Adaptive engineering of a hyperthermophilic archaeon on CO and discovering the underlying mechanism by multi-omics analysis

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Lee, Seong Hyuk ^a,b   Kim, Min Sik ^c   Lee, Jae Hak ^a   Kim, Tae Wan ^a,b   Bae, Seung Seob ^a   Lee, Sung Mok ^a   Jung, Hae Chang ^a,b   Yang, Tae Jun ^a   Choi, Ae Ran ^a   Cho, Yong Jun ^d   Lee, Jung Hyun ^a,b   Kwon, Kae Kyoung ^a,b   Lee, Hyun Sook ^a,b   Kang, Sung Gyun ^a,b  

^a Korea Research Institute of Ships and Ocean Engineering   (South Korea)

^b University of Science and Technology (UST)   (South Korea)

^c Korea Institute of Energy Research (KIER)   (South Korea)

^d ChunLab Inc   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON MONOXIDE; HYDROGEN;

ADAPTATION; ARCHAEAL GENE; ARCHAEAL GENOME; DNA METHYLATION; ENERGY METABOLISM; EPIGENETICS; GENE EXPRESSION PROFILING; GENETICS; GENOMICS; HEAT; METABOLIC ENGINEERING; METABOLISM; MUTATION; OXIDATION REDUCTION REACTION; PROCEDURES; THERMOCOCCUS;

ADAPTATION, PHYSIOLOGICAL; CARBON MONOXIDE; DNA METHYLATION; ENERGY METABOLISM; EPIGENOMICS; GENE EXPRESSION PROFILING; GENES, ARCHAEAL; GENOME, ARCHAEAL; GENOMICS; HOT TEMPERATURE; HYDROGEN; METABOLIC ENGINEERING; MUTATION; OXIDATION-REDUCTION; THERMOCOCCUS;

EID: 84962581771     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep22896     Document Type: Article

References (54)

1. Lee, J. W., Kim, T. Y., Jang, Y. S., Choi, S. & Lee, S. Y. Systems metabolic engineering for chemicals and materials. Trends in Biotechnol. 29, 370-378 (2011).
2. Aakar, Z. P., Turanli-Yildiz, B., Alkim, C. & Yilmaz, S. Evolutionary engineering of Saccharomyces cerevisiae for improved industrially important properties. FEMS Yeast Res. 12, 171-182 (2012).
3. Winkler, J. D. & Kao, K. C. Recent advances in the evolutionary engineering of industrial biocatalysts. Genomics 104, 406-411 (2014).
4. Adams, J. & Rosenzweig, F. Experimental microbial evolution: history and conceptual underpinnings. Genomics 104, 393-398 (2014).
5. Conrad, T. M., Lewis, N. E. & Palsson, B. . Microbial laboratory evolution in the era of genome-scale science. Mol Syst Biol. 7, 509 (2011).
6. Hindr T., Knibbe, C., Beslon, G. & Schneider, D. New insights into bacterial adaptation through in vivo and in silico experimental evolution. Nat Rev Microbiol. 10, 352-365 (2012).
7. Dettman, J. R. et al. Evolutionary insight from whole-genome sequencing of experimentally evolved microbes. Mol Ecol. 21, 2058-2077 (2012).
8. Latif, H. et al. Adaptive evolution of Thermotoga maritima reveals plasticity of the ABC transporter network. Appl. Environ. Microbiol. 81, 5477-5485 (2015).
9. Hallenbeck, P. C., Abo-Hashesh, M. & Ghosh, D. Strategies for improving biological hydrogen production. Bioresour Technol. 110, 1-9 (2012).
10. Nath, K. & Das, D. Improvement of fermentative hydrogen production: various approaches. Appl. Microbiol. Biotechnol. 65, 520-529 (2004).
11. Amend, J. P. & Shock, E. L. Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and Bacteria. FEMS Microbiol Rev. 25, 175-243 (2001).
12. Lee H. S. et al. The complete genome sequence of Thermococcus onnurineus NA1 reveals a mixed heterotrophic and carboxydotrophic metabolism. J. Bacteriol. 190, 7491-7499 (2008).
13. Rittmann, S. K.-M. R. et al. One-carbon substrate-based biohydrogen production: microbes, mechanism, and productivity. Biotechnol. Adv. 33, 165-177 (2015).
14. Kim, M. S. et al. CO-dependent H2 production by genetically engineered Thermococcus onnurineus NA1. Appl. Environ. Microbiol. 79, 2048-2053 (2013).
15. Kim, M.-S. et al. A novel CO-responsive transcriptional regulator and enhanced H2 production by an engineered Thermococcus onnurineus NA1 strain. Appl. Environ. Microbiol. 81, 1708-1714 (2015).
16. Lee, S. H. et al. Screening of a novel strong promoter by RNA sequencing and its application to H2 production in a hyperthermophilic archaeon. Appl. Microbiol. Biotechnol. 99, 4085-4092 (2015).
17. Lee, S. H. et al. Comparison of CO-dependent H2 production with strong promoters in Thermococcus onnurineus NA1. Appl. Microbiol. Biotechnol. 98, 979-986 (2014).
18. Flusberg, B. A. et al. Direct detection of DNA methylation during single-molecule, real-time sequencing. Nat Methods. 7, 461-465 (2010).
19. Casades, J. & Low, D. Epigenetic gene regulation in the bacterial world. Microbiol. Mol. Biol. Rev. 70, 830-856 (2006).
20. Fang, G. et al. Genome-wide mapping of methylated adenine residues in pathogenic Escherichia coli using single-molecule real-time sequencing. Nat. Biotechnol. 30, 1232-1239 (2012).
21. Bendall, M. L. et al. Exploring the roles of DNA methylation in the metal-reducing bacterium Shewanella oneidensis MR-1. J. Bacteriol. 195, 4966-4974 (2013).
22. Ouellette, M., Jackson, L., Chimileski, S. & Papke, R. T. Genome-wide DNA methylation analysis of Haloferax volcanii H26 and identification of DNA methyltransferase related PD-(D/E)XK nuclease family protein HVO-A0006. Front. Microbiol. 6, 1-11 (2015).
23. Torkelson, J. et al. Genome-wide hypermutation in a subpopulation of stationary-phase cells underlies recombination-dependent adaptive mutation. EMBO J. 16, 3303-3311 (1997).
24. Weiner, L. & Model, P. Role of an Escherichia coli stress-response operon in stationary-phase survival. Proc. Natl. Acad. Sci. USA 91, 2191-2195 (1994).
25. Kivisaar, M. Stationary phase mutagenesis: Mechanisms that accelerate adaptation of microbial populations under environmental stress. Environ Microbiol 5, 814-827 (2003).
26. Loewe, L., Textor, V. & Scherer, S. High deleterious genomic mutation rate in stationary phase of Escherichia coli. Science 302, 1558-1560 (2003).
27. Wolf, Y. I., Makarova, K. S., Yutin, N. & Koonin, E. V. Updated clusters of orthologous genes for Archaea: a complex ancestor of the Archaea and the byways of horizontal gene transfer. Biol. Direct 7, 46 (2012).
28. Nad, D., Oxidoreductase, P. H. S., Schut, G. J., Bridger, S. L. & Adams, M. W. W. Insights into the metabolism of elemental sulfur by the hyperthermophilic archaeon Pyrococcus furiosus: characterization of a coenzyme A-dependent NAD(P)H sulfur oxidoreductase. J. Bacteriol. 189, 4431-4441 (2007).
29. Santangelo, T. J., uboov L. & Reeve, J. N. Deletion of alternative pathways for reductant recycling in Thermococcus kodakarensis increases hydrogen production. Mol. Microbiol. 81, 897-911 (2011).
30. Kanai, T. et al. Distinct physiological roles of the three [NiFe]-hydrogenase orthologs in the hyperthermophilic archaeon Thermococcus kodakarensis. J. Bacteriol. 193, 3109-3116 (2011).
31. Lim, J. K., Mayer, F., Kang, S. G. & Mler, V. Energy conservation by oxidation of formate to carbon dioxide and hydrogen via a sodium ion current in a hyperthermophilic archaeon. Proc. Natl. Acad. Sci. USA 111, 11497-11502 (2014).
32. Kaminski, L. & Eichler, J. Haloferax volcanii N-glycosylation: Delineating the pathway of dTDP-rhamnose biosynthesis. Plos One. 9, e97441 (2014).
33. Lipscomb, G. L. et al. SurR: A transcriptional activator and repressor controlling hydrogen and elemental sulphur metabolism in Pyrococcus furiosus. Mol. Microbiol. 71, 332-349 (2009).
34. Kim, Y. J. et al. Formate-driven growth coupled with H2 production. Nature 467, 352-355 (2010).
35. Mackwan, R. R., Carver, G. T., Kissling, G. E., Drake, J. W. & Grogan, D. W. The rate and character of spontaneous mutation in Thermus thermophilus. Genetics 180, 17-25 (2008).
36. Grogan, D. W., Carver, G. T. & Drake, J. W. Genetic fidelity under harsh conditions: analysis of spontaneous mutation in the thermoacidophilic archaeon Sulfolobus acidocaldarius. Proc. Natl. Acad. Sci. USA 98, 7928-7933 (2001).
37. Hochheimer, A., Hedderich, R. & Thauer, R. K. The DNA binding protein Tfx from Methanobacterium thermoautotrophicum: structure, DNA binding properties and transcriptional regulation. Mol. Microbiol. 31, 641-650 (1999).
38. Ehrlich, M. et al. DNA methylation in thermophilic bacteria: N4-methylcytosine, 5-methylcytosine, and N5methyladenine. Nucleic Acids Res. 13, 1399-1412 (1985).
39. Ehrlich, M., Wilson, G. G., Kuo, K. C. & Gehrke, C. W. N4-methylcytosine as a minor base in bacterial DNA. J. Bacteriol. 169, 939-943 (1987).
40. Connolly, B. A., Fogg, M. J., Shuttleworth, G. & Wilson, B. T. Uracil recognition by archaeal family B DNA polymerases. Biochem. Soc. Trans. 31, 699-702 (2003).
41. Cho, W. et al. Optimal design and operation of a natural gas tri-reforming reactor for DME synthesis. Catal. Today 139, 261-267 (2009).
42. Bae, S. S. et al. Thermococcus onnurineus sp. nov., a hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent area at the PACMANUS field. J. Microbiol. Biotechnol. 16, 1826-1831 (2006).
43. Holden, J. F. et al. Diversity among three novel groups of hyperthermophilic deep-sea Thermococcus species from three sites in the northeastern Pacific Ocean. FEMS Microbiol. Ecol. 36, 51-60 (2001).
44. Sokolova, T. G. et al. The first evidence of anaerobic CO oxidation coupled with H2 production by a hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent. Extremophiles 8, 317-323 (2004).
45. Balch, W. E. & Wolfe, R. S. New approach to the cultivation of methanogenic bacteria: 2-mercaptoethanesulfonic acid (HS-CoM)-dependent growth of Methanobacterium ruminantium in a pressureized atmosphere. Appl. Environ. Microbiol. 32, 781-791 (1976).
46. Jeong, J. Y. et al. One-step sequence-and ligation-independent cloning as a rapid and versatile cloning method for functional genomics studies. Appl. Environ. Microbiol. 78, 5440-5443 (2012).
47. Matsumi, R., Manabe, K., Fukui, T., Atomi, H. & Imanaka, T. Disruption of a sugar transporter gene cluster in a hyperthermophilic archaeon using a host-marker system based on antibiotic resistance. J. Bacteriol. 189, 2683-2691 (2007).
48. Riggs, S. S. & Heindel, T. J. Measuring carbon monoxide gas-liquid mass transfer in a stirred tank reactor for syngas fermentation. Biotechnol. Prog. 22, 903-906 (2006).
49. Kundu, S., Premer, S. A., Hoy, J. A., Trent, J. T. & Hargrove, M. S. Direct measurement of equilibrium constants for high-affinity hemoglobins. Biophys. J. 84, 3931-3940 (2003).
50. Eid, J. et al. Real-time DNA sequencing from single polymerase molecules. Science 323, 133-138 (2009).
51. Schroeder, A. et al. The RIN: an RNA integrity number for assigning integrity values to RNA measurements. BMC Mol. Biol. 7, 3 (2006).
52. Anders, S. & Huber, W. Differential expression analysis for sequence count data. Genome Biol. 11, R106 (2010).
53. Robinson, M. D., Mccarthy, D. J. & Smyth, G. K. edgeR : a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 26, 139-140 (2010).
54. Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402 (1997).