1887

Abstract

Addition of stearyl alcohol to the culture medium of sp. NT80 induced expression of a significant amount of secretory lipase. Comparative proteomic analysis of extracellular proteins from NT80 cells grown in the presence or absence of stearyl alcohol revealed that stearyl alcohol induced expression of several secretory proteins including lipase, haemolysin-coregulated protein and nucleoside diphosphate kinase. Expression of these secreted proteins was upregulated at the transcriptional level. Stearyl alcohol also induced the synthesis of polyhydroxyalkanoate. Secretory protein EliA was required for all these responses of NT80 cells to stearyl alcohol. Accordingly, the effects of stearyl alcohol were significantly reduced in the deletion mutant cells of NT80 (Δ). The remaining concentration of stearyl alcohol in the culture supernatant of the wild-type cells, but not that in the culture supernatant of the Δ cells, clearly decreased during the course of growth. These observed phenotypes of the Δ mutant were rescued by gene complementation. The results suggested that EliA is essential for these cells to respond to stearyl alcohol, and that it plays an important role in the recognition and assimilation of stearyl alcohol by NT80 cells.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000225
2016-02-01
2020-01-23
Loading full text...

Full text loading...

/deliver/fulltext/micro/162/2/408.html?itemId=/content/journal/micro/10.1099/mic.0.000225&mimeType=html&fmt=ahah

References

  1. Akanuma G., Hara H., Ohnishi Y., Horinouchi S.. 2009; Dynamic changes in the extracellular proteome caused by absence of a pleiotropic regulator AdpA in Streptomyces griseus. Mol Microbiol73:898–912 [CrossRef][PubMed]
    [Google Scholar]
  2. Akanuma G., Ishibashi H., Miyagawa T., Yoshizawa R., Watanabe S., Shiwa Y., Yoshikawa H., Ushio K., Ishizuka M.. 2013; EliA facilitates the induction of lipase expression by stearyl alcohol in Ralstonia sp., NT80. FEMS Microbiol Lett339:48–56 [CrossRef][PubMed]
    [Google Scholar]
  3. Aparna G., Chatterjee A., Sonti R. V., Sankaranarayanan R.. 2009; A cell wall-degrading esterase of Xanthomonas oryzae requires a unique substrate recognition module for pathogenesis on rice. Plant Cell21:1860–1873 [CrossRef][PubMed]
    [Google Scholar]
  4. Baysse C., Cullinane M., Dénervaud V., Burrowes E., Dow J. M., Morrissey J. P., Tam L., Trevors J. T., O'Gara F.. 2005; Modulation of quorum sensing in Pseudomonas aeruginosa through alteration of membrane properties. Microbiology151:2529–2542 [CrossRef][PubMed]
    [Google Scholar]
  5. Beeby M., Cho M., Stubbe J., Jensen G. J.. 2012; Growth and localization of polyhydroxybutyrate granules in Ralstonia eutropha. J Bacteriol194:1092–1099 [CrossRef][PubMed]
    [Google Scholar]
  6. Beisson F., Li-Beisson Y., Pollard M.. 2012; Solving the puzzles of cutin and suberin polymer biosynthesis. Curr Opin Plant Biol15:329–337 [CrossRef][PubMed]
    [Google Scholar]
  7. Boekema B. K., Beselin A., Breuer M., Hauer B., Koster M., Rosenau F., Jaeger K. E., Tommassen J.. 2007; Hexadecane and Tween 80 stimulate lipase production in Burkholderia glumae by different mechanisms. Appl Environ Microbiol73:3838–3844 [CrossRef][PubMed]
    [Google Scholar]
  8. Bouchez Naı¨tali M., Rakatozafy H., Marchal R., Leveau J. Y., Vandecasteele J. P.. 1999; Diversity of bacterial strains degrading hexadecane in relation to the mode of substrate uptake. J Appl Microbiol86:421–428 [CrossRef][PubMed]
    [Google Scholar]
  9. Brigham C. J., Speth D. R., Rha C., Sinskey A. J.. 2012; Whole-genome microarray and gene deletion studies reveal regulation of the polyhydroxyalkanoate production cycle by the stringent response in Ralstonia eutropha H16. Appl Environ Microbiol78:8033–8044 [CrossRef][PubMed]
    [Google Scholar]
  10. Burtnick M. N., Brett P. J., Harding S. V., Ngugi S. A., Ribot W. J., Chantratita N., Scorpio A., Milne T. S., Dean R. E., other authors. 2011; The cluster 1 type VI secretion system is a major virulence determinant in Burkholderia pseudomallei. Infect Immun79:1512–1525 [CrossRef][PubMed]
    [Google Scholar]
  11. Buschhaus C., Jetter R.. 2011; Composition differences between epicuticular and intracuticular wax substructures: how do plants seal their epidermal surfaces?. J Exp Bot62:841–853 [CrossRef][PubMed]
    [Google Scholar]
  12. Büttner D., Bonas U.. 2010; Regulation and secretion of Xanthomonas virulence factors. FEMS Microbiol Rev34:107–133 [CrossRef][PubMed]
    [Google Scholar]
  13. Chakrabarty A. M.. 1998; Nucleoside diphosphate kinase: role in bacterial growth, virulence, cell signalling and polysaccharide synthesis. Mol Microbiol28:875–882 [CrossRef][PubMed]
    [Google Scholar]
  14. Chater K. F., Biró S., Lee K. J., Palmer T., Schrempf H.. 2010; The complex extracellular biology of Streptomyces. FEMS Microbiol Rev34:171–198 [CrossRef][PubMed]
    [Google Scholar]
  15. Ciprandi A., da Silva W. M., Santos A. V., de Castro Pimenta A. M., Carepo M. S., Schneider M. P., Azevedo V., Silva A.. 2013; Chromobacterium violaceum: important insights for virulence and biotechnological potential by exoproteomic studies. Curr Microbiol67:100–106 [CrossRef][PubMed]
    [Google Scholar]
  16. Clemmer K. M., Rather P. N.. 2008; The Lon protease regulates swarming motility and virulence gene expression in Proteus mirabilis. J Med Microbiol57:931–937 [CrossRef][PubMed]
    [Google Scholar]
  17. Coenye T., Goris J., De Vos P., Vandamme P., LiPuma J. J.. 2003; Classification of Ralstonia pickettii-like isolates from the environment and clinical samples as Ralstonia insidiosa sp. nov. Int J Syst Evol Microbiol53:1075–1080 [CrossRef][PubMed]
    [Google Scholar]
  18. Cottyn B., Cerez M. T., Van Outryve M. F., Barroga J., Swings J., Mew T. W.. 1996; Bacterial disease of rice I. Pathogenic bacteria associated with sheath rot complex and grain discoloration of rice in the Philippines. Plant Dis80:429–437 [CrossRef]
    [Google Scholar]
  19. de María P. D., Sánchez-Montero J. M., Alcántara A. R., Valero F., Sinisterra J. V.. 2005; Rational strategy for the production of new crude lipases from Candida rugosa. Biotechnol Lett27:499–503 [CrossRef][PubMed]
    [Google Scholar]
  20. Decoin V., Barbey C., Bergeau D., Latour X., Feuilloley M. G., Orange N., Merieau A.. 2014; A type VI secretion system is involved in Pseudomonas fluorescens bacterial competition. PLoS One9:e89411 [CrossRef][PubMed]
    [Google Scholar]
  21. Deive F. J., Carvalho E., Pastrana L., Rúa M. L., Longo M. A., Sanroman M. A.. 2009; Strategies for improving extracellular lipolytic enzyme production by Thermus thermophilus HB27. Bioresour Technol100:3630–3637 [CrossRef][PubMed]
    [Google Scholar]
  22. Gil F., Ipinza F., Fuentes J., Fumeron R., Villarreal J. M., Aspée A., Mora G. C., Vásquez C. C., Saavedra C.. 2007; The ompW (porin) gene mediates methyl viologen (paraquat) efflux in Salmonella enterica serovar typhimurium. Res Microbiol158:529–536 [CrossRef][PubMed]
    [Google Scholar]
  23. Goo E., Kang Y., Kim H., Hwang I.. 2010; Proteomic analysis of quorum sensing-dependent proteins in Burkholderia glumae. J Proteome Res9:3184–3199 [CrossRef][PubMed]
    [Google Scholar]
  24. Ham J. H., Melanson R. A., Rush M. C.. 2011; Burkholderia glumae: next major pathogen of rice?. Mol Plant Pathol12:329–339 [CrossRef][PubMed]
    [Google Scholar]
  25. Hardegger M., Koch A. K., Ochsner U. A., Fiechter A., Reiser J.. 1994; Cloning and heterologous expression of a gene encoding an alkane-induced extracellular protein involved in alkane assimilation from Pseudomonas aeruginosa. Appl Environ Microbiol60:3679–3687[PubMed]
    [Google Scholar]
  26. Hayden H. S., Lim R., Brittnacher M. J., Sims E. H., Ramage E. R., Fong C., Wu Z., Crist E., Chang J., other authors. 2012; Evolution of Burkholderia pseudomallei in recurrent melioidosis. PLoS One7:e36507 [CrossRef][PubMed]
    [Google Scholar]
  27. Hendrickson E. L., Beck D. A., Wang T., Lidstrom M. E., Hackett M., Chistoserdova L.. 2010; Expressed genome of Methylobacillus flagellatus as defined through comprehensive proteomics and new insights into methylotrophy. J Bacteriol192:4859–4867 [CrossRef][PubMed]
    [Google Scholar]
  28. Hisatsuka K., Nakahara T., Yamada K.. 1972; Protein-like activator for n-alkane oxidation by Pseudomonas aeruginosa S7B1. Agric Biol Chem36:1361–1369 [CrossRef]
    [Google Scholar]
  29. Hisatsuka K., Nakahara T., Minoda Y., Yamada K.. 1977; Formation of protein-like activator for n-alkane oxidation and its properties. Agric Biol Chem41:445–450 [CrossRef]
    [Google Scholar]
  30. Isaacson T., Kosma D. K., Matas A. J., Buda G. J., He Y., Yu B., Pravitasari A., Batteas J. D., Stark R. E., other authors. 2009; Cutin deficiency in the tomato fruit cuticle consistently affects resistance to microbial infection and biomechanical properties, but not transpirational water loss. Plant J60:363–377 [CrossRef][PubMed]
    [Google Scholar]
  31. Jendrossek D.. 2009; Polyhydroxyalkanoate granules are complex subcellular organelles (carbonosomes). J Bacteriol191:3195–3202 [CrossRef][PubMed]
    [Google Scholar]
  32. Jendrossek D., Handrick R.. 2002; Microbial degradation of polyhydroxyalkanoates. Annu Rev Microbiol56:403–432 [CrossRef][PubMed]
    [Google Scholar]
  33. Jeong Y., Kim J., Kim S., Kang Y., Nagamatsu T., Hwang I.. 2003; Toxoflavin produced by Burkholderia glumae causing rice grain rot is responsible for inducing bacterial wilt in many field crops. Plant Dis87:890–895 [CrossRef]
    [Google Scholar]
  34. Kabelitz N., Santos P. M., Heipieper H. J.. 2003; Effect of aliphatic alcohols on growth and degree of saturation of membrane lipids in Acinetobacter calcoaceticus. FEMS Microbiol Lett220:223–227 [CrossRef][PubMed]
    [Google Scholar]
  35. Kim Y. J., Paek S. H., Jin S., Park B. S., Ha U. H.. 2014; A novel Pseudomonas aeruginosa-derived effector cooperates with flagella to mediate the upregulation of interleukin 8 in human epithelial cells. Microb Pathog66:24–28 [CrossRef][PubMed]
    [Google Scholar]
  36. Kojima T., Nishiyama T., Maehara A., Ueda S., Nakano H., Yamane T.. 2004; Expression profiles of polyhydroxyalkanoate synthesis-related genes in Paracoccus denitrificans. J Biosci Bioeng97:45–53 [CrossRef][PubMed]
    [Google Scholar]
  37. Laemmli U. K.. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature227:680–685 [CrossRef][PubMed]
    [Google Scholar]
  38. Li Y., Beisson F., Ohlrogge J., Pollard M.. 2007; Monoacylglycerols are components of root waxes and can be produced in the aerial cuticle by ectopic expression of a suberin-associated acyltransferase. Plant Physiol144:1267–1277 [CrossRef][PubMed]
    [Google Scholar]
  39. Lopes M. S., Steinert N., Rojas J. D., Hillen W., Gomez J. G., Silva L. F.. 2011; Role of CcpA in polyhydroxybutyrate biosynthesis in a newly isolated Bacillus sp., MA3.3. J Mol Microbiol Biotechnol20:63–69 [CrossRef][PubMed]
    [Google Scholar]
  40. Lu H., Kalyuzhnaya M., Chandran K.. 2012; Comparative proteomic analysis reveals insights into anoxic growth of Methyloversatilis universalis FAM5 on methanol and ethanol. Environ Microbiol14:2935–2945 [CrossRef][PubMed]
    [Google Scholar]
  41. Macnab R. M.. 2004; Type III flagellar protein export and flagellar assembly. Biochim Biophys Acta1694:207–217 [CrossRef][PubMed]
    [Google Scholar]
  42. Mariappan V., Vellasamy K. M., Hashim O. H., Vadivelu J.. 2011; Profiling of Burkholderia cepacia secretome at mid-logarithmic and early-stationary phases of growth. PLoS One6:e26518 [CrossRef][PubMed]
    [Google Scholar]
  43. Mougous J. D., Cuff M. E., Raunser S., Shen A., Zhou M., Gifford C. A., Goodman A. L., Joachimiak G., Ordoñez C. L.. & other authors 2006; A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science312:1526–1530 [CrossRef][PubMed]
    [Google Scholar]
  44. Nandi B., Nandy R. K., Sarkar A., Ghose A. C.. 2005; Structural features, properties and regulation of the outer-membrane protein W (OmpW) of Vibrio cholerae. Microbiology151:2975–2986 [CrossRef][PubMed]
    [Google Scholar]
  45. Neeld D., Jin Y., Bichsel C., Jia J., Guo J., Bai F., Wu W., Ha U. H., Terada N., Jin S.. 2014; Pseudomonas aeruginosa injects NDK into host cells through a type III secretion system. Microbiology160:1417–1426 [CrossRef][PubMed]
    [Google Scholar]
  46. Neumann B., Pospiech A., Schairer H. U.. 1992; Rapid isolation of genomic DNA from Gram-negative bacteria. Trends Genet8:332–333 [CrossRef][PubMed]
    [Google Scholar]
  47. O'Toole G. A., Kolter R.. 1998; Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol30:295–304 [CrossRef][PubMed]
    [Google Scholar]
  48. Peeters N., Guidot A., Vailleau F., Valls M.. 2013; Ralstonia solanacearum, a widespread bacterial plant pathogen in the post-genomic era. Mol Plant Pathol14:651–662 [CrossRef][PubMed]
    [Google Scholar]
  49. Peoples O. P., Sinskey A. J.. 1989a; Poly-β-hydroxybutyrate biosynthesis in Alcaligenes eutrophus H16. Characterization of the genes encoding β-ketothiolase and acetoacetyl-CoA reductase. J Biol Chem264:15293–15297[PubMed]
    [Google Scholar]
  50. Peoples O. P., Sinskey A. J.. 1989b; Poly-β-hydroxybutyrate (PHB) biosynthesis in Alcaligenes eutrophus H16. Identification and characterization of the PHB polymerase gene (phbC). J Biol Chem264:15298–15303[PubMed]
    [Google Scholar]
  51. Pollard M., Beisson F., Li Y., Ohlrogge J. B.. 2008; Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci13:236–246 [CrossRef][PubMed]
    [Google Scholar]
  52. Pumirat P., Saetun P., Sinchaikul S., Chen S. T., Korbsrisate S., Thongboonkerd V.. 2009; Altered secretome of Burkholderia pseudomallei induced by salt stress. Biochim Biophys Acta1794:898–904 [CrossRef][PubMed]
    [Google Scholar]
  53. Raberg M., Bechmann J., Brandt U., Schlüter J., Uischner B., Voigt B., Hecker M., Steinbüchel A.. 2011; Versatile metabolic adaptations of Ralstonia eutropha H16 to a loss of PdhL, the E3 component of the pyruvate dehydrogenase complex. Appl Environ Microbiol77:2254–2263 [CrossRef][PubMed]
    [Google Scholar]
  54. Ratcliff W. C., Kadam S. V., Denison R. F.. 2008; Poly-3-hydroxybutyrate (PHB) supports survival and reproduction in starving rhizobia. FEMS Microbiol Ecol65:391–399 [CrossRef][PubMed]
    [Google Scholar]
  55. Records A. R.. 2011; The type VI secretion system: a multipurpose delivery system with a phage-like machinery. Mol Plant Microbe Interact24:751–757 [CrossRef][PubMed]
    [Google Scholar]
  56. Remenant B., Coupat-Goutaland B., Guidot A., Cellier G., Wicker E., Allen C., Fegan M., Pruvost O., Elbaz M.. & other authors 2010; Genomes of three tomato pathogens within the Ralstonia solanacearum species complex reveal significant evolutionary divergence. BMC Genomics11:379 [CrossRef][PubMed]
    [Google Scholar]
  57. Ruiz J. A., López N. I., Fernández R. O., Méndez B. S.. 2001; Polyhydroxyalkanoate degradation is associated with nucleotide accumulation and enhances stress resistance and survival of Pseudomonas oleovorans in natural water microcosms. Appl Environ Microbiol67:225–230 [CrossRef][PubMed]
    [Google Scholar]
  58. Schell M. A., Ulrich R. L., Ribot W. J., Brueggemann E. E., Hines H. B., Chen D., Lipscomb L., Kim H. S., Mrázek J., other authors. 2007; Type VI secretion is a major virulence determinant in Burkholderia mallei. Mol Microbiol64:1466–1485 [CrossRef][PubMed]
    [Google Scholar]
  59. Shakeri S., Roghanian R., Emtiazi G.. 2012; Surveillance of single-cell behavior in different subpopulations of Ralstonia pickettii AR1 during growth and polyhydroxybutyrate production phases by flow cytometry. J Basic Microbiol52:206–215 [CrossRef][PubMed]
    [Google Scholar]
  60. Sztajer H., Lünsdorf H., Erdmann H., Menge U., Schmid R.. 1992; Purification and properties of lipase from Penicillium simplicissimum. Biochim Biophys Acta1124:253–261 [CrossRef][PubMed]
    [Google Scholar]
  61. Tanadchangsaeng N., Kitagawa A., Yamamoto T., Abe H., Tsuge T.. 2009; Identification, biosynthesis, and characterization of polyhydroxyalkanoate copolymer consisting of 3-hydroxybutyrate and 3-hydroxy-4-methylvalerate. Biomacromolecules10:2866–2874 [CrossRef][PubMed]
    [Google Scholar]
  62. Tani A., Ishige T., Sakai Y., Kato N.. 2001; Gene structures and regulation of the alkane hydroxylase complex in Acinetobacter sp. strain M-1. J Bacteriol183:1819–1823 [CrossRef][PubMed]
    [Google Scholar]
  63. Throne-Holst M., Markussen S., Winnberg A., Ellingsen T. E., Kotlar H. K., Zotchev S. B.. 2006; Utilization of n-alkanes by a newly isolated strain of Acinetobacter venetianus: the role of two AlkB-type alkane hydroxylases. Appl Microbiol Biotechnol72:353–360 [CrossRef][PubMed]
    [Google Scholar]
  64. Tribelli P. M., López N. I.. 2011; Poly(3-hydroxybutyrate) influences biofilm formation and motility in the novel Antarctic species Pseudomonas extremaustralis under cold conditions. Extremophiles15:541–547 [CrossRef][PubMed]
    [Google Scholar]
  65. Tseng T. T., Tyler B. M., Setubal J. C.. 2009; Protein secretion systems in bacterial-host associations, and their description in the gene ontology. BMC Microbiol 9 (Suppl.1:S2 [CrossRef][PubMed]
    [Google Scholar]
  66. Tsuge T.. 2002; Metabolic improvements and use of inexpensive carbon sources in microbial production of polyhydroxyalkanoates. J Biosci Bioeng94:579–584 [CrossRef][PubMed]
    [Google Scholar]
  67. Ushio K., Hirata T., Yoshida K., Sakaue M., Hirose C., Suzuki T., Ishizuka M.. 1996; Superinducers for induction of thermostable lipase production by Pseudomonas species NT-163 and other Pseudomonas like bacteria. Biotechnol Tech10:267–272 [CrossRef]
    [Google Scholar]
  68. Van Hamme J. D., Singh A., Ward O. P.. 2003; Recent advances in petroleum microbiology. Microbiol Mol Biol Rev67:503–549 [CrossRef][PubMed]
    [Google Scholar]
  69. Wandersman C.. 1989; Secretion, processing and activation of bacterial extracellular proteases. Mol Microbiol3:1825–1831 [CrossRef][PubMed]
    [Google Scholar]
  70. Webb J. S., Givskov M., Kjelleberg S.. 2003; Bacterial biofilms: prokaryotic adventures in multicellularity. Curr Opin Microbiol6:578–585 [CrossRef][PubMed]
    [Google Scholar]
  71. Wehmhöner D., Häussler S., Tümmler B., Jänsch L., Bredenbruch F., Wehland J., Steinmetz I.. 2003; Inter- and intraclonal diversity of the Pseudomonas aeruginosa proteome manifests within the secretome. J Bacteriol185:5807–5814 [CrossRef][PubMed]
    [Google Scholar]
  72. Wentzel A., Ellingsen T. E., Kotlar H. K., Zotchev S. B., Throne-Holst M.. 2007; Bacterial metabolism of long-chain n-alkanes. Appl Microbiol Biotechnol76:1209–1221 [CrossRef][PubMed]
    [Google Scholar]
  73. Wu H. Y., Chung P. C., Shih H. W., Wen S. R., Lai E. M.. 2008; Secretome analysis uncovers an Hcp-family protein secreted via a type VI secretion system in Agrobacterium tumefaciens. J Bacteriol190:2841–2850 [CrossRef][PubMed]
    [Google Scholar]
  74. Yamada M., Yamashita K., Wakuda A., Ichimura K., Maehara A., Maeda M., Taguchi S.. 2007; Autoregulator protein PhaR for biosynthesis of polyhydroxybutyrate [P(3HB)] possibly has two separate domains that bind to the target DNA and P(3HB): functional mapping of amino acid residues responsible for DNA binding. J Bacteriol189:1118–1127 [CrossRef][PubMed]
    [Google Scholar]
  75. Zerbino D. R., Birney E.. 2008; Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res18:821–829 [CrossRef][PubMed]
    [Google Scholar]
  76. Zhang L., Xu J., Xu J., Zhang H., He L., Feng J.. 2014; TssB is essential for virulence and required for type VI secretion system in Ralstonia solanacearum. Microb Pathog74:1–7 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000225
Loading
/content/journal/micro/10.1099/mic.0.000225
Loading

Data & Media loading...

Supplements

Supplementary Data

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error