BioMetals

, Volume 30, Issue 1, pp 127–141 | Cite as

Proteome wide identification of iron binding proteins of Xanthomonas translucens pv. undulosa: focus on secretory virulent proteins

  • Ankita Sharma
  • Dixit Sharma
  • Shailender Kumar Verma
Article
  • 327 Downloads

Abstract

Xanthomonas translucens pv. undulosa (Xtu) causes Bacterial Leaf Streak disease in the staple food crops such as wheat and barley. The survival strategies of pathogen and host are determined by the complex interactions occurring between the host plants and the pathogenic microbes. Iron binding proteins are important in the plant–microbe interactions as they are indulged in enzyme catalysis, virulence, metabolic and transport activities. In the presented study, we have identified that ~9.8% of Xtu proteome possess iron binding sequence motifs. Further, the analysis of Xtu proteome for secretory iron binding virulent proteins (IBVPs) revealed the fact that iron co-regulate the function of secretory proteins in virulence. We have found 26 secretory IBVPs and observed that these proteins are diverse in their biological functions ranging from transport to antimicrobial resistance, Reactive oxygen species detoxification and carbohydrate catabolism. The inferences may instigate to design the new strategies to combat and control the microbial diseases of staple food crops.

Keywords

Xanthomonas translucens pv. undulosa Iron binding proteins Secretory iron binding virulent proteins Ton-B dependent receptors 

Supplementary material

10534_2017_9991_MOESM1_ESM.docx (80 kb)
Supplementary material 1 (DOCX 79 kb)
10534_2017_9991_MOESM2_ESM.docx (27 kb)
Supplementary material 2 (DOCX 26 kb)
10534_2017_9991_MOESM3_ESM.docx (15 kb)
Supplementary material 3 (DOCX 14 kb)
10534_2017_9991_MOESM4_ESM.docx (14 kb)
Supplementary material 4 (DOCX 13 kb)
10534_2017_9991_MOESM5_ESM.docx (13 kb)
Supplementary material 5 (DOCX 13 kb)

References

  1. Adhikari TB, Gurung S, Hansen JM, Bonman JM (2012) Pathogenic and genetic diversity of Xanthomonas translucens pv. undulosa in north Dakota. Phyto 102:390–402CrossRefGoogle Scholar
  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefPubMedGoogle Scholar
  3. Andreini C, Banci L, Bertini I, Elmi S, Rosato A (2007) Non-heme iron through the three domains of life. Proteins 67:317–324CrossRefPubMedGoogle Scholar
  4. Arguelles JC (2000) Physiological roles of trehalose in bacteria and yeasts: a comparative analysis. J. Arch Microbiol 174:217–224CrossRefGoogle Scholar
  5. Babor M, Gerzon S, Raveh B, Sobolev V, Edelman M (2008) Prediction of transition metal-binding sites from apo protein structures. Proteins 70:208–217CrossRefPubMedGoogle Scholar
  6. Banin E, Vasil ML, Greenberg EP (2005) Iron and Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci USA 102:11076–11081CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bebrone C (2007) Metallo-β-lactamases (classification, activity, genetic organization, structure, zinc coordination) and their superfamily. Biochem Pharmacol 74:1686–1701CrossRefPubMedGoogle Scholar
  8. Bendtsen JD, Jensen LJ, Blom N, Von Heijne G, Brunak S (2004) Feature-based prediction of non-classical and leaderless protein secretion. Protein Eng Des Sel 17:349–356CrossRefPubMedGoogle Scholar
  9. Bragard C, Verdier V, Maraite H (1995) Genetic diversity among Xanthomonas campestris strains pathogenic for small grains. Appl Environ Microbiol 61:1020–1026PubMedPubMedCentralGoogle Scholar
  10. Brickman TJ, McIntosh MA (1992) Overexpression and purification of ferric enterobactin esterase from Escherichia coli. Demonstration of enzymatic hydrolysis of enterobactin and its iron complex. J Biol Chem 267:12350–12355PubMedGoogle Scholar
  11. Bull CT, Deboer SH, Denny TP, Firrao G, Saux MF, Saddler GS, Scortichini M, Stead DE, Takikawa Y (2010) Comprehensive list of names of plant pathogenic bacteria 1980-2007. J Plant Pathol 92:551–592Google Scholar
  12. Buttner D, Bonas U (2010) Regulation and secretion of Xanthomonas virulence factors. FEMS Microbiol Rev 34:107–133CrossRefPubMedGoogle Scholar
  13. Cai CZ, Han LY, Ji ZL, Chen X, Chen YZ (2003) SVM-Prot: web-based support vector machine software for functional classification of a protein from its primary sequence. Nucleic Acids Res 31:3692–3697CrossRefPubMedPubMedCentralGoogle Scholar
  14. Chakraborty S, Newton AC (2011) Climate change, plant diseases and food security: an overview. Plant Pathol 60:2–14CrossRefGoogle Scholar
  15. Cobessi D, Celia H, Folschweiller N, Schalk IJ, Abdallah MA, Pattus F (2005) The crystal structure of the pyoverdine outer membrane receptor FpvA from Pseudomonas aeruginosa at 3.6 angstroms resolution. J Mol Biol 347:121–134CrossRefPubMedGoogle Scholar
  16. Cohen S, Sweeney HM, Leitner F (1967) Relation between iron uptake, pH of growth medium, and penicillinase formation in Staphylococcus aureus. J Bacteriol 93:1227–1235PubMedPubMedCentralGoogle Scholar
  17. Crumbliss AL, Harrington JM (2009) Iron sequestration by small molecules: thermodynamic and kinetic studies of natural siderophores and synthetic model compounds. Advance in inorganic chemistry 61:179–250CrossRefGoogle Scholar
  18. De Serrano LO, Camper AK, Richards AM (2016) An overview of siderophores for iron acquisition in microorganisms living in the extreme. Biometals 29:551–571CrossRefPubMedGoogle Scholar
  19. DeLano WL (2002) The PyMOL molecular graphics system. DeLano Scientific, Palo AltoGoogle Scholar
  20. Dellagi A, Rigault M, Segond D, Roux C, Kraepiel Y, Cellier F, Briat JF, Gaymard F, Expert D (2005) Siderophore mediated upregulation of Arabidopsis ferritin expression in response to Erwinia chrysanthemi infection. Plant J 43:262–272CrossRefPubMedGoogle Scholar
  21. Dellagi A, Segond D, Rigault M, Fagard M, Simon C, Saindrenan P, Expert D (2009) Microbial siderophores exert a subtle role in Arabidopsis during infection by manipulating the immune response and the iron status. Plant Physiol 150:1687–1696CrossRefPubMedPubMedCentralGoogle Scholar
  22. Djonovic S, Urbach JM, Drenkard E, Bush J, Feinbaum R, Ausubel JL, Traficante D, Risech M, Kocks C, Fischbach MA, Priebe GP, Ausubel FM (2013) Trehalose biosynthesis promotes Pseudomonas aeruginosa pathogenicity in plants. PLoS Pathog 9:e1003217CrossRefPubMedPubMedCentralGoogle Scholar
  23. Douet V, Expert D, Barras F, Py B (2009) Erwinia chrysanthemi iron metabolism: the unexpected implication of the inner membrane platform within the type II secretion system. J Bacteriol 191:795–804CrossRefPubMedGoogle Scholar
  24. Duveiller E, Maraite H (1993) Study on yield loss due to Xanthomonas campestris pv. undulosa in wheat under high rainfall temperate conditions. J Plant Dis Prot 100:453–459Google Scholar
  25. Elbein AD, Pan YT, Pastuszak I, Carroll D (2003) New insights on trehalose: a multifunctional molecule. Glycobiology 13:17R–27RCrossRefPubMedGoogle Scholar
  26. Eleutherio E, Panek A, De Mesquita JF, Trevisol E, Magalhães R (2015) Revisiting yeast trehalose metabolism. Curr genet 61:263–274PubMedGoogle Scholar
  27. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60:2126–2132CrossRefPubMedGoogle Scholar
  28. Enard C, Diolez A, Expert D (1988) Systemic virulence of Erwinia chrysanthemi 3937 requires a functional iron assimilation system. J Bacteriol 170:2419–2426CrossRefPubMedPubMedCentralGoogle Scholar
  29. Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, Potter SC, Punta M, Qureshi M, Sangrador-Vegas A, Salazar GA, Tate J, Bateman A (2016) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44:D279–D285CrossRefPubMedGoogle Scholar
  30. Forster RL, Schaad NW (1988) Control of black chaff of wheat with seed treatment and a foundation seed health program. Plant Dis 72:935–938CrossRefGoogle Scholar
  31. Foster AJ, Jenkinson JM, Talbot NJ (2003) Trehalose synthesis and metabolism are required at different stages of plant infection by Magnaporthe grisea. EMBO J 22:225–235CrossRefPubMedPubMedCentralGoogle Scholar
  32. Franza T, Expert D (2013) Role of iron homeostasis in the virulence of phytopathogenic bacteria: an ‘à la carte’menu. Mol Plant pathol 14:429–438CrossRefPubMedGoogle Scholar
  33. Frederick JR, Elkins JG, Bollinger N, Hassett DJ, McDermott TR (2001) Factors affecting catalase expression in Pseudomonas aeruginosa biofilms and planktonic cells. Appl Environ Microbiol 67:1375–1379CrossRefPubMedPubMedCentralGoogle Scholar
  34. Gaddy JA, Tomaras AP, Actis LA (2009) The Acinetobacter baumannii 19606 OmpA protein plays a role in biofilm formation on abiotic surfaces and in the interaction of this pathogen with eukaryotic cells. Infect Immun 77:3150–3160CrossRefPubMedPubMedCentralGoogle Scholar
  35. Gennaris A, Ezraty B, Henry C, Agrebi R, Vergnes A, Oheix E, Bos J, Leverrier P, Espinosa L, Szewczyk J, Vertommen D, Iranzo O, Collet JF, Barras F (2015) Repairing oxidized proteins in the bacterial envelope using respiratory chain electrons. Nature 528:409–412CrossRefPubMedPubMedCentralGoogle Scholar
  36. Golovin A, Dimitropoulos D, Oldfield T, Rachedi A, Henrick K (2005) MSDsite: a database search and retrieval system for the analysis and viewing of bound ligands and active sites. Proteins 58:190–199CrossRefPubMedGoogle Scholar
  37. Gough J, Karplus K, Hughey R, Chothia C (2001) Assignment of homology to genome sequences using a library of hidden Markov models that represent all proteins of known structure. J Mol Biol 313:903–919CrossRefPubMedGoogle Scholar
  38. Hassett DJ, Ma JF, Elkins JG, McDermott TR, Ochsner UA, West SE, Huang CT, Fredericks J, Burnett S, Stewart PS, McFeters G, Passador L, Iglewski BH (1999) Quorum sensing in Pseudomonas aeruginosa controls expression of catalase and superoxide dismutase genes and mediates biofilm susceptibility to hydrogen peroxide. Mol Microbiol 34:1082–1093CrossRefPubMedGoogle Scholar
  39. Hematy K, Cherk C, Somerville S (2009) Host–pathogen warfare at the plant cell wall. Curr Opin Plant Biol 12:406–413CrossRefPubMedGoogle Scholar
  40. Imai K, Asakawa N, Tsuji T, Akazawa F, Ino A, Sonoyama M, Mitaku S (2008) SOSUI-GramN: high performance prediction for sub-cellular localization of proteins in gram-negative bacteria. Bioinformation 2:417–421CrossRefPubMedPubMedCentralGoogle Scholar
  41. Imlay JA (2006) Iron-sulphur clusters and the problem with oxygen. Mol Microbiol 59:1073–1082CrossRefPubMedGoogle Scholar
  42. Jensen LJ, Gupta R, Blom N, Devos D, Tamames J, Kesmir C, Nielsen H, Staerfeldt HH, Rapacki K, Workman C, Andersen CA, Knudsen S, Krogh A, Valencia A, Brunak S (2002) Prediction of human protein function from post-translational modifications and localization features. J Mol Biol 319:1257–1265CrossRefPubMedGoogle Scholar
  43. Jones P, Binns D, Chang HY, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G, Pesseat S (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30:1236–1240CrossRefPubMedPubMedCentralGoogle Scholar
  44. Kall L, Krogh A, Sonnhammer EL (2007) Advantages of combined transmembrane topology and signal peptide prediction—the Phobius web server. Nucleic Acids Res 35:W429–W432CrossRefPubMedPubMedCentralGoogle Scholar
  45. Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10:845–858CrossRefPubMedGoogle Scholar
  46. Kikot GE, Hours RA, Alconada TM (2009) Contribution of cell wall degrading enzymes to pathogenesis of Fusarium graminearum: a review. J Basic Microbiol 49:231–241CrossRefPubMedGoogle Scholar
  47. Komatsu T, Ishihara S, Tsuchida E, Nishide H, Morokuma C, Nakamura S (2005) Heat-resistant oxygen-carrying hemoproteins consist of recombinant xylanases and synthetic iron (II) porphyrin. Biomacromolecules 6:1489–1494CrossRefPubMedGoogle Scholar
  48. Kragl C, Schrettl M, Abt B, Sarg B, Lindner HH, Haas H (2007) EstB-mediated hydrolysis of the siderophore triacetylfusarinine C optimizes iron uptake of Aspergillus fumigatus. Eukaryot Cell 6:1278–1285CrossRefPubMedPubMedCentralGoogle Scholar
  49. Krishnan S, Prasadarao NV (2012) Outer membrane protein A and OprF: versatile roles in Gram-negative bacterial infections. FEBS J 279:919–931CrossRefPubMedPubMedCentralGoogle Scholar
  50. Krogh A, Larsson B, Von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580CrossRefPubMedGoogle Scholar
  51. Langman L, Young IG, Frost GE, Rosenberg H, Gibson F (1972) Enterochelin system of iron transport in Escherichia coli: mutations affecting ferric-enterochelin esterase. J Bacteriol 112:1142–1149PubMedPubMedCentralGoogle Scholar
  52. Laskowski RA, Swindells MB (2011) LigPlot+: multiple ligand-protein interaction diagrams for drug discovery. J Chem Inf Model 51:2778–2786CrossRefPubMedGoogle Scholar
  53. Lin H, Fischbach MA, Liu DR, Walsh CT (2005) In vitro characterization of salmochelin and enterobactin trilactone hydrolases IroD, IroE, and Fes. J Am Chem Soc 127:11075–11084CrossRefPubMedPubMedCentralGoogle Scholar
  54. Lin HH, Han LY, Zhang HL, Zheng CJ, Xie B, Cao ZW, Chen YZ (2006) Prediction of the functional class of metal-binding proteins from sequence derived physicochemical properties by support vector machine approach. BMC Bioinformatics 7:1CrossRefGoogle Scholar
  55. Lu CH, Lin YS, Chen YC, Yu CS, Chang SY, Hwang JK (2006) The fragment transformation method to detect the protein structural motifs. Proteins 63:636–643CrossRefPubMedGoogle Scholar
  56. Lu CH, Lin Y, Lin JJ, Yu CS (2012) Prediction of metal ion–binding sites in proteins using the fragment transformation method. PLoS ONE 7:e39252CrossRefPubMedPubMedCentralGoogle Scholar
  57. Lubec G, Afjehi-Sadat L (2007) Limitations and pitfalls in protein identification by mass spectrometry. Chem Rev 107:3568–3584CrossRefPubMedGoogle Scholar
  58. Luo Y, Han Z, Chin SM, Linn S (1994) Three chemically distinct types of oxidants formed by iron-mediated Fenton reactions in the presence of DNA. Proc Natl Acad Sci 91:12438–12442CrossRefPubMedPubMedCentralGoogle Scholar
  59. Mathee K, Ciofu O, Sternberg C, Lindum PW, Campbell JI, Jensen P, Johnsen AH, Givskov M, Ohman DE, Molin S, Høiby N, Kharazmi A (1999) Mucoid conversion of Pseudomonas aeruginos by hydrogen peroxide: a mechanism for virulence activation in the cystic fibrosis lung. Microbiology 145:1349–1357CrossRefPubMedGoogle Scholar
  60. Meyer JM (2000) Pyoverdines: pigments, siderophores and potential taxonomic markers of fluorescent Pseudomonas species. Arch Microbiol 174:135–142CrossRefPubMedGoogle Scholar
  61. Muesch A, Hartmann E, Rohde K, Rubartelli A, Sitia R, Rapoport TA (1990) A novel pathway for secretory proteins? Trends Biochem Sci 15:86–88CrossRefPubMedGoogle Scholar
  62. Neilands JB (1995) Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270:26723–26726CrossRefPubMedGoogle Scholar
  63. Noinaj N, Guillier M, Barnard TJ, Buchanan SK (2010) TonB-dependent transporters: regulation, structure, and function. Annu Rev Microbiol 64:43–60CrossRefPubMedPubMedCentralGoogle Scholar
  64. Nwugo CC, Gaddy JA, Zimbler DL, Actis LA (2011) Deciphering the iron response in Acinetobacter baumannii: a proteomics approach. J Proteomics 74:44–58CrossRefPubMedGoogle Scholar
  65. Oerke EC (2006) Crop losses to pests. J Agri Sci 144:31–43CrossRefGoogle Scholar
  66. Oglesby AG, Farrow JM 3rd, Lee JH, Tomaras AP, Greenberg EP, Pesci EC, Vasil ML (2008) The influence of iron on Pseudomonas aeruginosa physiology: a regulatory link between iron and quorum sensing. J Biol Chem 283:15558–15567CrossRefPubMedPubMedCentralGoogle Scholar
  67. Pandey A, Sonti RV (2010) Role of the FeoB protein and siderophore in promoting virulence of Xanthomonas oryzae pv. oryzae on rice. J Bacteriol 192:3187–3203CrossRefPubMedPubMedCentralGoogle Scholar
  68. Peng Z, Hu Y, Xie J, Potnis N, Akhunova A, Jones J, Liu Z, White FF, Liu S (2016) Long read and single molecule DNA sequencing simplifies genome assembly and TAL effector gene analysis of Xanthomonas translucens. BMC Genom 17:1CrossRefGoogle Scholar
  69. Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786CrossRefPubMedGoogle Scholar
  70. Postle K, Larsen RA (2007) TonB-dependent energy transduction between outer and cytoplasmic membranes. Biometals 20:453–465CrossRefPubMedGoogle Scholar
  71. Prasannath K (2013) Pathogenicity and virulence factors of phytobacteria. Sch Acad J Biosci 1:24–33Google Scholar
  72. Pugsley AP (1993) The complete general secretory pathway in gram-negative bacteria. Microbiol Rev 57:50–108PubMedPubMedCentralGoogle Scholar
  73. Rajagopal L, Sundari CS, Balasubramanian D, Sonti RV (1997) The bacterial pigment xanthomonadin offers protection against photodamage. FEBS Lett 415:125–128CrossRefPubMedGoogle Scholar
  74. Reid TJ, Murthy MR, Sicignano A, Tanaka N, Musick WD, Rossmann MG (1981) Structure and heme environment of beef liver catalase at 2.5 A resolution. Proc Natl Acad Sci 78:4767–4771CrossRefPubMedPubMedCentralGoogle Scholar
  75. Rott P, Fleites L, Marlow GC, Royer M, Gabriel DW (2009) An OmpA family outer membrane protein is required for both disease symptom development and sugarcane stalk colonization by Xanthomonas albilineans. Phytopathology 99:S110–S111Google Scholar
  76. Rubartellisg A, Bajettos A, Allavenaz G, Wollman E, Sitia R (1992) Secretion of thioredoxin by normal and neoplastic cells through a leaderless secretory. J Biol Chem 267:24161–24164Google Scholar
  77. Schauer K, Rodionov DA, de Reuse H (2008) New substrates for TonB-dependent transport: do we only see the ‘tip of the iceberg’? Trends Biochem Sci 33:330–338CrossRefPubMedGoogle Scholar
  78. Shane WW, Baumer JS, Teng PS (1987) Crop losses caused by Xanthomonas streak on spring wheat and barley. Plant Dis 71:927–930CrossRefGoogle Scholar
  79. Sideri TC, Willetts SA, Avery SV (2009) Methionine sulphoxide reductases protect iron–sulphur clusters from oxidative inactivation in yeast. Microbiology 155:612–623CrossRefPubMedPubMedCentralGoogle Scholar
  80. Smani Y, Fàbrega A, Roca I, Sánchez-Encinales V, Vila J, Pachón J (2014) Role of OmpA in the multidrug resistance phenotype of Acinetobacter baumannii. Antimicrob Agents Chemother 58:1806–1808CrossRefPubMedPubMedCentralGoogle Scholar
  81. Stewart PS, Roe F, Rayner J, Elkins JG, Lewandowski Z, Ochsner UA, Hassett DJ (2000) Effect of catalase on hydrogen peroxide penetration into Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 66:836–838CrossRefPubMedPubMedCentralGoogle Scholar
  82. Sun YY, Chi H, Sun L (2016) Pseudomonas fluorescens filamentous hemagglutinin, an iron-regulated protein, is an important virulence factor that modulates bacterial pathogenicity. Front Microbiol 7:1320PubMedPubMedCentralGoogle Scholar
  83. Taguchi F, Suzuki T, Inagaki Y, Toyoda K, Shiraishi T, Ichinose Y (2010) The siderophore pyoverdine of Pseudomonas syringae pv. tabaci 6605 is an intrinsic virulence factor in host tobacco infection. J Bacteriol 192:117–126CrossRefPubMedGoogle Scholar
  84. Tusnady GE, Simon I (2001) The HMMTOP transmembrane topology prediction server. Bioinformatics 17:849–850CrossRefPubMedGoogle Scholar
  85. Urban M, Pant R, Raghunath A, Irvine AG, Pedro H, Hammond-Kosack KE (2014) The pathogen-host interactions database (PHI-base): additions and future developments. Nucleic Acids Res 43:D645–D655CrossRefPubMedPubMedCentralGoogle Scholar
  86. Valente E, Assis MC, Alvim IM, Pereira GM, Plotkowski MC (2000) Pseudomonas aeruginosa induces apoptosis in human endothelial cells. Microb Pathog 29:345–356CrossRefPubMedGoogle Scholar
  87. Verma SK, Kumar S, Sheikh I, Malik S, Mathpal P, Chugh V, Kumar S, Prasad R, Dhaliwal HS (2016a) Transfer of useful variability of high grain iron and zinc from Aegilops kotschyi into wheat through seed irradiation approach. Int J Radiat Biol 92:132–139CrossRefPubMedGoogle Scholar
  88. Verma SK, Kumar S, Sheikh I, Sharma P, Mathpal P, Malik S, Kundu P, Awasthi A, Kumar S, Prasad R, Dhaliwal HS (2016b) Induced homoeologous pairing for transfer of useful variability for high grain Fe and Zn from Aegilops kotschyi into wheat. Plant Mol Biol Rep 34:1083CrossRefGoogle Scholar
  89. White FF, Potnis N, Jones JB, Koebnik R (2009) The type III effectors of Xanthomonas. Mol Plant Pathol 10:749–766CrossRefPubMedGoogle Scholar
  90. Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, Geer RC, He J, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Bryant SH (2015) CDD: NCBI’s conserved domain database. Nucleic Acids Res 43:D222–226CrossRefPubMedGoogle Scholar
  91. Yamashita MM, Wesson L, Eisenman G, Eisenberg D (1990) Where metal ions bind in proteins. Proc Natl Acad Sci 87:5648–5652CrossRefPubMedPubMedCentralGoogle Scholar
  92. Yang L, Nilsson M, Gjermansen M, Givskov M, Tolker Nielsen T (2009) Pyoverdine and PQS mediated subpopulation interactions involved in Pseudomonas aeruginosa biofilm formation. Mol Microbiol 74:1380–1392CrossRefPubMedGoogle Scholar
  93. Yu CS, Lin CJ, Hwang JK (2004) Predicting subcellular localization of proteins for Gram-negative bacteria by support vector machines based on peptide compositions. Protein Sci 13:1402–1406CrossRefPubMedPubMedCentralGoogle Scholar
  94. Yu NY, Wagner JR, Laird MR, Melli G, Rey S, Lo R, Dao P, Sahinalp SC, Ester M, Foster LJ, Brinkman FS (2010) PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics 26:1608–1615CrossRefPubMedPubMedCentralGoogle Scholar
  95. Zhu M, Valdebenito M, Winkelmann G, Hantke K (2005) Functions of the siderophore esterases IroD and IroE in iron-salmochelin utilization. Microbiology 151:2363–2372CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Ankita Sharma
    • 1
  • Dixit Sharma
    • 1
  • Shailender Kumar Verma
    • 1
  1. 1.Centre for Computational Biology and Bioinformatics, School of Life SciencesCentral University of Himachal PradeshShahpur, District-KangraIndia

Personalised recommendations