Evolutionary patterns of carbohydrate transport and metabolism in Halomonas boliviensis as derived from its genome sequence: influences on polyester production
Tóm tắt
Halomonas boliviensis is a halophilic bacterium that is included in the γ-Proteobacteria sub-group, and is able to assimilate different types of carbohydrates. H. boliviensis is also able to produce poly(3-hydroxybutyrate) (PHB) in high yields using glucose as the carbon precursor. Accumulation of PHB by microorganisms is induced by excess of intracellular NADH. The genome sequences and organization in microorganisms should be the result of evolution and adaptation influenced by mutation, gene duplication, horizontal gen transfer (HGT) and recombination. Furthermore, the nearly neutral theory of evolution sustains that genetic modification of DNA could be neutral or selected, albeit most mutations should be at the border between neutrality and selection, i.e. slightly deleterious base substitutions in DNA are followed by a slightly advantageous substitutions. This article reports the genome sequence of H. boliviensis. The chromosome size of H. boliviensis was 4 119 979 bp, and contained 3 863 genes. A total of 160 genes of H. boliviensis were related to carbohydrate transport and metabolism, and were organized as: 70 genes for metabolism of carbohydrates; 47 genes for ABC transport systems and 43 genes for TRAP-type C4-dicarboxylate transport systems. Protein sequences of H. boliviensis related to carbohydrate transport and metabolism were selected from clusters of orthologous proteins (COGs). Similar proteins derived from the genome sequences of other 41 archaea and 59 bacteria were used as reference. We found that most of the 160 genes in H. boliviensis, c.a. 44%, were obtained from other bacteria by horizontal gene transfer, while 13% of the genes were acquired from haloarchaea and thermophilic archaea, only 34% of the genes evolved among Proteobacteria and the remaining genes encoded proteins that did not cluster with any of the proteins obtained from the reference strains. Furthermore, the diversity of the enzymes derived from these genes led to polymorphism in glycolysis and gluconeogenesis. We found further that an optimum ratio of glucose and sucrose in the culture medium of H. boliviensis favored cell growth and PHB production. Results obtained in this article depict that most genetic modifications and enzyme polymorphism in the genome of H. boliviensis were mainly influenced by HGT rather than nearly neutral mutations. Molecular adaptation and evolution experienced by H. boliviensis were also a response to environmental conditions such as the type and amount of carbohydrates in its ecological niche. Consequently, the genome evolution of H. boliviensis showed to be strongly influenced by the type of microorganisms, genetic interaction among microbial species and its environment. Such trend should also be experienced by other prokaryotes. A system for PHB production by H. boliviensis that takes into account the evolutionary adaptation of this bacterium to the assimilation of combinations of carbohydrates suggests the feasibility of a bioprocess economically viable and environmentally friendly.
Tài liệu tham khảo
Ohta T: The nearly neutral theory of molecular evolution. Annu Rev Ecol Syst. 1992, 23: 263-286. 10.1146/annurev.es.23.110192.001403.
Puigbò P, Wolf YI, Koonin EV: The tree and net components of prokaryote evolution. Genome Biol Evol. 2010, 2: 745-756. 10.1093/gbe/evq062.
Orr H: The genetic theory of adaptation: a brief history. Nature Reviews. 2005, 6: 119-127.
Puigbò P, Wolf YI, Koonin EV: Search for a 'Tree of Life' in the thicket of the phylogenetic forest. J Biology. 2009, 8: 1-17. 10.1186/jbiol111.
Schliep K, Lopez P, Lapointe FJ, Bapteste E: Harvesting evolutionary signals in a forest of prokaryotic gene trees. Mol Biol Evol. 2010, 28: 1393-1405.
Cai L, Tan D, Aibaidula G, Dong X, Chen J, Tian W, Chen G: Comparative genomics study of polyhydroxyalkanoates (PHA) and ectoine relevant genes from Halomonas sp. TD01 revealed extensive horizontal gene transfer events and co-evolutionary relationships. Microb Cell Fact. 2011, 10: 88-10.1186/1475-2859-10-88.
Oren A: Microbial life at high salt concentrations: phylogenetic and metabolic diversity. Saline Systems. 2008, 4: 2-10.1186/1746-1448-4-2.
Oren A, Larimer F, Richardson P, Lapidus A, Csonka LN: How to be moderately halophilic with broad salt tolerance: clues from the genome of Chromohalobacter salexigens. Extremophiles. 2005, 9: 275-279. 10.1007/s00792-005-0442-7.
Schvibbert K, et al: A blueprint of ectoine metabolism from the genome of the industrial producer Halomonas elongata DSM 2581T. Environ Microbiol. 2010, 13: 1973-1994.
Lin Y, et al: Draft genome sequence of Halomonas sp. strain HAL1, a moderately halophilic arsenite-oxidizing bacterium isolated from gold-mine soil. J Bacteriol. 2011, 194: 199-200.
Roberts MF: Organic compatible solutes of halotolerant and halophilic microorganism. Saline Systems. 2005, 1: 5-10.1186/1746-1448-1-5.
Eanes WF: Molecular population genetics and selection in the glycolytic pathway. J Exp Biol. 2011, 214: 165-171. 10.1242/jeb.046458.
Eanes WF: Analysis of selection on enzyme polymorphism. Annu Rev Ecol Syst. 1999, 30: 301-326. 10.1146/annurev.ecolsys.30.1.301.
Hartl D, Dykhuizen D, Dean A: Limits of adaptation: the evolution of selective neutrality. Genetics. 1985, 111: 655-674.
Quillaguamán J, Hatti-Kaul R, Mattiasson B, Alvarez MT, Delgado O: Halomonas boliviensis sp. nov., an alkalitolerant, moderate halophile bacterium isolated from soil around a Bolivian hypersaline lake. Int J Syst Evol Microbiol. 2004, 54: 721-725. 10.1099/ijs.0.02800-0.
Quillaguamán J, Van-Thuoc D, Guzmán H, Guzmán D, Martín J, Akaraonye E, Hatti-Kaul R: Poly(3-hydroxybutyrate) production by Halomonas boliviensis in fed-batch culture. Appl Microbiol Biotechnol. 2008, 78: 227-232. 10.1007/s00253-007-1297-x.
Van-Thuoc D, Guzmán H, Quillaguamán J, Hatti-Kaul R: High productivity of ectoines by Halomonas boliviensis using a combined two-step fed-batch culture and milking process. J Biotechnol. 2010, 147: 46-51. 10.1016/j.jbiotec.2010.03.003.
Quillaguamán J, Delgado O, Mattiasson B, Hatti-Kaul R: Poly(β-hydroxybutyrate) production by a moderate halophile, Halomonas boliviensis LC1. Enzyme Microb Technol. 2006, 38: 148-154. 10.1016/j.enzmictec.2005.05.013.
Steinbüchel A, Füchtenbush B: Bacterial and other biological systems for polyester production. Trends Biotechnol. 1998, 16: 419-427. 10.1016/S0167-7799(98)01194-9.
Philip S, Keshavarz T, Roy I: Polyhydroxyalkanoates: biodegradable polymers with a range of applications. J Chem Technol Biotechnol. 2007, 82: 233-247. 10.1002/jctb.1667.
Lee SY: Plastic bacteria? Progress and prospects for polyhydroxyalkanoate production in bacteria. Trends Biotechnol. 1996, 14: 431-438. 10.1016/0167-7799(96)10061-5.
Choi J, Lee S: Factors affecting the economics of polyhydroxyalkanoate production by bacterial fermentation. Appl Microbiol Biotechnol. 1998, 51: 13-21.
Delcher A, Bratke K, Powers E, Salzberg S: Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics. 2007, 23: 673-679. 10.1093/bioinformatics/btm009.
Tatusov R, et al: The COG database: an updated version includes eukaryotes. BMC Bioinforma. 2003, 4: 41-10.1186/1471-2105-4-41.
Jensen L, Julien P, Kuhn M, von Mering C, Muller J, Doerks T, Bork P: eggNOG: automated construction and annotation of orthologous groups of genes. Nucleic Acids Res. 2008, 36: D250-D254.
Edgar R: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32: 1792-1797. 10.1093/nar/gkh340.
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011, 10: 2731-2739.
Huson D, Bryant D: Application of phylogenetic networks in evolutionary studies. Mol Biol Evol. 2006, 23: 254-267.
Huson D, Dezulian T, Klopper T, Steel M: Phylogenetic supernetworks from partial trees. IEEE/ACM Trans Comput Biol Bioinform. 2004, 1: 151-158. 10.1109/TCBB.2004.44.
Lee SY, Wong HH, Choi J, Lee SH, Lee SC, Han CS: Production of medium-chain-length polyhydroxyalkanoates by high-cell-density cultivation of Pseudomonas putida under phosphorus limitation. Biotechnol Bioeng. 2000, 68: 466-470. 10.1002/(SICI)1097-0290(20000520)68:4<466::AID-BIT12>3.0.CO;2-T.
Onraedt A, Wlcarius B, Soetaert W, Vandamme E: Optimization of ectoine synthesis through fed-batch fermentation of Brevibacterium epidermis. Biotechnol Prog. 2005, 21: 1206-1212.
Arahal DR, García MT, Vargas C, Cánovas D, Nieto JJ, Ventosa A: Chromohalobacter salexigens sp. nov., a moderately halophilic species that includes Halomonas elongata DSM 3043 and ATCC 33174. Int J Syst Evol Microbiol. 2001, 51: 1457-1462.
Arahal DR, Ventosa A: The family Halomonadaceae. The Prokaryotes. A handbook on the biology of bacteria. Edited by: Dworkin M, et al. 2006, New York: Springer, 811-835.
Gandbhir M, Rashed I, Marlière P, Mutzel R: Convergent evolution of amino acid usage in archaebacterial and eubacterial linages adapted to high salt. Res Microbiol. 1995, 146: 113-120. 10.1016/0923-2508(96)80889-8.
Kimura M: Evolutionary rate at the molecular level. Nature. 1968, 217: 624-626. 10.1038/217624a0.
Kreitman M: The neutral theory is dead. Long live the neutral theory. Bioessays. 1996, 18: 678-683. 10.1002/bies.950180812.
Kanehisa M, et al: From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res. 2006, 34: D354-D357. 10.1093/nar/gkj102.
Quillaguamán J, Hashim S, Bento F, Mattiasson B, Hatti-Kaul R: Poly(β-hydroxybutyrate) production by a moderate halophile, Halomonas boliviensis LC1 using starch hydrolysate as substrate. J Appl Microbiol. 2005, 99: 151-157. 10.1111/j.1365-2672.2005.02589.x.
de Kok A, Hengeveld AF, Martin A, Westphal AH: The pyruvate dehydrogenase multi-enzyme comples from Gram-negative bacteria. Biochim Biophys Acta. 1998, 1385: 353-366. 10.1016/S0167-4838(98)00079-X.
Danson MJ: Central metabolism of the Archaea. New Compr Biochem. 1993, 26: 1-24.
Jolley KA, et al: 2-oxoacid dehydrogenase mutienzyme complexes in the halophilic Archaea? Gene sequences and protein structural predictions. Microbiology. 2000, 146: 1061-1069.
Sawyer S, Dykhuizen D, Hartl D: Confidence interval for the number of selectively neutral amino acid polymorphism. Proc Natl Acad Sci USA. 1987, 84: 6225-6228. 10.1073/pnas.84.17.6225.
Quillaguamán J, Guzmán H, Van-Thuoc D, Hatti-Kaul R: Synthesis and production of polyhydroxyalkanoates by halophiles: current potential and future prospects. Appl Microbiol Biotechnol. 2010, 85: 1687-1696. 10.1007/s00253-009-2397-6.
Babel W, Ackermann JU, Breuer U: Physiology, regulation, and limits of the synthesis of poly (3HB). Advances in Biochemical Engineering/Biotechnology: Biopolyesters. Edited by: Scheper T, Babel W, Steinbüchel A. 2001, Berlin: Springer, 125-157.
Doi Y, Tamaki A, Kunioka M, Soga K: Production of copolyesters of 3-hydroxybutyrate and 3-hydroxyvalerate by Alcaligenes eutrophus from butyric and pentanoic acids. Appl Microbiol Biotechnol. 1988, 28: 330-334. 10.1007/BF00268190.
Lee SY, Lee KM, Chang HN, Steinbüchel A: Comparison of recombinant Escherichia coli strains for synthesis and accumulation of poly-(3-hydroxybutyric acid) and morphological changes. Biotechnol Bioeng. 1994, 44: 1337-1347. 10.1002/bit.260441110.
Page WJ: Production of poly-β-hydroxybutyrate by Azotobacter vinelandii UWD in media containing sugars and complex nitrogen. Appl Microbiol Biotechnol. 1992, 38: 117-121.