Complete genome sequence, metabolic model construction and phenotypic characterization of Geobacillus LC300, an extremely thermophilic, fast growing, xylose-utilizing bacterium

Metabolic Engineering

Volumn 32, Issue , 2015, Pages 74-81

  Cordova, Lauren T ^a   Long, Christopher P ^a   Venkataramanan, Keerthi P ^a   Antoniewicz, Maciek R ^a  

^a UNIVERSITY OF DELAWARE   (United States)

Author keywords

Genome analysis; High cell density fermentation; Metabolic network model; Thermophile; Xylose metabolism

Indexed keywords

BATCH CELL CULTURE; BIOTECHNOLOGY; CELLS; CYTOLOGY; DISSOLVED OXYGEN; ESCHERICHIA COLI; GENES; GLUCOSE; METABOLISM; PHYSIOLOGY;

BIOTECHNOLOGICAL POTENTIALS; BIOTECHNOLOGY APPLICATIONS; GENOME ANALYSIS; HIGH CELL DENSITY FERMENTATIONS; LOW DISSOLVED OXYGEN; METABOLIC NETWORK MODELS; PHENOTYPIC CHARACTERIZATION; THERMOPHILE;

METABOLIC ENGINEERING;

DISSOLVED OXYGEN; GALACTOSE; GLUCOSE; MANNOSE; XYLOSE; CULTURE MEDIUM;

ARTICLE; BACTERIAL CELL; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL STRAIN; CELL DENSITY; CONTROLLED STUDY; ENERGY METABOLISM; ESCHERICHIA COLI; FED BATCH CULTURE; GENOME ANALYSIS; GEOBACILLUS; GEOBACILLUS STEAROTHERMOPHILUS; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PHENOTYPE; PRIORITY JOURNAL; BATCH CELL CULTURE; BIOMASS; CULTURE MEDIUM; FERMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; KINETICS; METABOLIC ENGINEERING; METABOLISM; PROCEDURES;

BATCH CELL CULTURE TECHNIQUES; BIOMASS; CULTURE MEDIA; ENERGY METABOLISM; FERMENTATION; GENOME, BACTERIAL; GEOBACILLUS; GLUCOSE; KINETICS; METABOLIC ENGINEERING; METABOLIC NETWORKS AND PATHWAYS; OXIDATIVE PHOSPHORYLATION; XYLOSE;

EID: 84943239543     PISSN: 10967176     EISSN: 10967184     Source Type: Journal    
DOI: 10.1016/j.ymben.2015.09.009     Document Type: Article

References (58)

1. Ahn W.S., Antoniewicz M.R. Parallel labeling experiments with [1,2-(13)C]glucose and [U-(13)C]glutamine provide new insights into CHO cell metabolism. Metab. Eng. 2013, 15:34-47.
2. Anand A., Kumar V., Satyanarayana T. Characteristics of thermostable endoxylanase and beta-xylosidase of the extremely thermophilic bacterium Geobacillus thermodenitrificans TSAA1 and its applicability in generating xylooligosaccharides and xylose from agro-residues. Extremophiles: Life Under Extreme Cond. 2013, 17:357-366.
3. Antoniewicz M.R. 13C metabolic flux analysis: optimal design of isotopic labeling experiments. Curr. Opin. Biotechnol. 2013, 24:1116-1121.
4. Antoniewicz M.R. Dynamic metabolic flux analysis - tools for probing transient states of metabolic networks. Curr. Opin. Biotechnol. 2013, 24:973-978.
5. Antoniewicz M.R. Methods and advances in metabolic flux analysis: a mini-review. J. Ind. Microbiol. Biotechnol. 2015, 42:317-325.
6. Antoniewicz M.R., Kelleher J.K., Stephanopoulos G. Accurate assessment of amino acid mass isotopomer distributions for metabolic flux analysis. Anal. Chem. 2007, 79:7554-7559.
7. Antoniewicz M.R., Kelleher J.K., Stephanopoulos G. Measuring deuterium enrichment of glucose hydrogen atoms by gas chromatography/mass spectrometry. Anal. Chem. 2011, 83:3211-3216.
8. Antoniewicz M.R., Stephanopoulos G., Kelleher J.K. Evaluation of regression models in metabolic physiology: predicting fluxes from isotopic data without knowledge of the pathway. Metabolomics 2006, 2:41-52.
9. Au J., Choi J., Jones S.W., Venkataramanan K.P., Antoniewicz M.R. Parallel labeling experiments validate Clostridium acetobutylicum metabolic network model for C metabolic flux analysis. Metab. Eng. 2014, 26:23-33.
10. Aziz R.K., Bartels D., Best A.A., DeJongh M., Disz T., Edwards R.A., Formsma K., Gerdes S., Glass E.M., Kubal M., Meyer F., Olsen G.J., Olson R., Osterman A.L., Overbeek R.A., McNeil L.K., Paarmann D., Paczian T., Parrello B., Pusch G.D., Reich C., Stevens R., Vassieva O., Vonstein V., Wilke A., Zagnitko O. The RAST Server: rapid annotations using subsystems technology. BMC Genom. 2008, 9:75.
11. Blumer-Schuette S.E., Kataeva I., Westpheling J., Adams M.W., Kelly R.M. Extremely thermophilic microorganisms for biomass conversion: status and prospects. Curr. Opin. Biotechnol. 2008, 19:210-217.
12. Canakci S., Cevher Z., Inan K., Tokgoz M., Bahar F., Kacagan M., Sal F.A., Belduz A.O. Cloning, purification and characterization of an alkali-stable endoxylanase from thermophilic Geobacillus sp. 71. World J. Microbiol. Biotechnol. 2012, 28:1981-1988.
13. Chang T., Yao S. Thermophilic, lignocellulolytic bacteria for ethanol production: current state and perspectives. Appl. Microbiol. Biotechnol. 2011, 92:13-27.
14. Coorevits A., Dinsdale A.E., Halket G., Lebbe L., De Vos P., Van Landschoot A., Logan N.A. Taxonomic revision of the genus Geobacillus: emendation of Geobacillus, G. stearothermophilus, G. jurassicus, G. toebii, G. thermodenitrificans and G. thermoglucosidans (nom. corrig., formerly'thermoglucosidasius'); transfer of Bacillus thermantarcticus to the genus as G. thermantarcticus comb. nov.; proposal of Caldibacillus debilis gen. nov., comb. nov.; transfer of G. tepidamans to Anoxybacillus as A. tepidamans comb. nov.; and proposal of Anoxybacillus caldiproteolyticus sp. nov. Int. J. Syst. Evol. Microbiol. 2012, 62:1470-1485.
15. 13C Metabolic flux analysis of the extremely thermophilic, fast growing, xylose-utilizing Geobacillus strain LC300. Metab. Eng 2015, 10.1016/j.ymben.2015.06.004.
16. Cripps R.E., Eley K., Leak D.J., Rudd B., Taylor M., Todd M., Boakes S., Martin S., Atkinson T. Metabolic engineering of Geobacillus thermoglucosidasius for high yield ethanol production. Metab. Eng. 2009, 11:398-408.
17. Crown S.B., Antoniewicz M.R. Parallel labeling experiments and metabolic flux analysis: past, present and future methodologies. Metab. Eng. 2013, 16:21-32.
18. Crown S.B., Antoniewicz M.R. Publishing 13C metabolic flux analysis studies: a review and future perspectives. Metab. Eng. 2013, 20:42-48.
19. Dauner M., Sauer U. Stoichiometric growth model for riboflavin-producing Bacillus subtilis. Biotechnol. Bioeng. 2001, 76:132-143.
20. Elleuche S., Schroder C., Sahm K., Antranikian G. Extremozymes-Biocatalysts with unique properties from extremophilic microorganisms. Curr. Opin. Biotechnol. 2014, 29:116-123.
21. Ezeji T.C., Bahl H. Purification, characterization, and synergistic action of phytate-resistant alpha-amylase and alpha-glucosidase from Geobacillus thermodenitrificans HRO10. J. Biotechnol. 2006, 125:27-38.
22. Ezeji T.C., Wolf A., Bahl H. Isolation, characterization, and identification of Geobacillus thermodenitrificans HRO10, an alpha-amylase and alpha-glucosidase producing thermophile. Can. J. Microbiol. 2005, 51:685-693.
23. Feng L., Wang W., Cheng J., Ren Y., Zhao G., Gao C., Tang Y., Liu X., Han W., Peng X., Liu R., Wang L. Genome and proteome of long-chain alkane degrading Geobacillus thermodenitrificans NG80-2 isolated from a deep-subsurface oil reservoir. Proc. Natl. Acad. Sci. USA 2007, 104:5602-5607.
24. Fernandez C.A., Des Rosiers C., Previs S.F., David F., Brunengraber H. Correction of 13C mass isotopomer distributions for natural stable isotope abundance. J. Mass Spectrom. 1996, 31:255-262.
25. Goebel B.M., Stackebrandt E. Cultural and phylogenetic analysis of mixed microbial populations found in natural and commercial bioleaching environments. Appl. Environ. Microbiol. 1994, 60:1614-1621.
26. Gonzalez R., Tao H., Shanmugam K.T., York S.W., Ingram L.O. Global gene expression differences associated with changes in glycolytic flux and growth rate in Escherichia coli during the fermentation of glucose and xylose. Biotechnol. Prog. 2002, 18:6-20.
27. He L., Xiao Y., Gebreselassie N., Zhang F., Antoniewicz M.R., Tang Y.J., Peng L. Central metabolic responses to the overproduction of fatty acids in Escherichia coli based on 13C-metabolic flux analysis. Biotechnol. Bioeng. 2014, 111:575-585.
28. Kupor S.R., Fraenkel D.G. 6-phosphogluconolactonase mutants of Escherichia coli and a maltose blue gene. J. Bacteriol. 1969, 100:1296-1301.
29. La Duc M.T., Dekas A., Osman S., Moissl C., Newcombe D., Venkateswaran K. Isolation and characterization of bacteria capable of tolerating the extreme conditions of clean room environments. Appl. Environ. Microbiol. 2007, 73:2600-2611.
30. 13C metabolic flux analysis. Metab. Eng. 2012, 14:533-541.
31. Leighty R.W., Antoniewicz M.R. COMPLETE-MFA: complementary parallel labeling experiments technique for metabolic flux analysis. Metab. Eng. 2013, 20:49-55.
32. Lin L., Xu J. Dissecting and engineering metabolic and regulatory networks of thermophilic bacteria for biofuel production. Biotechnol. Adv. 2013, 31:827-837.
33. Lin P.P., Rabe K.S., Takasumi J.L., Kadisch M., Arnold F.H., Liao J.C. Isobutanol production at elevated temperatures in thermophilic Geobacillus thermoglucosidasius. Metab. Eng. 2014, 24:1-8.
34. Liu J.K., O'Brien E.J., Lerman J.A., Zengler K., Palsson B.O., Feist A.M. Reconstruction and modeling protein translocation and compartmentalization in Escherichia coli at the genome-scale. BMC Syst. Biol. 2014, 8:110.
35. Loftie-Eaton W., Taylor M., Horne K., Tuffin M.I., Burton S.G., Cowan D.A. Balancing redox cofactor generation and ATP synthesis: key microaerobic responses in thermophilic fermentations. Biotechnol. Bioeng. 2013, 110:1057-1065.
36. Long C.P., Antoniewicz M.R. Metabolic flux analysis of Escherichia coli knockouts: lessons from the Keio collection and future outlook. Curr. Opin. Biotechnol. 2014, 28:127-133.
37. Long C.P., Antoniewicz M.R. Quantifying biomass composition by gas chromatography/mass spectrometry. Anal. Chem. 2014, 86:9423-9427.
38. Lynd L.R. Production of ethanol from lignocellulosic materials using thermophilic bacteria: critical evaluation of potential and review. Production of Ethanol from Lignocellulosic Materials Using Thermophilic Bacteria: Critical Evaluation of Potential and Review 1989, 1-52. Springer-Verlag, Heidelberg. A. Fiechter (Ed.).
39. Marchant R., Banat I.M., Rahman T.J., Berzano M. The frequency and characteristics of highly thermophilic bacteria in cool soil environments. Environ. Microbiol. 2002, 4:595-602.
40. Marchant R., Banat I.M., Rahman T.J., Berzano M. What are high-temperature bacteria doing in cold environments?. Trends Microbiol. 2002, 10:120-121.
41. Muhd Sakaff M.K., Abdul Rahman A.Y., Saito J.A., Hou S., Alam M. Complete genome sequence of the thermophilic bacterium Geobacillus thermoleovorans CCB_US3_UF5. J. Bacteriol. 2012, 194:1239.
42. Nazina T.N., Tourova T.P., Poltaraus A.B., Novikova E.V., Grigoryan A.A., Ivanova A.E., Lysenko A.M., Petrunyaka V.V., Osipov G.A., Belyaev S.S., Ivanov M.V. Taxonomic study of aerobic thermophilic bacilli: descriptions of Geobacillus subterraneus gen. nov., sp. nov. and Geobacillus uzenensis sp. nov. from petroleum reservoirs and transfer of Bacillus stearothermophilus, Bacillus thermocatenulatus, Bacillus thermoleovorans, Bacillus kaustophilus, Bacillus thermodenitrificans to Geobacillus as the new combinations G. stearothermophilus, G. th. Int. J. Syst. Evol. Microbiol. 2001, 51:433-446.
43. Neidhardt F.C. Escherichia Coli and Salmonella Typhimurium 1987, ASM Press.
44. Patrick W.M., Quandt E.M., Swartzlander D.B., Matsumura I. Multicopy suppression underpins metabolic evolvability. Mol. Biol. Evol. 2007, 24:2716-2722.
45. Rozanov A.S., Logacheva M.D., Peltek S.E. Draft genome sequences of geobacillus stearothermophilus strains 22 and 53, isolated from the garga hot spring in the barguzin river valley of the Russian federation. Genome Announc. 2014, 2.
46. Shintani M., Ohtsubo Y., Fukuda K., Hosoyama A., Ohji S., Yamazoe A., Fujita N., Nagata Y., Tsuda M., Hatta T., Kimbara K. Complete genome sequence of the thermophilic polychlorinated biphenyl degrader geobacillus sp. Strain JF8 (NBRC 109937). Genome Announc. 2014, 2.
47. Stephanopoulos G.N., Aristidou A.A., Nielsen J. Metabolic engineering: principles and methodologies 1998, Academic Press.
48. 13C-metabolic flux analysis of the extremophile Thermus thermophilus HB8. Metab. Eng. 2014, 24:173-180.
49. Takami H., Takaki Y., Chee G.J., Nishi S., Shimamura S., Suzuki H., Matsui S., Uchiyama I. Thermoadaptation trait revealed by the genome sequence of thermophilic Geobacillus kaustophilus. Nucleic Acids Res. 2004, 32:6292-6303.
50. Tang Y.J., Sapra R., Joyner D., Hazen T.C., Myers S., Reichmuth D., Blanch H., Keasling J.D. Analysis of metabolic pathways and fluxes in a newly discovered thermophilic and ethanol-tolerant Geobacillus strain. Biotechnol. Bioeng. 2009, 102:1377-1386.
51. Taylor M.P., Eley K.L., Martin S., Tuffin M.I., Burton S.G., Cowan D.A. Thermophilic ethanologenesis: future prospects for second-generation bioethanol production. Trends Biotechnol. 2009, 27:398-405.
52. Thomason L.C., Court D.L., Datta A.R., Khanna R., Rosner J.L. Identification of the Escherichia coli K-12 ybhE gene as pgl, encoding 6-phosphogluconolactonase. J. Bacteriol. 2004, 186:8248-8253.
53. Verma D., Anand A., Satyanarayana T. Thermostable and alkalistable endoxylanase of the extremely thermophilic bacterium Geobacillus thermodenitrificans TSAA1: cloning, expression, characteristics and its applicability in generating xylooligosaccharides and fermentable sugars. Appl. Biochem. Biotechnol. 2013, 170:119-130.
54. Wasylenko T.M., Stephanopoulos G. Metabolomic and C-metabolic flux analysis of a xylose-consuming Saccharomyces cerevisiae strain expressing xylose isomerase. Biotechnol. Bioeng. 2015, 112:470-483.
55. Xiao Z., Wang X., Huang Y., Huo F., Zhu X., Xi L., Lu J.R. Thermophilic fermentation of acetoin and 2,3-butanediol by a novel Geobacillus strain. Biotechnol. Biofuels 2012, 5:88.
56. Zhao Y., Caspers M.P., Abee T., Siezen R.J., Kort R. Complete genome sequence of Geobacillus thermoglucosidans TNO-09.020, a thermophilic sporeformer associated with a dairy-processing environment. J. Bacteriol. 2012, 194:4118.
57. Zhou H., Cheng J.S., Wang B.L., Fink G.R., Stephanopoulos G. Xylose isomle rapid xylose utilization and ethanol production by Saccharomyces cerevisiae. Metab. Eng. 2012, 14:611-622.
58. Zimenkov D., Gulevich A., Skorokhodova A., Biriukova I., Kozlov Y., Mashko S. Escherichia coli ORF ybhE is pgl gene encoding 6-phosphogluconolactonase (EC 3.1.1.31) that has no homology with known 6PGLs from other organisms. FEMS Microbiol. Lett. 2005, 244:275-280.