Transcriptomic analysis reveals new regulatory roles of Clp signaling in secondary metabolite biosynthesis and surface motility in Lysobacter enzymogenes OH11

Applied Microbiology and Biotechnology

Volumn 98, Issue 21, 2014, Pages 9009-9020

  Wang, Yansheng ^a   Zhao, Yuxin ^a   Zhang, Juan ^a   Zhao, Yangyang ^a   Shen, Yan ^a   Su, Zhenhe ^a   Xu, Gaoge ^a   Du, Liangcheng ^c   Huffman, Justin M ^d   Venturi, Vittorio ^e   Qian, Guoliang ^a   Liu, Fengquan ^a,b  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b INSTITUTE OF PLANT PROTECTION   (China)

^c UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^d PENNSYLVANIA STATE UNIVERSITY   (United States)

^e INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

Author keywords

Clp; HSAF; Lysobacter enzymogenes; Surface motility; WAP 8294A2

Indexed keywords

ANTIBIOTICS; ANTIFUNGAL AGENTS; BIOCHEMISTRY; BIOMOLECULES; BIOSYNTHESIS; FUNCTIONAL GROUPS; METABOLITES; SIGNALING; TRANSCRIPTION;

ANTI-BACTERIAL FACTORS; BIOLOGICAL CONTROL AGENT; CLP; CYCLIC ADENOSINE MONOPHOSPHATE (CAMP); HISTONE ACETYLTRANSFERASES; HSAF; LYSOBACTER; WAP-8294A2;

GENE EXPRESSION REGULATION;

ANTIBIOTIC AGENT; CYCLIC AMP; ENDOPEPTIDASE CLP; HISTONE ACETYLTRANSFERASE; ANTIINFECTIVE AGENT; TRANSCRIPTION FACTOR;

ANTIBIOTIC BIOSYNTHESIS; ANTIFUNGAL ACTIVITY; ARTICLE; BACTERIAL STRAIN; BIOINFORMATICS; BIOSYNTHESIS; DELETION MUTANT; GENE CLUSTER; GENE EXPRESSION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LYSOBACTER; LYSOBACTER ENZYMOGENES; MICROARRAY ANALYSIS; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSCRIPTOMICS; WILD TYPE; XANTHOMONADACEAE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; LOCOMOTION; METABOLISM; PHYSIOLOGY; SECONDARY METABOLISM;

ANTI-INFECTIVE AGENTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; LOCOMOTION; LYSOBACTER; MICROARRAY ANALYSIS; SECONDARY METABOLISM; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84925465329     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-014-6072-1     Document Type: Article

References (47)

1. Agarwal S, Hunnicutt DW, McBride MJ (1997) Cloning and characterization of the Flavobacterium johnsoniae (Cytophaga johnsonae) gliding motility gene, gldA. Proc Natl Acad Sci U S A 94:12139–12144
2. Aiba H (1985) Transcription of the Escherichia coli adenylate-cyclase gene is negatively regulated by camp-camp receptor protein. J Biol Chem 260(5):3063–3070
3. Angus-Hill ML, Dutnall RN, Tafrov ST, Sternglanz R, Ramakrishnan V (1999) Crystal structure of the histone acetyltransferase Hpa2: a tetrameric member of the Gcn5-related N-acetyltransferase superfamily. J Mol Biol 294(5):1311–1325
4. Atlung T, Ingmer H (1997) H-NS: a modulator of environmentally regulated gene expression. Mol Microbiol 24(1):7–17
5. Beatson SA, Whitchurch CB, Sargent JL, Levesque RC, Mattick JS (2002) Differential regulation of twitching motility and elastase production by Vfr in Pseudomonas aeruginosa. J Bacteriol 184(13):3605–3613
6. Burdman S, Bahar O, Parker JK, De La Fuente L (2011) Involvement of type IV pili in pathogenicity of plant pathogenic bacteria. Genes 2(4):706–735
7. Christensen P, Cook FD (1978) Lysobacter, a new genus of nonfruiting, gliding bacteria with high base ratio. Int J Syst Bacteriol 28:367–393
8. Donadio S, Monciardini P, Sosio M (2007) Polyketide synthases and nonribosomal peptide synthetases: the emerging view from bacterial genomics. Nat Prod Rep 24(5):1073–1109
9. Dyda F, Klein DC, Hickman AB (2000) GCN5-related N-acetyltransferases: a structural overview. Annu Rev Biophys Biomol Struct 29:81–103
10. Giesler LJ, Yuen GY (1998) Evaluation of Stenotrophomonas maltophilia strain C3 for biocontrol of brown patch disease. Crop Prot 17(6):509–513
11. Gorshkova I, Moore JL, McKenney KH, Schwarz FP (1995) Thermodynamics of cyclic nucleotide binding to the cAMP receptor protein and its T127L mutant. J Biol Chem 270(37):21679–21683
12. Gosset G, Zhang ZG, Nayyar S, Cuevas WA, Saier MH Jr (2004) Transcriptome analysis of Crp-dependent catabolite control of gene expression in Escherichia coli. J Bacteriol 186(11):3516–3524
13. Gunasekera A, Ebright YW, Ebright RH (1992) DNA sequence determinants for binding of the Escherichia coli catabolite gene activator protein. J Biol Chem 267(21):14713–14720
14. Guo Y, Guo HY, Zhang L, Xie HY, Zhao X, Wang FX, Li Z, Wang YH, Ma SL, Tao JP, Wang WX, Zhou YX, Yang WP, Cheng J (2005) Genomic analysis of anti-hepatitis B virus (HBV) activity by small interfering RNA and lamivudine in stable HBV-producing cells. J Virol 79(22):14392–14403
15. He YW, Ng AY, Xu M, Lin K, Wang LH, Dong YH, Zhang LH (2007) Xanthomonas campestris cell-cell communication involves a putative nucleotide receptor protein Clp and a hierarchical signalling network. Mol Microbiol 64(2):281–292
16. 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 furfural stress. Appl Microbiol Biotechnol 95(1):189–199
17. Hoang TT, Karkhoff-Schweizer RR, Kutchma AJ, Schweizer HP (1998) A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212(1):77–86
18. Kobayashi DY, Yuen GY (2005) The role of clp-regulated factors in antagonism against Magnaporthe poae and biological control of summer patch disease of Kentucky bluegrass by Lysobacter enzymogenes C3. Can J Microbiol 51(8):719–723
19. Kobayashi DY, Reedy RM, Palumbo JD, Zhou JM, Yuen GY (2005) A clp gene homologue belonging to the Crp gene family globally regulates lytic enzyme production, antimicrobial activity, and biological control activity expressed by Lysobacter enzymogenes strain C3. Appl Environ Microbiol 71(1):261–269
20. Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, Roop RM 2nd, Peterson KM (1995) Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166(1):175–176
21. Kuo MH, Allis CD (1998) Roles of histone acetyltransferases and deacetylases in gene regulation. Bioessays 20(8):615–626
22. Li SJ, Du LC, Yuen GY, Harris SD (2006) Distinct ceramide synthases regulate polarized growth in the filamentous fungus Aspergillus nidulans. Mol Biol Cell 17(3):1218–1227
23. Lou LL, Qian GL, Xie YX, Hang JL, Chen HT, Zaleta-Rivera K, Li YY, Shen YM, Dussault PH, Liu FQ, Du LC (2011) Biosynthesis of HSAF, a tetramic acid-containing macrolactam from Lysobacter enzymogenes. J Am Chem Soc 133(4):643–645
24. Mansfield J, Genin S, Magori S, Citovsky V, Sriariyanum M, Ronald P, Dow M, Verdier V, Beer SV, Machado MA, Toth I, Salmond G, Foster GD (2012) Top 10 plant pathogenic bacteria in molecular plant pathology. Mol Plant Pathol 13(6):614–629
25. Mathioni SM, Patel N, Riddick B, Sweigard JA, Czymmek KJ, Caplan JL, Kunjeti SG, Kunjeti S, Raman V, Hillman BI, Kobayashi DY, Donofrio NM (2013) Transcriptomics of the rice blast fungus Magnaporthe oryzae in response to the bacterial antagonist Lysobacter enzymogenes reveals candidate fungal defense response genes. PLoS ONE 8(10):e76487
26. Mattick JS (2002) Type IV pili and twitching motility. Annu Rev Microbiol 56:289–314
27. Musso RE, Di Lauro R, Adhya S, de Crombrugghe B (1977) Dual control for transcription of the galactose operon by cyclic AMP and its receptor protein at two interspersed promoters. Cell 12(3):847–854
28. Neuwald AF, Landsman D (1997) GCN5-related histone N-acetyltransferases belong to a diverse superfamily that includes the yeast SPT10 protein. Trends Biochem Sci 22(5):154–155
29. Pastan I, Adhya S (1976) Cyclic adenosine 5’-monophosphate in Escherichia coli. Bacteriol Rev 40(3):527–551
30. Patel N, Cornejo M, Lambert D, Craig A, Hillman BI, Kobayashi DY (2011) A multifunctional role for the type IV pilus in the bacterial biological control agent Lysobacter enzymogenes. Phytopathology 101(6):S138
31. Pesavento C, Hengge R (2009) Bacterial nucleotide-based second messengers. Curr Opin Microbiol 12(2):170–176
32. Qian GL, Hu BS, Jiang YH, Liu FQ (2009) Identification and characterization of Lysobacter enzymogenes as a biological control agent against some fungal pathogens. Agr Sci China 8(1):68–75
33. Qian GL, Wang YL, Liu YR, Xu FF, He YW, Du LC, Venturi V, Fan JQ, Hu BS, Liu FQ (2013) Lysobacter enzymogenes uses two distinct cell-cell signaling systems for differential regulation of secondary-metabolite biosynthesis and colony morphology. Appl Environ Microbiol 79(21):6604–6616
34. Qian GL, Xu FF, Venturi V, Du LC, Liu FQ (2014) Roles of a solo LuxR in the biological control agent Lysobacter enzymogenes strain OH11. Phytopathology 104(3):224–231
35. Qu S, Zhang YQ, Liu L, Wang L, Han YP, Yang RF, Zhou DS, Liu MY (2013) Cyclic AMP receptor protein is a repressor of adenylyl cyclase gene cyaA in Yersinia pestis. Can J Microbiol 59(5):304–310
36. Reverchon S, Expert D, Robert-Baudouy J, Nasser W (1997) The cyclic AMP receptor protein is the main activator of pectinolysis genes in Erwinia chrysanthemi. J Bacteriol 179(11):3500–3508
37. Takahashi M, Blazy B, Baudras A, Hillen W (1989) Ligand-modulated binding of a gene regulatory protein to DNA. Quantitative analysis of cyclic-AMP induced binding of CRP from Escherichia coli to non-specific and specific DNA targets. J Mol Biol 207(4):783–796
38. Tao F, He YW, Wu DH, Swarup S, Zhang LH (2010) The cyclic nucleotide monophosphate domain of Xanthomonas campestris global regulator Clp defines a new class of cyclic di-GMP effectors. J Bacteriol 192(4):1020–1029
39. Ussery DW, Hinton JC, Jordi BJ, Granum PE, Seirafi A, Stephen RJ, Tupper AE, Berridge G, Sidebotham JM, Higgins CF (1994) The chromatin-associated protein H-NS. Biochimie 76(10–11):968–980
40. Wang Y, Qian GL, Li YY, Wang YS, Wang YL, Wright S, Li YZ, Shen YM, Liu FQ, Du LC (2013) Biosynthetic mechanism for sunscreens of the biocontrol agent Lysobacter enzymogenes. PLoS ONE 8(6):e66633
41. Williams RM, Rimsky S (1997) Molecular aspects of the E. coli nucleoid protein, H-NS: a central controller of gene regulatory networks. FEMS Microbiol Lett 156(2):175–185
42. Xie YX, Wright S, Shen YM, Du LC (2012) Bioactive natural products from Lysobacter. Nat Prod Rep 29(11):1277–1287
43. Yu FG, Zaleta-Rivera K, Zhu XC, Huffman J, Millet JC, Harris SD, Yuen GY, Li XC, Du LC (2007) Structure and biosynthesis of heat-stable antifungal factor (HSAF), a broad-spectrum antimycotic with a novel mode of action. Antimicrob Agents Ch 51(1):64–72
44. Zhang Z, Yuen GY (1999) Biological control of Bipolaris sorokiniana on tall fescue by Stenotrophomonas maltophilia strain C3. Phytopathology 89(9):817–822
45. Zhang W, Li YY, Qian GL, Wang Y, Chen HT, Li YZ, Liu FQ, Shen YM, Du LC (2011) Identification and characterization of the anti-methicillin-resistant Staphylococcus aureus WAP-8294A2 biosynthetic gene cluster from Lysobacter enzymogenes OH11. Antimicrob Agents Ch 55(12):5581–5589
46. Zhang J, Du LC, Liu FQ, Xu FF, Hu BS, Venturi V, Qian GL (2014) Involvement of both PKS and NRPS in antibacterial activity in Lysobacter enzymogenes OH11. FEMS Microbiol Lett 355(2):170–176
47. Zheng DL, Constantinidou C, Hobman JL, Minchin SD (2004) Identification of the CRP regulon using in vitro and in vivo transcriptional profiling. Nucleic Acids Res 32(19):5874–5893