Rapid metabolic analysis of Rhodococcus opacus PD630 via parallel 13C-metabolite fingerprinting

Biotechnology and Bioengineering

Volumn 113, Issue 1, 2016, Pages 91-100

  Hollinshead, Whitney D ^a   Henson, William R ^a   Abernathy, Mary ^a   Moon, Tae Seok ^a   Tang, Yinjie J ^a  

^a WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

Author keywords

13C MFA; Catabolite repression; Entner Doudoroff (ED) pathway; Gluconeogenesis; Phenol

Indexed keywords

AMINO ACIDS; GLUCOSE; PHENOLS; PHYSIOLOGY;

13C-MFA; CATABOLITE REPRESSION; ENTNER-DOUDOROFF; GLUCONEOGENESIS; LIGNOCELLULOSIC FEEDSTOCKS; METABOLITE FINGERPRINTING; PHOSPHOENOLPYRUVATE CARBOXYLASE; RHODOCOCCUS OPACUS PD630;

METABOLISM;

CARBON;

METABOLISM; METABOLOMICS; PROCEDURES; RHODOCOCCUS; STAINING; TIME FACTOR;

CARBON ISOTOPES; METABOLIC NETWORKS AND PATHWAYS; METABOLOMICS; RHODOCOCCUS; STAINING AND LABELING; TIME FACTORS;

EID: 84947967425     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.25702     Document Type: Article

References (58)

1. Alper H, Stephanopoulos G. 2009. Engineering for biofuels: Exploiting innate microbial capacity or importing biosynthetic potential? Nat Rev Microbiol 7(10):715-723.
2. Alvarez HM, Mayer F, Fabritius D, Steinbuchel A. 1996. Formation of intracytoplasmic lipid inclusions by Rhodococcus opacus strain PD630. Arch Microbiol 165(6):377-386.
3. Antoniewicz MR. 2015. Methods and advances in metabolic flux analysis: A mini-review. J Ind Microbiol Biotechnol 42(3):317-325.
4. 13C metabolic flux analysis. Metab Eng 26c:23-33.
5. Borodina I, Schöller C, Eliasson A, Nielsen J. 2005. Metabolic network analysis of Streptomyces tenebrarius, a Streptomyces Species with an active Entner-Doudoroff Pathway. Appl Environ Microbiol 71(5):2294-2302.
6. Boshoff HIM, Barry CE. 2005. Tuberculosis - metabolism and respiration in the absence of growth. Nat Rev Microbiol 3(1):70-80.
7. Bredholdt H, Galatenko OA, Engelhardt K, Fjaervik E, Terekhova LP, Zotchev SB. 2007. Rare actinomycete bacteria from the shallow water sediments of the Trondheim fjord, Norway: Isolation, diversity and biological activity. Environ Microbiol 9(11):2756-2764.
8. 13C metabolite labeling patterns from cells. Curr Opin Biotechnol 34:189-201.
9. Chartrain M, Jackey B, Taylor C, Sandford V, Gbewonyo K, Lister L, Dimichele L, Hirsch C, Heimbuch B, Maxwell C, Pascoe D, Buckland B, Greasham G. 1998. Bioconversion of indene to cis (1S, 2R) indandiol and trans (1R, 2R) indandiol by Rhodococcus species. J Ferment Bioeng 86(6):550-558.
10. Chavarría M, Nikel PI, Pérez-Pantoja D, de Lorenzo V. 2013. The Entner-Doudoroff pathway empowers Pseudomonas putidaKT2440 with a high tolerance to oxidative stress. Environ Microbiol 15(6):1772-1785.
11. Chubukov V, Uhr M, Le Chat L, Kleijn RJ, Jules M, Link H, Aymerich S, Stelling J, Sauer U. 2013. Transcriptional regulation is insufficient to explain substrate induced flux changes in Bacillus subtilis. Mol Syst Biol 9(1):709.
12. Crown SB, Antoniewicz MR. 2013a. Parallel labeling experiments and metabolic flux analysis: Past, present and future methodologies. Metab Eng 16:21-32.
13. Crown SB, Antoniewicz MR. 2013b. Publishing 13C metabolic flux analysis studies: a review and future perspectives. Metab Eng 20:42-48.
14. Crown SB, Long CP, Antoniewicz MR. 2015. Integrated 13C-metabolic flux analysis of 14 parallel labeling experiments in Escherichia coli. Metab Eng 28:151-158.
15. Feisthauer S, Wick LY, Kästner M, Kaschabek SR, Schlömann M, Richnow HH. 2008. Differences of heterotrophic 13CO2 assimilation by Pseudomonas knackmussii strain B13 and Rhodococcus opacus 1CP and potential impact on biomarker stable isotope probing. Environ Microbiol 10(6):1641-1651.
16. Fischer E, Sauer U. 2005. Large-scale in vivo flux analysis shows rigidity and suboptimal performance of Bacillus subtilis metabolism. Nat Genet 37(6):636-640.
17. Flamholz A, Noor E, Bar-Even A, Liebermeister W, Milo R. 2013. Glycolytic strategy as a tradeoff between energy yield and protein cost. Proc Natl Acad Sci 110(24):10039-10044.
18. Giffin MM, Modesti L, Raab RW, Wayne LG, Sohaskey CD. 2012. ald of Mycobacterium tuberculosis encodes both the alanine dehydrogenase and the putative glycine dehydrogenase. J Bacteriol 194(5):1045-1054.
19. Gonçalves ER, Hara H, Miyazawa D, Davies JE, Eltis LD, Mohn WW. 2006. Transcriptomic assessment of isozymes in the biphenyl pathway of Rhodococcus sp. Strain RHA1. Appl Environ Microbiol 72(9):6183-6193.
20. Gunnarsson N, Bruheim P, Nielsen J. 2004. Glucose metabolism in the antibiotic producing actinomycete Nonomuraea sp. ATCC 39727. Biotechnol Bioeng 88(5):652-663.
21. Gygi SP, Rochon Y, Franza BR, Aebersold R. 1999. Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 19(3):1720-1730.
22. Harwood CS, Parales RE. 1996. The beta-ketoadipate pathway and the biology of self-identity. Annu Rev Microbiol 50:553-590.
23. Hermann R, Lehmann M, Büchs J. 2003. Characterization of gas-liquid mass transfer phenomena in microtiter plates. Biotechnol Bioeng 81(2):178-186.
24. Heux S, Poinot J, Massou S, Sokol S, Portais J-C. 2014. A novel platform for automated high-throughput fluxome profiling of metabolic variants. Metab Eng 25:8-19.
25. Holder JW, Ulrich JC, DeBono AC, Godfrey PA, Desjardins CA, Zucker J, Zeng QD, Leach ALB, Ghiviriga I, Dancel C, Abeel T, Gevers D, Kodira C, Desany B, Affourtit J, Birren B, Sinskey A. 2011. Comparative and functional genomics of Rhodococcus opacus PD630 for biofuels development. Plos Genetics 7(9):e1002219.
26. Hong SH, Park SJ, Moon SY, Park JP, Lee SY. 2003. In silico prediction and validation of the importance of the Entner-Doudoroff pathway in poly(3-hydroxybutyrate) production by metabolically engineered Escherichia coli. Biotechnol Bioeng 83(7):854-863.
27. Hoynes-O'Connor A, Hinman K, Kirchner L, Moon TS. 2015. De novo design of heat-repressible RNA thermosensors in E. coli. Nucleic Acids Res 43(12):6166-6179.
28. 13C-flux profiling reveals conservation of the Entner-Doudoroff pathway as glycolytic strategy among glucose-using marine bacteria. Appl Environ Microbiol 81(7):2408-2422.
29. Kurosawa K, Plassmeier J, Kalinowski J, Rückert C, Sinskey AJ. 2015. Engineering l-arabinose metabolism in triacylglycerol-producing Rhodococcus opacus for lignocellulosic fuel production. Metab Eng 30:89-95.
30. LeBlanc JC, Gonçalves ER, Mohn WW. 2008. Global response to desiccation stress in the soil actinomycete Rhodococcus jostii RHA1. Appl Environ Microbiol 74(9):2627-2636.
31. Long CP, Antoniewicz MR. 2014. Quantifying biomass composition by gas chromatography/mass spectrometry. Anal Chem 86(19):9423-9427.
32. Mathews CK, Holde KEv, Appling DR, Anthony-Cahill SJ. 2013. Biochemistry: Prentice Hall.
33. McLeod MP, Warren RL, Hsiao WWL, Araki N, Myhre M, Fernandes C, Miyazawa D, Wong W, Lillquist AL, Wang D, Dosanjh M, Hara H, Petrescu A, Morin RD, Yang G, Stott JM, Schein JE, Shin H, Smailus D, Siddiqui AS, Marra MA, Jones SJ, Holt R, Brinkman FS, Miyauchi K, Fukuda M, Davies JE, Mohn WW, Eltis LD. 2006. The complete genome of Rhodococcus sp RHA1 provides insights into a catabolic powerhouse. Proc Natl Acad Sci 103(42):15582-15587.
34. Nakashima N, Mitani Y, Tamura T. 2005. Actinomycetes as host cells for production of recombinant proteins. Microb Cell Fact 4(1):7.
35. Ng CY, Farasat I, Maranas CD, Salis HM. 2015. Rational design of a synthetic Entner-Doudoroff pathway for improved and controllable NADPH regeneration. Metab Eng 29:86-96.
36. Paje MLF, Neilan BA, Couperwhite I. 1997. A Rhodococcus species that thrives on medium saturated with liquid benzene. Microbiol 143(9):2975-2981.
37. Peng L, Arauzo-Bravo MJ, Shimizu K. 2004. Metabolic flux analysis for a ppc mutant Escherichia coli based on 13C-labelling experiments together with enzyme activity assays and intracellular metabolite measurements. FEMS Microbiol Lett 235(1):17-23.
38. Ruan Z, Hollinshead W, Isaguirre C, Tang YJ, Liao W, Liu Y. 2015. Effects of inhibitory compounds in lignocellulosic hydrolysates on Mortierella isabellina growth and carbon utilization. Bioresour Technol 183:18-24.
39. Suthers PF, Dasika MS, Kumar VS, Denisov G, Glass JI, Maranas CD. 2009. A Genome-scale metabolic reconstruction of Mycoplasma genitalium, iPS189. PLoS Comput Biol 5(2):e1000285.
40. Szoköl J, Rucká L, Šimčíková M, Halada P, Nešvera J, Pátek M. 2014. Induction and carbon catabolite repression of phenol degradation genes in Rhodococcus erythropolis and Rhodococcus jostii. Appl Microbiol Biotechnol 98(19):8267-8279.
41. 13C isotopic fingerprints. J R Soc Interface 9(76):2767-2780.
42. Tang K-H, Feng X, Tang YJ, Blankenship RE. 2009a. Carbohydrate metabolism and carbon fixation in Roseobacter denitrificans OCh114. PLoS ONE 4(10): e7233.
43. Tang Y, Shui W, Myers S, Feng X, Bertozzi C, Keasling J. 2009b. Central metabolism in Mycobacterium smegmatis during the transition from O2-rich to O2-poor conditions as studied by isotopomer-assisted metabolite analysis. Biotechnol Lett 31(8):1233-1240.
44. Urbano SB, Di Capua C, Cortez N, Farias ME, Alvarez HM. 2014. Triacylglycerol accumulation and oxidative stress in Rhodococcus species: Differential effects of pro-oxidants on lipid metabolism. Extremophiles 18(2):375-384.
45. 13C-based metabolism analysis. Microb Cell Fact 13(1):42.
46. Vesely M, Knoppova M, Nesvera J, Patek M. 2007. Analysis of catRABC operon for catechol degradation from phenol-degrading Rhodococcus erythropolis. Appl Microbiol Biotechnol 76(1):159-168.
47. Wahl SA, Dauner M, Wiechert W. 2004. New tools for mass isotopomer data evaluation in 13C flux analysis: Mass isotope correction, data consistency checking, and precursor relationships. Biotechnol Bioeng 85(3):259-268.
48. Wang B, Rezenom YH, Cho K-C, Tran JL, Lee DG, Russell DH, Gill JJ, Young R, Chu K-H. 2014. Cultivation of lipid-producing bacteria with lignocellulosic biomass: Effects of inhibitory compounds of lignocellulosic hydrolysates. Bioresour Technol 161(0):162-170.
49. Whyte LG, Schultz A, van Beilen JB, Luz AP, Pellizari V, Labbe D, Greer CW. 2002. Prevalence of alkane monooxygenase genes in Arctic and Antarctic hydrocarbon-contaminated and pristine soils. FEMS Microbiol Ecol 41(2):141-150.
50. Wiechert W, Siefke C, de Graaf AA, Marx A. 1997. Bidirectional reaction steps in metabolic networks: II. Flux estimation and statistical analysis. Biotechnol Bioeng 55(1):118-135.
51. You L, Page L, Feng X, Berla B, Pakrasi HB, Tang YJ. 2012. Metabolic pathway confirmation and discovery through 13C-labeling of proteinogenic amino acids. J Vis Exp 59:e 3583.
52. Young JD, Shastri AA, Stephanopoulos G, Morgan JA. 2011. Mapping photoautotrophic metabolism with isotopically nonstationary 13C flux analysis. Metab Eng 13(6):656-665.
53. Zaitsev GM, Uotila JS, Tsitko IV, Lobanok AG, Salkinoja-Salonen MS. 1995. Utilization of Halogenated Benzenes, Phenols, and Benzoates by Rhodococcus opacus GM-14. Appl Environ Microbiol 61(12):4191-4201.
54. Zhang Y, Adams IP, Ratledge C. 2007. Malic enzyme: The controlling activity for lipid production? Overexpression of malic enzyme in Mucor circinelloides leads to a 2.5-fold increase in lipid accumulation. Microbiology 153:2013-2025.
55. Zhang Y, Lin Z, Liu Q, Li Y, Wang Z, Ma H, Chen T, Zhao X. 2014. Engineering of Serine-Deamination pathway, Entner-Doudoroff pathway and pyruvate dehydrogenase complex to improve poly(3-hydroxybutyrate) production in Escherichia coli. Microb Cell Fact 13(1):172.
56. 13C-fluxomics. Nucleic Acids Res 43(D1):D549-D557.
57. 13C-labeled acetate and glucose using GC-MS and powerful flux calculation method. J Biotechnol 101(2):101-117.
58. Zhuang W-Q, Yi S, Feng X, Zinder SH, Tang YJ, Alvarez-Cohen L. 2011. Selective utilization of exogenous amino acids by Dehalococcoides ethenogenes strain 195 and its effects on growth and dechlorination activity. Appl Environ Microbiol 77(21):7797-7803.