Global transcriptome response to ionic liquid by a tropical rain forest soil bacterium, Enterobacter lignolyticus

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 32, 2012, Pages

  Khudyakov, Jane I ^a,b   D'Haeseleer, Patrik ^a,b   Borglin, Sharon E ^c   DeAngelis, Kristen M ^a,c   Woo, Hannah ^a,c   Lindquist, Erika A ^d   Hazen, Terry C ^a,c   Simmons, Blake A ^a,e   Thelen, Michael P ^a,b  

^a JOINT BIOENERGY INSTITUTE   (United States)

^b LAWRENCE LIVERMORE NATIONAL LABORATORY   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^d DOE JOINT GENOME INSTITUTE   (United States)

^e SANDIA NATIONAL LABORATORIES   (United States)

Author keywords

Differential gene expression; Membrane lipids; Osmotic stress osmolytes; Whole genome metabolic reconstruction

Indexed keywords

1 ETHYL 3 METHYLIMIDAZOLIUMCHLORIDE; CYCLOPROPANE; FATTY ACID; IONIC LIQUID; LIGNOCELLULOSE; PORIN; SCAVENGER; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BACTERIUM ISOLATION; BIOENGINEERING; CELL MEMBRANE; CONTROLLED STUDY; DOWN REGULATION; ENTEROBACTER; ENTEROBACTER LIGNOLYTICUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; RNA SEQUENCE; SOIL MICROFLORA; TROPICAL RAIN FOREST; UPREGULATION;

BASE SEQUENCE; BIOENGINEERING; BIOFUELS; DRUG RESISTANCE; ENTEROBACTER; GENE EXPRESSION REGULATION, BACTERIAL; IMIDAZOLES; IONIC LIQUIDS; MOLECULAR SEQUENCE DATA; PHOSPHOLIPIDS; SEQUENCE ANALYSIS, RNA; SOIL MICROBIOLOGY; TRANSCRIPTOME; TREES; TROPICAL CLIMATE;

BACTERIA (MICROORGANISMS); ENTEROBACTER;

EID: 84864680611     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1112750109     Document Type: Article

References (78)

1. US Department of Energy (2006) Breaking the Biological Barriers to Cellulosic Ethanol: A Joint Research Agenda. Report from the December 2005 Workshop, DOE/SC-0095, US Department of Energy Office of Science. Available at www.genomicscience.energy.gov/biofuels/2005workshop/.
2. Simmons BA, Loque D, Blanch HW (2008) Next-generation biomass feedstocks for biofuel production. Genome Biol 9:242.
3. Himmel ME, et al. (2007) Biomass recalcitrance: Engineering plants and enzymes for biofuels production. Science 315:804-807.
4. Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850-861.
5. Achyuthan KE, et al. (2010) Supramolecular self-assembled chaos: Polyphenolic lignin's barrier to cost-effective lignocellulosic biofuels. Molecules 15:8641-8688.
6. da Costa Sousa L, Chundawat SP, Balan V, Dale BE (2009) 'Cradle-to-grave' assessment of existing lignocellulose pretreatment technologies. Curr Opin Biotechnol 20: 339-347.
7. Li C, et al. (2010) Comparison of dilute acid and ionic liquid pretreatment of switchgrass: Biomass recalcitrance, delignification and enzymatic saccharification. Bioresour Technol 101:4900-4906.
8. Cheng G, et al. (2011) Transition of cellulose crystalline structure and surface morphology of biomass as a function of ionic liquid pretreatment and its relation to enzymatic hydrolysis. Biomacromolecules 12:933-941.
9. Singh S, Simmons BA, Vogel KP (2009) Visualization of biomass solubilization and cellulose regeneration during ionic liquid pretreatment of switchgrass. Biotechnol Bioeng 104:68-75.
10. Mora-Pale M, Meli L, Doherty TV, Linhardt RJ, Dordick JS (2011) Room temperature ionic liquids as emerging solvents for the pretreatment of lignocellulosic biomass. Biotechnol Bioeng 108:1229-1245.
11. Pham TP, Cho CW, Yun YS (2010) Environmental fate and toxicity of ionic liquids: A review. Water Res 44:352-372.
12. Quijano G, Couvert A, Amrane A (2010) Ionic liquids: Applications and future trends in bioreactor technology. Bioresour Technol 101:8923-8930.
13. Romero A, Santos A, Tojo J, Rodríguez A (2008) Toxicity and biodegradability of imidazolium ionic liquids. J Hazard Mater 151:268-273.
14. Xu Q, Singh A, Himmel ME (2009) Perspectives and new directions for the production of bioethanol using consolidated bioprocessing of lignocellulose. Curr Opin Biotechnol 20:364-371.
15. Elkins JG, Raman B, Keller M (2010) Engineered microbial systems for enhanced conversion of lignocellulosic biomass. Curr Opin Biotechnol 21:657-662.
16. Margeot A, Hahn-Hagerdal B, Edlund M, Slade R, Monot F (2009) New improvements for lignocellulosic ethanol. Curr Opin Biotechnol 20:372-380.
17. Connor MR, Liao JC (2009) Microbial production of advanced transportation fuels in non-natural hosts. Curr Opin Biotechnol 20:307-315.
18. Nicolaou SA, Gaida SM, Papoutsakis ET (2010) A comparative view of metabolite and substrate stress and tolerance in microbial bioprocessing: From biofuels and chemicals, to biocatalysis and bioremediation. Metab Eng 12:307-331.
19. Docherty KM, Kulpa CF (2005) Toxicity and antimicrobial activity of imidazolium and pyridinium ionic liquids. Green Chem 7:185-189. (Pubitemid 40592193)
20. Ganske F, Bornscheuer UT (2006) Growth of Escherichia coli, Pichia pastoris and Bacillus cereus in the presence of the ionic liquids [BMIM][BF4] and [BMIM][PF6] and Organic Solvents. Biotechnol Lett 28:465-469.
21. Lee SM, Chang WJ, Choi AR, Koo YM (2005) Influence of ionic liquids on the growth of Escherichia coli. Korean J Chem Eng 22:687-690.
22. Matsumoto M, Mochiduki K, Kondo K (2004) Toxicity of ionic liquids and organic solvents to lactic acid-producing bacteria. J Biosci Bioeng 98:344-347. (Pubitemid 40013199)
23. DeAngelis KM, et al. (2011) Characterization of trapped lignin-degrading microbes in tropical forest soil. PLoS ONE 6:e19306.
24. Allgaier M, et al. (2010) Targeted discovery of glycoside hydrolases from a switchgrass-adapted compost community. PLoS ONE 5:e8812.
25. Reddy AP, et al. (2011) Bioenergy feedstock-specific enrichment of microbial populations during high-solids thermophilic deconstruction. Biotechnol Bioeng 108:2088-2098.
26. Deangelis KM, et al. (2011) Complete genome sequence of "Enterobacter lignolyticus" SCF1. Stand Genomic Sci 5:69-85.
27. Zavrel M, Bross D, Funke M, Büchs J, Spiess AC (2009) High-throughput screening for ionic liquids dissolving (ligno-)cellulose. Bioresour Technol 100:2580-2587.
28. Bochner BR (2003) New technologies to assess genotype-phenotype relationships. Nat Rev Genet 4:309-314.
29. Bochner BR, Savageau MA (1977) Generalized indicator plate for genetic, metabolic, and taxonomic studies with microorganisms. Appl Environ Microbiol 33:434-444. (Pubitemid 8099796)
30. Borglin S, et al. (2012) Application of phenotypic microarrays to environmental microbiology. Curr Opin Biotechnol 23:41-48.
31. Borglin S, Joyner D, Jacobsen J, Mukhopadhyay A, Hazen TC (2009) Overcoming the anaerobic hurdle in phenotypic microarrays: Generation and visualization of growth curve data for Desulfovibrio vulgaris Hildenborough. J Microbiol Methods 76:159-168.
32. Zwietering MH, Jongenburger I, Rombouts FM, van't Riet K (1990) Modeling of the bacterial growth curve. Appl Environ Microbiol 56:1875-1881. (Pubitemid 20202159)
33. Baba T, et al. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: The Keio collection. Mol Syst Biol 2:1-11.
34. Docherty KM, Dixon JK, Kulpa CF, Jr. (2007) Biodegradability of imidazolium and pyridinium ionic liquids by an activated sludge microbial community. Biodegradation 18:481-493. (Pubitemid 47030027)
35. Empadinhas N, da Costa MS (2008) Osmoadaptation mechanisms in prokaryotes: Distribution of compatible solutes. Int Microbiol 11:151-161.
36. Zhang YM, Rock CO (2008) Membrane lipid homeostasis in bacteria. Nat Rev Microbiol 6:222-233.
37. Cronan JE, Jr. (2002) Phospholipid modifications in bacteria. Curr Opin Microbiol 5:202-205.
38. Ramos JL, et al. (2002) Mechanisms of solvent tolerance in gram-negative bacteria. Annu Rev Microbiol 56:743-768. (Pubitemid 35217473)
39. Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: A revolutionary tool for transcriptomics. Nat Rev Genet 10:57-63.
40. van Vliet AH (2010) Next generation sequencing of microbial transcriptomes: Challenges and opportunities. FEMS Microbiol Lett 302:1-7.
41. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106.
42. Weber H, Polen T, Heuveling J, Wendisch VF, Hengge R (2005) Genome-wide analysis of the general stress response network in Escherichia coli: SigmaS-dependent genes, promoters, and sigma factor selectivity. J Bacteriol 187:1591-1603. (Pubitemid 40289359)
43. Karp PD, Paley S, Romero P (2002) The Pathway Tools software. Bioinformatics 18(Suppl 1):S225-S232. (Pubitemid 41185657)
44. Zafarani-Moattar MT, Sarmad S (2011) Osmotic and activity coefficient of 1-ethyl-3-methylimidazolium chloride in aqueous solutions of tri-potassium phosphate, potassium carbonate, and potassium chloride at T = 298.15 K. Calphad 35:331-341.
45. Ren Q, Chen K, Paulsen IT (2007) TransportDB: A comprehensive database resource for cytoplasmic membrane transport systems and outer membrane channels. Nucleic Acids Res 35(Database issue):D274-D279. (Pubitemid 46056214)
46. Fernandes P, Ferreira BS, Cabral JM (2003) Solvent tolerance in bacteria: Role of efflux pumps and cross-resistance with antibiotics. Int J Antimicrob Agents 22:211-216. (Pubitemid 37103202)
47. Delcour AH (2009) Outer membrane permeability and antibiotic resistance. Biochim Biophys Acta 1794:808-816.
48. Dunlop MJ, et al. (2011) Engineering microbial biofuel tolerance and export using efflux pumps. Mol Syst Biol 7:487.
49. Davin-Regli A, et al. (2008) Membrane permeability and regulation of drug "influx and efflux" in enterobacterial pathogens. Curr Drug Targets 9:750-759.
50. Chang YY, Cronan JE, Jr. (1999) Membrane cyclopropane fatty acid content is a major factor in acid resistance of Escherichia coli. Mol Microbiol 33:249-259.
51. Shabala L, Ross T (2008) Cyclopropane fatty acids improve Escherichia coli survival in acidified minimal media by reducing membrane permeability to H+ and enhanced ability to extrude H+. Res Microbiol 159:458-461.
52. Zhao Y, et al. (2003) Expression of a cloned cyclopropane fatty acid synthase gene reduces solvent formation in Clostridium acetobutylicum ATCC 824. Appl Environ Microbiol 69:2831-2841. (Pubitemid 36560363)
53. Machado MC, López CS, Heras H, Rivas EA (2004) Osmotic response in Lactobacillus casei ATCC 393: Biochemical and biophysical characteristics of membrane. Arch Biochem Biophys 422:61-70. (Pubitemid 38064311)
54. Broadbent JR, Larsen RL, Deibel V, Steele JL (2010) Physiological and transcriptional response of Lactobacillus casei ATCC 334 to acid stress. J Bacteriol 192:2445-2458.
55. Escolar L, Pérez-Martín J, de Lorenzo V (1999) Opening the iron box: Transcriptional metalloregulation by the Fur protein. J Bacteriol 181:6223-6229. (Pubitemid 29512928)
56. Kunin CM, Tong HH, Maher WE (1993) Naturally-occurring, osmo-remedial variants of Escherichia coli. J Med Microbiol 38:216-221. (Pubitemid 23087257)
57. Tschech A, Pfennig N (1984) Growth-yield increase linked to caffeate reduction in Acetobacterium-woodii. Arch Microbiol 137:163-167. (Pubitemid 14157100)
58. Widdel F, Kohring GW, Mayer F (1983) Studies on dissimilatory sulfate-reducing bacteria that decompose fatty-acids. 3. Characterization of the filamentous gliding Desulfonema-Limicola Gen-Nov Sp-Nov, and Desulfonema-Magnum Sp-Nov. Arch Microbiol 134:286-294.
59. Janssen PH, Schuhmann A, Mörschel E, Rainey FA (1997) Novel anaerobic ultramicrobacteria belonging to the Verrucomicrobiales lineage of bacterial descent isolated by dilution culture from anoxic rice paddy soil. Appl Environ Microbiol 63:1382-1388.
60. White DC, Ringelberg DB (1998) Signature Lipid Biomarker Analysis. Techniques in Microbial Ecology (Oxford Univ Press, New York), pp 255-272.
61. Guckert JB, Antworth CP, Nichols PD, White DC (1985) Phospholipid, ester-linked fatty-acid profiles as reproducible assays for changes in prokaryotic community structure of estuarine sediments. FEMS Microbiol Ecol 31:147-158.
62. Pfiffner SM, et al. (2006) Deep subsurface microbial biomass and community structure in Witwatersrand Basin mines. Geomicrobiol J 23:431-442. (Pubitemid 44458115)
63. Griffiths BS, Ritz K, Ebblewhite N, Dobson G (1999) Soil microbial community structure: Effects of substrate loading rates. Soil Biol Biochem 31:145-153. (Pubitemid 28548175)
64. Salomonova S, et al. (2003) Determination of phospholipid fatty acids in sediments. Chemica 42:39-49.
65. Steger K, Jarvis A, Smårs S, Sundh I (2003) Comparison of signature lipid methods to determine microbial community structure in compost. J Microbiol Methods 55:371-382. (Pubitemid 37177035)
66. Moore-Kucera J, Dick RP (2008) PLFA profiling of microbial community structure and seasonal shifts in soils of a Douglas-fir chronosequence. Microb Ecol 55:500-511. (Pubitemid 351421338)
67. Cusack DF, Silver WL, Torn MS, Burton SD, Firestone MK (2011) Changes in microbial community characteristics and soil organic matter with nitrogen additions in two tropical forests. Ecology 92:621-632.
68. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760.
69. Robinson MD, Oshlack A (2010) A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol 11:R25.
70. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57:289-300.
71. Caspi R, et al. (2008) The MetaCyc Database of metabolic pathways and enzymes and the BioCyc collection of Pathway/Genome Databases. Nucleic Acids Res 36(Database issue):D623-D631. (Pubitemid 351149796)
72. Markowitz VM, et al. (2010) The integrated microbial genomes system: An expanding comparative analysis resource. Nucleic Acids Res 38(Database issue):D382-D390.
73. Aziz RK, et al. (2008) The RAST Server: Rapid annotations using subsystems technology. BMC Genomics 9:75.
74. Karp PD, et al. (2005) Expansion of the BioCyc collection of pathway/genome databases to 160 genomes. Nucleic Acids Res 33:6083-6089. (Pubitemid 41742547)
75. Dehal PS, et al. (2010) MicrobesOnline: An integrated portal for comparative and functional genomics. Nucleic Acids Res 38(Database issue):D396-D400.
76. Ramakers C, Ruijter JM, Deprez RH, Moorman AF (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339:62-66. (Pubitemid 36263221)
77. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45.
78. Ouellet M, Adams PD, Keasling JD, Mukhopadhyay A (2009) A rapid and inexpensive labeling method for microarray gene expression analysis. BMC Biotechnol 9:97.