Stenotrophomonas comparative genomics reveals genes and functions that differentiate beneficial and pathogenic bacteria

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Alavi, Peyman ^a   Starcher, Margaret R ^a   Thallinger, Gerhard G ^a   Zachow, Christin ^a   Müller, Henry ^a   Berg, Gabriele ^a  

^a GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

Author keywords

Genomics; Human pathogens; Stress Protecting Agent (SPA); Transcriptomics

Indexed keywords

ANTIBIOTIC AGENT; CHITINASE; HEAT SHOCK PROTEIN; PROTEINASE; SPERMIDINE; BACTERIAL POLYSACCHARIDE; BACTERIAL PROTEIN;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; BIOLOGICAL CONTROL AGENT; CONTROLLED STUDY; GENOME ANALYSIS; HUMAN; NONHUMAN; QUORUM SENSING; RISK ASSESSMENT; SALT TOLERANCE; SEQUENCE HOMOLOGY; SPECIES COMPARISON; STENOTROPHOMONAS; STENOTROPHOMONAS MALTOPHILIA; STENOTROPHOMONAS RHIZOPHILA; TEMPERATURE SENSITIVITY; TYPE II SECRETION SYSTEM; TYPE V SECRETION SYSTEM; TYPE VI SECRETION SYSTEM; UPREGULATION; BACTERIAL SECRETION SYSTEM; COMPARATIVE STUDY; ENZYMOLOGY; FIMBRIA; GENETICS; GENOTYPE ENVIRONMENT INTERACTION; HEAT SHOCK RESPONSE; HOST PATHOGEN INTERACTION; MICROBIOLOGY; PATHOGENICITY; PLANT; RHIZOSPHERE; SPECIES DIFFERENCE;

BACTERIA (MICROORGANISMS); STENOTROPHOMONAS; STENOTROPHOMONAS MALTOPHILIA; STENOTROPHOMONAS RHIZOPHILA;

BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CHITINASE; FIMBRIAE, BACTERIAL; GENE-ENVIRONMENT INTERACTION; GENES, BACTERIAL; HEAT-SHOCK RESPONSE; HOST-PATHOGEN INTERACTIONS; HUMANS; PLANTS; POLYSACCHARIDES, BACTERIAL; QUORUM SENSING; RHIZOSPHERE; SPECIES SPECIFICITY; STENOTROPHOMONAS;

EID: 84902300477     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-482     Document Type: Article

References (52)

1. Hartmann A, Rothballer M, Schmid M. Lorenz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research. Plant and Soil 2008, 312(1-2):7-14.
2. Berg G, Eberl L, Hartmann A. The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environ Microbiol 2005, 7(11):1673-1685. 10.1111/j.1462-2920.2005.00891.x, 16232283.
3. Mendes R, Garbeva P, Raaijmakers JM. The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev 2013, 37(5):634-663. 10.1111/1574-6976.12028, 23790204.
4. Berg G, Roskot N, Smalla K. Genotypic and phenotypic relationships between clinical and environmental isolates of Stenotrophomonas maltophilia. J Clin Microbiol 1999, 37(11):3594-3600. 85701, 10523559.
5. Martinez JL. Bacterial pathogens: from natural ecosystems to human hosts. Environ Microbiol 2013, 15(2):325-333. 10.1111/j.1462-2920.2012.02837.x, 22857004.
6. Berg G, Egamberdieva D, Lugtenberg B, Hagemann M. Symbiotic plant-microbe interactions: stress protection, plant growth promotion, and biocontrol by Stenotrophomonas. Symbioses and Stress 2010, 445-460. Netherlands: Anonymous Springer.
7. Hirsch PR, Mauchline TH. Who's who in the plant root microbiome?. Nat Biotechnol 2012, 30(10):961-962. 10.1038/nbt.2387, 23051815.
8. Ryan RP, Monchy S, Cardinale M, Taghavi S, Crossman L, Avison MB, Berg G, van der Lelie D, Dow JM. The versatility and adaptation of bacteria from the genus Stenotrophomonas. Nat Rev Microbiol 2009, 7(7):514-525. 10.1038/nrmicro2163, 19528958.
9. Brooke JS. Stenotrophomonas maltophilia: an emerging global opportunistic pathogen. Clin Microbiol Rev 2012, 25(1):2-41. 10.1128/CMR.00019-11, 3255966, 22232370.
10. Sanchez MB, Hernandez A, Martinez JL. Stenotrophomonas maltophilia drug resistance. Future Microbiol 2009, 4(6):655-660. 10.2217/fmb.09.45, 19659422.
11. Wolf A, Fritze A, Hagemann M, Berg G. Stenotrophomonas rhizophila sp. nov., a novel plant-associated bacterium with antifungal properties. Int J Syst Evol Microbiol 2002, 52(Pt 6):1937-1944.
12. Ribbeck-Busch K, Roder A, Hasse D, de Boer W, Martinez JL, Hagemann M, Berg G. A molecular biological protocol to distinguish potentially human pathogenic Stenotrophomonas maltophilia from plant-associated Stenotrophomonas rhizophila. Environ Microbiol 2005, 7(11):1853-1858. 10.1111/j.1462-2920.2005.00928.x, 16232300.
13. Berg G, Alavi P, Schmidt C, Egamberdieva D, Kamilova F, Lugtenberg B. Molecular Microbial Ecology of the Rhizosphere. Volume 2 2013, Oxford, UK: Wiley-Blackwell, de Bruijn FJ, 1.
14. Schmidt CS, Alavi M, Cardinale M, Müller H, Berg G. Stenotrophomonas rhizophila DSM14405T promotes plant growth probably by altering fungal communities in the rhizosphere. Biol Fertility Soils 2012, 48(8):947-960.
15. Egamberdieva D, Kucharova Z, Davranov K, Berg G, Makarova N, Azarova T, Chebotar V, Tikhonovich I, Kamilova F, Validov SZ. Bacteria able to control foot and root rot and to promote growth of cucumber in salinated soils. Biol Fertility Soils 2011, 47(2):197-205.
16. Berg G. Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 2009, 84(1):11-18. 10.1007/s00253-009-2092-7, 19568745.
17. Ehlers R. Regulation of Biological Control Agents 2011, 417. Dordrecht, Heidelberg, London, New York: Springer Science+Business Media.
18. Schenk PM, Carvalhais LC, Kazan K. Unraveling plant-microbe interactions: can multi-species transcriptomics help?. Trends Biotechnol 2012, 30(3):177-184. 10.1016/j.tibtech.2011.11.002, 22209623.
19. Köberl M, Schmidt R, Ramadan EM, Bragina A, Müller H, Berg G. Biocontrol Strategies and Next Generation Sequencing: Organic Desert Agriculture in Egypt 2013, Brisbane, Australia: iConcept Press.
20. Crossman LC, Gould VC, Dow JM, Vernikos GS, Okazaki A, Sebaihia M, Saunders D, Arrowsmith C, Carver T, Peters N, Adlem E, Kerhornou A, Lord A, Murphy L, Seeger K, Squares R, Rutter S, Quail MA, Rajandream MA, Harris D, Churcher C, Bentley SD, Parkhill J, Thomson NR, Avison MB. The complete genome, comparative and functional analysis of Stenotrophomonas maltophilia reveals an organism heavily shielded by drug resistance determinants. Genome Biol 2008, 9(4):R74-2008-9-4-r74.
21. Taghavi S, Garafola C, Monchy S, Newman L, Hoffman A, Weyens N, Barac T, Vangronsveld J, van der Lelie D. Genome survey and characterization of endophytic bacteria exhibiting a beneficial effect on growth and development of poplar trees. Appl Environ Microbiol 2009, 75(3):748-757. 10.1128/AEM.02239-08, 2632133, 19060168.
22. Barber CE, Tang JL, Feng JX, Pan MQ, Wilson TJ, Slater H, Dow JM, Williams P, Daniels MJ. A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule. Mol Microbiol 1997, 24(3):555-566. 10.1046/j.1365-2958.1997.3721736.x, 9179849.
23. Wang LH, He Y, Gao Y, Wu JE, Dong YH, He C, Wang SX, Weng LX, Xu JL, Tay L, Fang RX, Zhang LH. A bacterial cell-cell communication signal with cross-kingdom structural analogues. Mol Microbiol 2004, 51(3):903-912.
24. Deng Y, Wu J, Tao F, Zhang LH. Listening to a new language: DSF-based quorum sensing in Gram-negative bacteria. Chem Rev 2011, 111(1):160-173. 10.1021/cr100354f, 21166386.
25. Ryan RP, Dow JM. Communication with a growing family: diffusible signal factor (DSF) signaling in bacteria. Trends Microbiol 2011, 19(3):145-152. 10.1016/j.tim.2010.12.003, 21227698.
26. Slater H, Alvarez-Morales A, Barber CE, Daniels MJ, Dow JM. A two-component system involving an HD-GYP domain protein links cell-cell signalling to pathogenicity gene expression in Xanthomonas campestris. Mol Microbiol 2000, 38(5):986-1003.
27. Fouhy Y, Scanlon K, Schouest K, Spillane C, Crossman L, Avison MB, Ryan RP, Dow JM. Diffusible signal factor-dependent cell-cell signaling and virulence in the nosocomial pathogen Stenotrophomonas maltophilia. J Bacteriol 2007, 189(13):4964-4968. 10.1128/JB.00310-07, 1913462, 17468254.
28. Pratt LA, Kolter R. Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol Microbiol 1998, 30(2):285-293. 10.1046/j.1365-2958.1998.01061.x, 9791174.
29. Vande Broek A, Lambrecht M, Vanderleyden J. Bacterial chemotactic motility is important for the initiation of wheat root colonization by Azospirillum brasilense. Microbiology 1998, 144(Pt 9):2599-2606.
30. de Weert S, Vermeiren H, Mulders IH, Kuiper I, Hendrickx N, Bloemberg GV, Vanderleyden J, De Mot R, Lugtenberg BJ. Flagella-driven chemotaxis towards exudate components is an important trait for tomato root colonization by Pseudomonas fluorescens. Mol Plant Microbe Interact 2002, 15(11):1173-1180. 10.1094/MPMI.2002.15.11.1173, 12423023.
31. Minkwitz A, Berg G. Comparison of antifungal activities and 16S ribosomal DNA sequences of clinical and environmental isolates of Stenotrophomonas maltophilia. J Clin Microbiol 2001, 39(1):139-145. 10.1128/JCM.39.1.139-145.2001, 87693, 11136762.
32. Roder A, Hoffmann E, Hagemann M, Berg G. Synthesis of the compatible solutes glucosylglycerol and trehalose by salt-stressed cells of Stenotrophomonas strains. FEMS Microbiol Lett 2005, 243(1):219-226. 10.1016/j.femsle.2004.12.005, 15668022.
33. Huang TP, Somers EB, Wong AC. Differential biofilm formation and motility associated with lipopolysaccharide/exopolysaccharide-coupled biosynthetic genes in Stenotrophomonas maltophilia. J Bacteriol 2006, 188(8):3116-3120. 10.1128/JB.188.8.3116-3120.2006, 1446987, 16585771.
34. Smith HE, Damman M, van der Velde J, Wagenaar F, Wisselink HJ, Stockhofe-Zurwieden N, Smits MA. Identification and characterization of the cps locus of Streptococcus suis serotype 2: the capsule protects against phagocytosis and is an important virulence factor. Infect Immun 1999, 67(4):1750-1756. 96524, 10085014.
35. Boyce JD, Adler B. The capsule is a virulence determinant in the pathogenesis of Pasteurella multocida M1404 (B:2). Infect Immun 2000, 68(6):3463-3468. 10.1128/IAI.68.6.3463-3468.2000, 97626, 10816499.
36. Reckseidler SL, DeShazer D, Sokol PA, Woods DE. Detection of bacterial virulence genes by subtractive hybridization: identification of capsular polysaccharide of Burkholderia pseudomallei as a major virulence determinant. Infect Immun 2001, 69(1):34-44. 10.1128/IAI.69.1.34-44.2001, 97852, 11119486.
37. Cuccui J, Milne TS, Harmer N, George AJ, Harding SV, Dean RE, Scott AE, Sarkar-Tyson M, Wren BW, Titball RW, Prior JL. Characterization of the Burkholderia pseudomallei K96243 capsular polysaccharide I coding region. Infect Immun 2012, 80(3):1209-1221. 10.1128/IAI.05805-11, 3294636, 22252864.
38. Monday SR, Schiller NL. Alginate synthesis in Pseudomonas aeruginosa: the role of AlgL (alginate lyase) and AlgX. J Bacteriol 1996, 178(3):625-632. 177704, 8550492.
39. Lyczak JB, Cannon CL, Pier GB. Lung infections associated with cystic fibrosis. Clin Microbiol Rev 2002, 15(2):194-222. 10.1128/CMR.15.2.194-222.2002, 118069, 11932230.
40. Stapper AP, Narasimhan G, Ohman DE, Barakat J, Hentzer M, Molin S, Kharazmi A, Hoiby N, Mathee K. Alginate production affects Pseudomonas aeruginosa biofilm development and architecture, but is not essential for biofilm formation. J Med Microbiol 2004, 53(Pt 7):679-690.
41. Al-Whaibi MH, Siddiqui MH, Al-Munqadhi BM, Sakran AM, Ali HM, Basalah MO. Influence of plant growth regulators on growth performance and photosynthetic pigments status of Eruca sativa Mill. J Med Plants Res 2012, 6(10):1948-1954.
42. Alavi P, Starcher MR, Zachow C, Muller H, Berg G. Root-microbe systems: the effect and mode of interaction of Stress Protecting Agent (SPA) Stenotrophomonas rhizophila DSM14405 (T.). Front Plant Sci 2013, 4:141. 3653106, 23717321.
43. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 2010, 11:119-2105-11-119.
44. Laslett D, Canback B. ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res 2004, 32(1):11-16. 10.1093/nar/gkh152, 373265, 14704338.
45. Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T, Ussery DW. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 2007, 35(9):3100-3108. 10.1093/nar/gkm160, 1888812, 17452365.
46. Van Domselaar GH, Stothard P, Shrivastava S, Cruz JA, Guo A, Dong X, Lu P, Szafron D, Greiner R, Wishart DS. BASys: a web server for automated bacterial genome annotation. Nucleic Acids Res 2005, 33(Web Server issue):W455-9. 1160269, 15980511.
47. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS, Smirnov S, Sverdlov AV, Vasudevan S, Wolf YI, Yin JJ, Natale DA. The COG database: an updated version includes eukaryotes. BMC Bioinformatics 2003, 4:41. 10.1186/1471-2105-4-41, 222959, 12969510.
48. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, Holm L, Sonnhammer EL, Eddy SR, Bateman A. The Pfam protein family's database. Nucleic Acids Res 2010, 38(Database issue):D211-D222. 2808889, 19920124.
49. Gene Ontology Consortium Creating the gene ontology resource: design and implementation. Genome Res 2001, 11(8):1425-1433. 10.1101/gr.180801, 311077, 11483584, Gene Ontology Consortium.
50. Darling AE, Mau B, Perna NT. ProgressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 2010, 5(6):e11147. 10.1371/journal.pone.0011147, 2892488, 20593022.
51. Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, Parkhill J. ACT: the Artemis Comparison Tool. Bioinformatics 2005, 21(16):3422-3423. 10.1093/bioinformatics/bti553, 15976072.
52. Carver T, Thomson N, Bleasby A, Berriman M, Parkhill J. DNAPlotter: circular and linear interactive genome visualization. Bioinformatics 2009, 25(1):119-120. 10.1093/bioinformatics/btn578, 2612626,2612626, 18990721.