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Genomic Analysis of Chromohalobacter Salexigens: Clues About Its Carbon Metabolism and the Nature of Its Halophilic Properties

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Genomic Analysis of Chromohalobacter Salexigens: Clues About Its Carbon Metabolism and the Nature of Its Halophilic Properties Genomic analysis of Chromohalobacter salexigens: clues about its carbon metabolism and the nature of its halophilic properties Aharon Oren1, Laszlo N. Csonka2, Frank Larimer3, Paul Richardson4, Alla Lapidus 4, Bradley W. Goodner5 and Adam D. Ewing5 1 The Hebrew University of Jerusalem, Jerusalem, Israel; 2 Purdue University, West Lafayette IN, USA; 3 Oak Ridge National Laboratory, Oak Ridge TN, USA; 4DOE Joint Genome Institute, Walnut Creek CA, USA; 5 Hiram College, Hiram, OH, USA Chromohalobacter salexigens DSM 3043 is a moderately halophilic member of the γ-Proteobacteria. It grows at salt concentrations between 0.9 and 25% Over 60% of the ORFS show the highest similarity to orthologs from other with an optimum at 7.5-10%. Pulsed-field gel γ-Proteobacteria. From the sequence, we find good indication that the electrophoresis of total DNA showed that C. salexigens organism has all the enzymes of glycolysis, hexose monophosphate shunt, possesses a chromosome of ~3.9 Mbp (63.9% G+C) Entner-Doudoroff pathway and the TCA cycle. We were able to rationalize and a low copy plasmid of < 100 kbp. the pathways of metabolism of many of the common sugars and mono- and dicarboxylic acids. We could account only partially for the metabolic A draft sequence of the C. salexigens genome has pathway of benzoate, 4-hydroxybenzoate, and 3,4-hydroxybenzoate. been determined to an 8X coverage by the Joint Genome Institute of the US Department of Energy. Within the 3.7 Mbp unique sequences generated, 3370 predicted protein-coding genes were identified and provisionally annotated (http://genome.jgi.psf.org/microbial/index.html). Comparison of the amino acid composition of different categories of proteins of C. CO - salexigens and non-halophilic γ-Proteobacteria (E. coli, P. aeruginosa, V. cholerae) 2 showed only a slight excess of acidic residues in the cytoplasmic proteins, and no benzoate benzoate 1,2-dioxygenase (EC 1.14.12.10) α subunit: 4e-27, § subunit: No sigificant match, significant differences were found in the acidity of membrane-bound proteins. In contrast, electron transfer component (EC 1.18.1.3): 8e-16 -O C OH 2 the periplasmic binding proteins of the ABC transport systems of C. salexigens have a OH pronouncedly lower mean pI value than the non-halophiles. V. cholerae, adapted to dihydroxycylohexadiene carboxylate dehydrogenase (EC 1.3.1.55): e-27 brackish water, shows intermediate values. OH OH - CO2 - catechol 1,2-dioxygenase CO2 (EC 1.13.11.1): 2e-11 catechol 2,3-dioxygenase (EC 1.13.11.2): e-6 cis, cis-muconate cycloisomerase OH (EC 5.5.1.1): 5e-16 CO - - 2 CO2 O CHO C O 2-hydroxymuconic semialdehyde muconolactone isomerase hydrolase (EC 3.1.1.-): 2e-8 O (EC 5.3.3.4): No significant match - - CO2 CO2 O C O CH2 2-oxopent-4-enoate hydratase 3-oxoadipate enol-lactone (EC 4.2.1.80): no significant match hydrolase (EC 3.1.1.24): e-36 O O O - - - O2CCH2CH2CCH2CO CO2 3-oxoadipate CoA-transferase (EC 2.8.3.6) subunit A: No sigificant match, HO subunit B: 5e-8 CH 3 O O - 4-hydroxy-2-oxopentanoate aldolase O2CCH2CH2CCH2C-S-CoA (EC 4.1.3.-): 4e-06 O O 3-oxoacyl-CoA thiolase CH CO - CH3CH + 3 2 (EC 2.3.1.16): e-72 acetaldehyde pyruvate O O - O CCH CH C-S-CoA 2 2 2 + CH3C-S-CoA succinyl-CoA acetyl-CoA ‘Halophilic’ signatures of periplasmic binding proteins of ABC meta-cleavage pathway ortho-cleavage pathway transporters, ribosomal proteins, and selected enzymes of the central metabolic pathways of C. salexigens as compared to E. Mean pI values of different categories of proteins of Chromohalobacter salexigens, as coli, P. aeruginosa, V. cholerae and Halobacterium NRC-1. The compared with the orthologs form the non-halophilic Escherichia coli K-12, Pseudomonas values are given in mole-percent of the total number of amino aeruginosa PA01, Vibrio cholerae O1 El Tor N16961, and the extremely halophilic acid residues or as ratios, as appropriate. Boldface: special Benzoate metabolic pathways. The expect values indicate features of the C. salexigens and the Halobacterium proteins. the tblastn similarity scores of C. salexigens ORFS against archaeon Halobacterium sp. NRC-1. queries from genes from the P. putida TOL plasmid (for the reactions from benzoate to catechol and for the meta pathway) and from Acinetobacter (for the ortho pathway). Conclusions 1. The sequence information shows that C. salexigens is a versatile heterotroph, and can at least partially metabolize a number of aromatic and xenobiotic compounds. This opens the possibility that the organism might be exploited for biological cleanup of highly saline polluted environments. References 2. The acidic nature of the C. salexigens periplasmic substrate binding proteins is indicative of salt adaptation and possibly Csonka, L.N., O’Connor, K., Larimer, F., Richardson, P., Lapidus, A., Ewing, salt dependence of these proteins, and indicates that salt requirement of proteins located external to the cytoplasmic A.D., Goodner, B.W., and Oren, A. 2005. What we can deduce about membrane may determine salt requirement of many prokaryotes. metabolism in the moderate halophile Chromohalobacter salexigens from its genomic sequence. In: Gunde-Cimerman, N., Oren, A., and Plemenitaš, A. This work was performed under the auspices of the US Department of Energy's Office of Science, Biological and Environmental Research Program, (eds.). Adaptation to life at high salt concentrations in Archaea, Bacteria, and by the University of California, Lawrence Livermore National Laboratory under Contract No. W-7405-Eng-48, Lawrence Berkeley National and Eukarya. Springer, Dordrecht, in press. Laboratory under Contract No. DE-AC02-05CH11231 and Los Alamos National Laboratory under Contract No. W-7405-ENG-36. Oren, A., Larimer, F., Richardson, P., Lapidus, A., and Csonka, L.N. 2005. LBNL-57689 Poster How to be moderately halophilic with a broad salt tolerance: clues from the genome of Chromohalobacter salexigens. Extremophiles, in press .
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