., dione) is a potent biological antioxidant with stronger 2009; Miyashita, 2009). Commercially, xanthophllys are antioxidant activity than –carotene and Vitamin E produced from microorganisms such as the red yeast (Johnson and An, 1991). Astaxanthin is used in fish Phaffia rhodozyma and the green algae Haematococcus pluvialis (Nelis and Leenher, 1991) as well as by chemical synthesis. However the current sources are not able to satisfy world demand, hence the need to search for *Corresponding author. E-mail: [email protected]. Tel.: alternative sources. Some bacteria that belong to the genus +254 721 794 666. Paracoccus sp. are known to secrete astaxanthin and are Osanjo et al. 427 are under patent protection. MATERIALS AND METHODS More than 20 species of the genus Paracoccus have Isolation and growth conditions been described in literature (Kelly et al., 2006a, 2006b). The most highly studied member of the genus is Para- Water and soil samples were taken from the out-flow of the hot coccus denitrificans, first described by Beijeirinck and springs of Lake Bogoria (0° 22’S and 36° 05’E), inoculated over- Minkman (1910) as Micrococcus denitrificans and later night at 37°C in a modified Horikoshi (MH) medium (Horikoshi and Akiba, 1982) made up of yeast extract 5 gl-1; peptone 5 gl-1; glucose renamed by Davis et al. (1969). The genome of P. denitri- -1 -1 -1 -1 2 gl ; KH2PO4 1 gl ; MgSO4.7H2 O 0.2 gl ; agar 15 g l ; Na2CO3 ficans was sequenced in 2004. It is not known to produce -1 -1 (7.5% w/v) 40 ml l ; Trace elements (SL 10) 1 ml l . Colonies were carotenoids. further isolated on the same medium. Strain BOG6T, which formed Paracoccus species are Gram negative, catalase- bright red colonies was selected for further analysis. Unless other- positive, oxidase-positive bacteria that contain C18: 17c wise stated, strain BOG6T was routinely grown on a modified as a major component of the cellular fatty acids and are Horikoshi (MH) medium at 37°C. metabolically versatile (Kelly et al., 2006b). Members of the species that have been shown to produce caro- Phylogenetic analysis and G+C content of the DNA tenoids, and are under intellectual property protection include: P. carotinifaciens, P. marcusii, P. zeaxanthinifa- Genomic DNA was prepared as described in Golyshina et al. ciens and P. haeundaensis (Berry et al., 2003; (2000). The 16S rDNA was amplified using the primer pair F27 (5’- AGAGTTTGATCCTGGCTCAG-3’) and R1492 (5’- Hirschberg and Harker, 1999; Tsubokura et al., 1999a, TACGGYTACCTTACGACTT-3’) that amplifies bacterial 16S rDNA Lee et al., 2004). from position 27 to 1492 in the E. coli numbering system. The The Paracoccus have been isolated from diverse envi- primers were supplied by MWG Biotech, Ebersberg, Germany. The ronments such as soil, sludge and sea water. Lake PCR amplifications were done under the conditions described pre- Bogoria, the site of isolation of strain BOG6T, is an viously (Yakimov et al., 1998, Golyshina et al., 2000). The amplifi- alkaline-saline, Athalassic lake located in the Kenyan Rift cation products were purified from agarose gel using the QIAXEX II 2 extraction kit (Qiagen) using the manufacturer’s protocol. Purified Valley. It covers an area of 20 km and its pH ranges 16S rDNA was sequenced directly in an Applied Biosystems 373A from 9 - 11 while the lake temperature fluctuates between DNA Sequencer using Thermus aquaticus (Taq) DNA polymerase 30 - 90°C depending on the site. The alkalinity is due to with the PCR primers (F27 and R1492) in the forward and reverse its unique geochemistry. It lies in a closed basin that was directions, and the Perkin-Elmer fluorescent dye-labelled dideoxy- created by a tilt faulting. The predominant bedrock is nucleotides (Perkin-Elmer, USA). The reactions were incubated in a alkaline trachyte lavas of the lower Pleistocene era. Perkin-Elmer thermocycler, and after removal of excess primers the fluorescent labeled fragment sets were resolved by electrophoresis Evaporation and leaching causes concentration of salts in the ABI 373A automatic sequencer and bases called by the pro- particularly sodium carbonate (McCall, 1967; Grant et al., gram ABI Sequence Analysis Software v3.3 for Macintosh (Apple 1990). The large temperature variation is due to the hot Inc, USA). springs and geysers that dot its shores and emit their The sequence was added to an alignment of homologous bacte- outflow into the lake. rial 16S rDNA primary structures using the MUSCLE program (Edgar, 2004). Phylogenetic analyses were performed using MEGA Our investigations were conducted in a bioprospecting software, version 4.0 (Tamura et al., 2007) with distance-based effort to find new and robust biocatalysts and secondary neighbour-joining, maximum-parsimony and maximum-likelihood metabolites from microorganisms of the Kenyan soda methods (Felstein, 1985; Saitou and Nei, 1987; Tamura et al., lakes. The hot springs of Lake Bogoria were chosen for 2004). Confidence in the topology obtained from these analyses their high temperature and pH. Thus this environment was gauged using bootstrap resampling methods in MEGA soft- was deemed to provide a unique habitat for isolation of ware, version 4.0 and included 1000 replications. Bayesian analysis was completed using MRBAYES, version 3.1.2. (Ronquist and thermohalotolerant alkaliphiles. Huelsenbeck, 2001) using four-chain Metropolis-coupled Markov The purpose of this paper is to establish that isolate Chain Monte Carlo (MCMCMC) analysis. The general time- T BOG6 produces carotenoids of industrial interest, and reversible model of nucleotide evolution was used with an assump- further to describe its taxonomic position. A taxonomic tion of a discrete gamma distribution (GTR+I+C). Trees were approach encompassing morphological and metabolic sampled every 1000 generations for a total of 1 000 000 trees. The properties and molecular methods was employed to cha- first 1000 trees were deleted as the ‘burn-in’ of the chain. The log- T likelihood scores of sample points against generation time were racterise the isolate BOG6 . For construction of phylo- plotted using TRACER software, version 1.4.1 (available at genetic trees, the 16S ribosomal RNA (rRNA) gene http://tree.bio.ed.ac.uk/software/tracer/) to ensure stationarity was sequence was used. 16S rRNA is classically used in achieved. Trees and
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