Discovery of ethanol-responsive small RNAs in Zymomonas mobilis

Applied and Environmental Microbiology

Volumn 80, Issue 14, 2014, Pages 4189-4198

  Cho, Seung Hee ^a   Lei, Roy ^a   Henninger, Trey D ^a   Contreras, Lydia M ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

METABOLISM;

AEROBIC AND ANAEROBIC CONDITIONS; COMPUTATIONAL PREDICTIONS; DIFFERENTIAL EXPRESSIONS; ENERGY APPLICATIONS; EXPERIMENTAL APPROACHES; METABOLIC FUNCTION; TRANSCRIPTIONAL REGULATOR; TRANSCRIPTOME ANALYSIS;

ETHANOL;

BACTERIUM; BIOFUEL; COMPUTER SIMULATION; ETHANOL; FERMENTATION; GENE EXPRESSION; METABOLISM; MOLECULAR ANALYSIS; RNA;

ALCOHOL; BACTERIAL RNA; CULTURE MEDIUM; GLUCOSE;

BIOLOGY; CHROMOSOME MAP; CULTURE MEDIUM; FERMENTATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HIGH THROUGHPUT SEQUENCING; METABOLISM; SEQUENCE ANALYSIS; ZYMOMONAS;

CHROMOSOME MAPPING; COMPUTATIONAL BIOLOGY; CULTURE MEDIA; ETHANOL; FERMENTATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GLUCOSE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; RNA, BACTERIAL; SEQUENCE ANALYSIS, RNA; TRANSCRIPTION, GENETIC; ZYMOMONAS;

EID: 84903155275     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00429-14     Document Type: Article

References (55)

1. Osman YA, Ingram LO. 1985. Mechanism of ethanol inhibition of fermentation in Zymomonas mobilis CP4. J. Bacteriol. 164:173-180.
2. Stanley D, Bandara A, Fraser S, Chambers PJ, Stanley GA. 2010. The ethanol stress response and ethanol tolerance of Saccharomyces cerevisiae. J. Appl. Microbiol. 109:13-24. http://dx.doi.org/10.1111/j.1365-2672.2009.04657.x.
3. Rogers PL, Jeon YJ, Lee KJ, Lawford HG. 2007. Zymomonas mobilis for fuel ethanol and higher value products. Adv. Biochem. Eng. Biotechnol. 108:263-288. http://dx.doi.org/10.1007/10_2007_060.
4. Yang S, Tschaplinski TJ, Engle NL, Carroll SL, Martin SL, Davison BH, Palumbo AV, Rodriguez M, Jr, Brown SD. 2009. Transcriptomic and metabolomic profiling of Zymomonas mobilis during aerobic and anaerobic fermentations. BMC Genomics 10:34. http://dx.doi.org/10.1186 /1471-2164-10-34.
5. Moreau RA, Powell MJ, Fett WF, Whitaker BD. 1997. The effect of ethanol and oxygen on the growth of Zymomonas mobilis and the levels of hopanoids and other membrane lipids. Curr. Microbiol. 35:124-128. http://dx.doi.org/10.1007/s002849900224.
6. Swings J, De Ley J. 1977. The biology of Zymomonas. Bacteriol. Rev. 41:1-46.
7. Bringer S, Finn R, Sahm H. 1984. Effect of oxygen on the metabolism of Zymomonas mobilis. Arch. Microbiol. 139:376-381. http://dx.doi.org/10.1007/BF00408383.
8. Widiastuti H, Kim JY, Selvarasu S, Karimi IA, Kim H, Seo JS, Lee DY. 2011. Genome-scale modeling and in silico analysis of ethanologenic bacteria Zymomonas mobilis. Biotechnol. Bioeng. 108:655-665. http://dx.doi.org/10.1002/bit.22965.
9. Jeffries TW. 2005. Ethanol fermentation on the move. Nat. Biotechnol. 23:40-41. http://dx.doi.org/10.1038/nbt0105-40.
10. Carey VC, Ingram LO. 1983. Lipid composition of Zymomonas mobilis: effects of ethanol and glucose. J. Bacteriol. 154:1291-1300.
11. Yang S, Pappas KM, Hauser LJ, Land ML, Chen GL, Hurst GB, Pan C, Kouvelis VN, Typas MA, Pelletier DA, Klingeman DM, Chang YJ, Samatova NF, Brown SD. 2009. Improved genome annotation for Zymomonas mobilis. Nat. Biotechnol. 27:893-894. http://dx.doi.org/10.1038/nbt1009-893.
12. Zhang M, Eddy C, Deanda K, Finkelstein M, Picataggio S. 1995. Metabolic engineering of a pentose metabolism pathway in ethanologenic Zymomonas mobilis. Science 267:240-243. http://dx.doi.org/10.1126 /science.267.5195.240.
13. Wassarman KM. 2002. Small RNAs in bacteria: diverse regulators of gene expression in response to environmental changes. Cell 109:141-144. http: //dx.doi.org/10.1016/S0092-8674(02)00717-1.
14. Livny J, Waldor MK. 2007. Identification of small RNAs in diverse bacterial species. Curr. Opin. Microbiol. 10:96-101. http://dx.doi.org/10.1016/j.mib.2007.03.005.
15. Aiba H. 2007. Mechanism of RNA silencing by Hfq-binding small RNAs. Curr. Opin. Microbiol. 10:134-139. http://dx.doi.org/10.1016/j.mib.2007.03.010.
16. Gudapaty S, Suzuki K, Wang X, Babitzke P, Romeo T. 2001. Regulatory interactions of Csr components: the RNA binding protein CsrA activates csrB transcription in Escherichia coli. J. Bacteriol. 183:6017-6027. http: //dx.doi.org/10.1128/JB.183.20.6017-6027.2001.
17. Storz G, Vogel J, Wassarman KM. 2011. Regulation by small RNAs in bacteria: expanding frontiers. Mol. Cell 43:880-891. http://dx.doi.org/10.1016/j.molcel.2011.08.022.
18. Altuvia S, Weinstein-Fischer D, Zhang A, Postow L, Storz G. 1997. A small, stable RNA induced by oxidative stress: role as a pleiotropic regulator and antimutator. Cell 90:43-53. http://dx.doi.org/10.1016/S0092-8674(00)80312-8.
19. Gottesman S, McCullen CA, Guillier M, Vanderpool CK, Majdalani N, Benhammou J, Thompson KM, FitzGerald PC, Sowa NA, FitzGerald DJ. 2006. Small RNA regulators and the bacterial response to stress. Cold Spring Harbor Symp. Quant. Biol. 71:1-11. http://dx.doi.org/10.1101/sqb.2006.71.016.
20. Georg J, Hess WR. 2011. Regulatory RNAs in cyanobacteria: developmental decisions, stress responses and a plethora of chromosomally encoded cis-antisense RNAs. Biol. Chem. 392:291-297. http://dx.doi.org/10.1515/BC.2011.046.
21. Sridhar J, Gunasekaran P. 2013. Computational small RNA prediction in bacteria. Bioinform. Biol. Insights 7:83-95. http://dx.doi.org/10.4137/BBI.S11213.
22. Altuvia S. 2007. Identification of bacterial small non-coding RNAs: experimental approaches. Curr. Opin. Microbiol. 10:257-261. http://dx.doi.org/10.1016/j.mib.2007.05.003.
23. Tsai CH, Baranowski C, Livny J, McDonough KA, Wade JT, Contreras LM. 2013. Identification of novel sRNAs in mycobacterial species. PLoS One 8:e79411. http://dx.doi.org/10.1371/journal.pone.0079411.
24. Vogel J, Luisi BF. 2011. Hfq and its constellation of RNA. Nat. Rev. Microbiol. 9:578-589. http://dx.doi.org/10.1038/nrmicro2615.
25. Sittka A, Lucchini S, Papenfort K, Sharma CM, Rolle K, Binnewies TT, Hinton JC, Vogel J. 2008. Deep sequencing analysis of small noncodingRNA and mRNA targets of the global post-transcriptional regulator, Hfq. PLoS Genet. 4:e1000163. http://dx.doi.org/10.1371/journal.pgen.1000163.
26. Yang S, Pelletier DA, Lu TY, Brown SD. 2010. The Zymomonas mobilis regulator hfq contributes to tolerance against multiple lignocellulosic pretreatment inhibitors. BMC Microbiol. 10:135. http://dx.doi.org/10.1186 /1471-2180-10-135.
27. Chen Y, Indurthi DC, Jones SW, Papoutsakis ET. 2011. Small RNAs in the genus Clostridium. mBio 2:e00340-10. http://dx.doi.org/10.1128 /mBio.00340-10.
28. Borden JR, Jones SW, Indurthi D, Chen Y, Terry Papoutsakis E. 2010. A genomic-library based discovery of a novel, possibly synthetic, acidtolerance mechanism in Clostridium acetobutylicum involving noncoding RNAs and ribosomal RNA processing. Metab. Eng. 12:268-281. http://dx.doi.org/10.1016/j.ymben.2009.12.004.
29. Venkataramanan KP, Jones SW, McCormick KP, Kunjeti SG, Ralston MT, Meyers BC, Papoutsakis ET. 2013. The Clostridium small RNome that responds to stress: the paradigm and importance of toxic metabolite stress in C. acetobutylicum. BMC Genomics 14:849. http://dx.doi.org/10.1186/1471-2164-14-849.
30. Seo JS, Chong H, Park HS, Yoon KO, Jung C, Kim JJ, Hong JH, Kim H, Kim JH, Kil JI, Park CJ, Oh HM, Lee JS, Jin SJ, Um HW, Lee HJ, Oh SJ, Kim JY, Kang HL, Lee SY, Lee KJ, Kang HS. 2005. The genome sequence of the ethanologenic bacterium Zymomonas mobilis ZM4. Nat. Biotechnol. 23:63-68. http://dx.doi.org/10.1038/nbt1045.
31. DiChiara JM, Contreras-Martinez LM, Livny J, Smith D, McDonough KA, Belfort M. 2010. Multiple small RNAs identified in Mycobacterium bovis BCG are also expressed in Mycobacterium tuberculosis and Mycobacterium smegmatis. Nucleic Acids Res. 38:4067-4078. http://dx.doi.org /10.1093/nar/gkq101.
32. Li H, Durbin R. 2010. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26:589-595. http://dx.doi.org /10.1093/bioinformatics/btp698.
33. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP. 2011. Integrative genomics viewer. Nat. Biotechnol. 29:24-26. http://dx.doi.org/10.1038/nbt.1754.
34. Beauregard A, Smith EA, Petrone BL, Singh N, Karch C, McDonough KA, Wade JT. 2013. Identification and characterization of small RNAs in Yersinia pestis. RNA Biol. 10:397-405. http://dx.doi.org/10.4161/rna.23590.
35. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9:357-359. http://dx.doi.org/10.1038/nmeth.1923.
36. Gottesman S. 2005. Micros for microbes: non-coding regulatory RNAs in bacteria. Trends Genet. 21:399-404. http://dx.doi.org/10.1016/j.tig.2005.05.008.
37. Várallyay E, Burgyan J, Havelda Z. 2008. MicroRNA detection by northern blotting using locked nucleic acid probes. Nat. Protoc. 3:190-196. http://dx.doi.org/10.1038/nprot.2007.528.
38. Livny J. 2012. Bioinformatic discovery of bacterial regulatory RNAs using SIPHT. Methods Mol. Biol. 905:3-14. http://dx.doi.org/10.1007/978-1-61779-949-5_1.
39. Vogel J, Sharma CM. 2005. How to find small non-coding RNAs in bacteria. Biol. Chem. 386:1219-1238. http://dx.doi.org/10.1515/BC.2005.140.
40. Lamichhane G, Arnvig KB, McDonough KA. 2013. Definition and annotation of (myco)bacterial non-coding RNA. Tuberculosis (Edinb.) 93: 26-29. http://dx.doi.org/10.1016/j.tube.2012.11.010.
41. Olivarius S, Plessy C, Carninci P. 2009. High-throughput verification of transcriptional starting sites by Deep-RACE. Biotechniques 46:130-132. http://dx.doi.org/10.2144/000113066.
42. Thanonkeo P, Sootsuwan K, Leelavacharamas V, Yamada M. 2007. Cloning and transcriptional analysis of groES and groEL in ethanolproducing bacterium Zymomonas mobilis TISTR 548. Pak. J. Biol. Sci. 10:13-22. http://dx.doi.org/10.3923/pjbs.2007.13.22.
43. An H, Scopes RK, Rodriguez M, Keshav KF, Ingram LO. 1991. Gel electrophoretic analysis of Zymomonas mobilis glycolytic and fermenta-tive enzymes: identification of alcohol dehydrogenase II as a stress protein. J. Bacteriol. 173:5975-5982.
44. Yang S, Pan C, Tschaplinski TJ, Hurst GB, Engle NL, Zhou W, Dam P, Xu Y, Rodriguez M, Jr, Dice L, Johnson CM, Davison BH, Brown SD. 2013. Systems biology analysis of Zymomonas mobilis ZM4 ethanol stress responses. PLoS One 8:e68886. http://dx.doi.org/10.1371/journal.pone.0068886.
45. Koo JT, Alleyne TM, Schiano CA, Jafari N, Lathem WW. 2011. Global discovery of small RNAs in Yersinia pseudotuberculosis identifies Yersiniaspecific small, noncoding RNAs required for virulence. Proc. Natl. Acad. Sci. USA. 108:E709-E717. http://dx.doi.org/10.1073/pnas.1101655108.
46. DiChiara JM, Contreras-Martinez LM, Livny J, Smith D, McDonough KA, Belfort M. 2010. Multiple small RNAs identified in Mycobacterium bovis BCG are also expressed in Mycobacterium tuberculosis and Mycobacterium smegmatis. Nucleic Acids Res. 38:4067-4078. http://dx.doi.org /10.1093/nar/gkq101.
47. Zhang A, Wassarman KM, Rosenow C, Tjaden BC, Storz G, Gottesman S. 2003. Global analysis of small RNA and mRNA targets of Hfq. Mol. Microbiol. 50:1111-1124. http://dx.doi.org/10.1046/j.1365-2958.2003.03734.x.
48. Loh E, Dussurget O, Gripenland J, Vaitkevicius K, Tiensuu T, Mandin P, Repoila F, Buchrieser C, Cossart P, Johansson J. 2009. A trans-acting riboswitch controls expression of the virulence regulator PrfA in Listeria monocytogenes. Cell 139:770-779. http://dx.doi.org/10.1016/j.cell.2009.08.046.
49. Vogel J, Bartels V, Tang TH, Churakov G, Slagter-Jager JG, Huttenhofer A, Wagner EG. 2003. RNomics in Escherichia coli detects new sRNA species and indicates parallel transcriptional output in bacteria. Nucleic Acids Res. 31:6435-6443. http://dx.doi.org/10.1093/nar/gkg867.
50. Kawano M, Reynolds AA, Miranda-Rios J, Storz G. 2005. Detection of 5'-and 3'-UTR-derived small RNAs and cis-encoded antisense RNAs in Escherichia coli. Nucleic Acids Res. 33:1040-1050. http://dx.doi.org/10.1093/nar/gki256.
51. Chao Y, Papenfort K, Reinhardt R, Sharma CM, Vogel J. 2012. An atlas of Hfq-bound transcripts reveals 3' UTRs as a genomic reservoir of regulatory small RNAs. EMBO J. 31:4005-4019. http://dx.doi.org/10.1038 /emboj.2012.229.
52. Kawano M, Reynolds AA, Miranda-Rios J, Storz G. 2005. Detection of 5'-and 3'-UTR-derived small RNAs and cis-encoded antisense RNAs in Escherichia coli. Nucleic Acids Res. 33:1040-1050. http://dx.doi.org/10.1093/nar/gki256.
53. He MX, Wu B, Shui ZX, Hu QC, Wang WG, Tan FR, Tang XY, Zhu QL, Pan K, Li Q, Su XH. 2012. Transcriptome profiling of Zymomonas mobilis under ethanol stress. Biotechnol. Biofuels 5:75. http://dx.doi.org /10.1186/1754-6834-5-75.
54. Zuroff TR, Xiques SB, Curtis WR. 2013. Consortia-mediated bioprocessing of cellulose to ethanol with a symbiotic Clostridium phytofermentans/yeast co-culture. Biotechnol. Biofuels 6:59. http://dx.doi.org/10.1186 /1754-6834-6-59.
55. Goodman AE, Rogers PL, Skotnicki ML. 1982. Minimal medium for isolation of auxotrophic Zymomonas mutants. Appl. Environ. Microbiol. 44:496-498.