Microbial Ecology

, Volume 72, Issue 3, pp 669–681 | Cite as

Evidence for an Opportunistic and Endophytic Lifestyle of the Bursaphelenchus xylophilus-Associated Bacteria Serratia marcescens PWN146 Isolated from Wilting Pinus pinaster

  • Cláudia S. L. VicenteEmail author
  • Francisco X. Nascimento
  • Pedro Barbosa
  • Huei-Mien Ke
  • Isheng J. Tsai
  • Tomonori Hirao
  • Peter J. A. Cock
  • Taisei Kikuchi
  • Koichi Hasegawa
  • Manuel Mota
Plant Microbe Interactions


Pine wilt disease (PWD) results from the interaction of three elements: the pathogenic nematode, Bursaphelenchus xylophilus; the insect-vector, Monochamus sp.; and the host tree, mostly Pinus species. Bacteria isolated from B. xylophilus may be a fourth element in this complex disease. However, the precise role of bacteria in this interaction is unclear as both plant-beneficial and as plant-pathogenic bacteria may be associated with PWD. Using whole genome sequencing and phenotypic characterization, we were able to investigate in more detail the genetic repertoire of Serratia marcescens PWN146, a bacterium associated with B. xylophilus. We show clear evidence that S. marcescens PWN146 is able to withstand and colonize the plant environment, without having any deleterious effects towards a susceptible host (Pinus thunbergii), B. xylophilus nor to the nematode model C. elegans. This bacterium is able to tolerate growth in presence of xenobiotic/organic compounds, and use phenylacetic acid as carbon source. Furthermore, we present a detailed list of S. marcescens PWN146 potentials to interfere with plant metabolism via hormonal pathways and/or nutritional acquisition, and to be competitive against other bacteria and/or fungi in terms of resource acquisition or production of antimicrobial compounds. Further investigation is required to understand the role of bacteria in PWD. We have now reinforced the theory that B. xylophilus-associated bacteria may have a plant origin.


Bursaphelenchus xylophilus Endophyte Nematode Serratia marcescens Pine wilt disease 



The authors would like to thank Prof. John Jones (The James Hutton Institute) for advice on an earlier draft of this manuscript; Sonia Humphris, Jenny A. Morris, and Pete Hedley (The James Hutton Institute) for all the support given in Serratia sp. PWN146 sequencing. This work was supported by the JSPS KAKENHI Grant numbers P14394 (to CSLV) and 26450204 (to KH); the European Project REPHRAME—Development of improved methods for detection, control and eradication of pine wood nematode in support of EU Plant Health policy, European Union Seventh Framework Programme FP7-KBBE-2010-4; and FEDER Funds through the Operational Programme for Competitiveness Factors - COMPETE and National Funds through FCT—Foundation for Science and Technology under the Strategic Project PEst-C/AGR/UI0115/2011.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Sequence Data

The nucleotide sequence data reported is available in the EMBL database under the accession number ERS1151563.

Supplementary material

248_2016_820_MOESM1_ESM.tif (973 kb)
ESM 1 Figure S1 Genome-to-genome alignment of Serratia marcescens PWN146 with S. marcescens CAV1492, S. marcescens SmUNAM836 and S. marcescens subsp. marcescens Db11 using MAUVE. Locally collinear blocks (LCD) with the same colour indicate syntenic regions. In each LCD, the height of the similarity profile indicates the level of conservation in that genome region. White areas may indicate specific sequences of the genome. The genome rearrangements are indicated by different colour lines. (TIF 973 kb)
248_2016_820_MOESM2_ESM.docx (120 kb)
ESM 2 Table S1 Gene Ontology Serratia marcescens PWN146 complete genome (chromosome and plasmids). These results are based upon BLAST2GO [31] analysis of S. marcescens PWN146 proteome. Table S2 List of genomic islands predicted by at least one method (SIGI-HMM, IslandPath-DIMOB, IslandPick) in IslandViewer 3.0 [39], using the available genomes as reference: S. marcescens Db11, S. marcescens CAV1492, S. marcescens WW4, S. marcescens SM39, and S. marcescens FGI94. A, indicate the unique genes found in S. marcescens PWN146 genome using OrthoFinder [41] in all-against-all BlastP between PWN146 and all S. marcescens completely sequenced (Table 1). Table S3 Nematicidal effect of Serratia marcescens PWN146 to Bursaphelenchus xylophilus. Determination in accordance with Barbosa et al. []. Table S4 List of genes putatively involved in Serratia marcescens PWN146 plant-associated life-style. The list is complemented with KEGG annotation and the description accordingly. Table S5 Biochemical characterization of Serratia marcescens PWN146 according to the VITEK 2 Systems, with GN (Gram-negative) cards. Positive and negative results are indicated, respectively, by (+) and (−). (DOCX 119 kb)
248_2016_820_MOESM3_ESM.tif (30 kb)
ESM 3 Figure S2 Classification of KEGG KO terms of Serratia marcescens PWN146 complete genome (chromosome and plasmids). This classification was obtained in KEGG BLASTKoala tool [32]. (TIF 30 kb)
248_2016_820_MOESM4_ESM.tif (1.2 mb)
ESM 4 Figure S3 SEM images of Bursaphelenchus xylophilus Ka4 without bacteria association. (TIF 1202 kb)
248_2016_820_MOESM5_ESM.tif (181 kb)
ESM 5 Figure S4 Pathogenicity trials in 4-year-old Pinus thunbergii. The treatments established were: (1) control P. thunbergii (inoculation with sterile ddH2O); (2) P. thunbergii inoculated with B. xylophilus Ka4; (3) P. thunbergii inoculated with S. marcescens PWN146; and (4) P. thunbergii inoculated with B. xylophilus Ka4 in association with S. marcescens PWN146.WAI indicates weeks after inoculation. (TIF 180 kb)


  1. 1.
    Vicente C, Espada M, Vieira P, Mota M (2012) Pine Wilt Disease: a threat to European forestry. Eur J Plant Pathol 133:89–99CrossRefGoogle Scholar
  2. 2.
    Jones JT, Moens M, Mota M, Li H, Kikuchi T (2008) Bursaphelenchus xylophilus: opportunities in comparative genomics and molecular host–parasite interactions. Mol Plant Pathol 9:357–368CrossRefPubMedGoogle Scholar
  3. 3.
    Futai K (2013) Pine wood nematode, Bursaphelenchus xylophilus. Annu Rev Phytopathol 51:61–83, 65CrossRefPubMedGoogle Scholar
  4. 4.
    Zhao L, Mota M, Vieira P, Butcher RA, Sun J (2014) Interspecific communication between pinewood nematode, its insect vector, and associated microbes. Trends Parasitol 30:299–308CrossRefPubMedGoogle Scholar
  5. 5.
    Zhao BGZ, Ang HLW, An SFH, An ZMH (2003) Distribution and pathogenicity of bacteria species carried by Bursaphelenchus xylophilus in China. Nematol 5:899–906CrossRefGoogle Scholar
  6. 6.
    Zhao BG, Lin F (2005) Mutualistic symbiosis between Bursaphelenchus xylophilus and bacteria of the genus Pseudomonas. Forest Pathology 35:339–345CrossRefGoogle Scholar
  7. 7.
    Vicente CSL, Ikuyo Y, Mota M, Hasegawa K (2013) Pinewood nematode-associated bacteria contribute to oxidative stress resistance of Bursaphelenchus xylophilus. BMC Microbiol 13:299CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Cheng XY, Tian XL, Wang YS, Lin RM, Mao ZC, Chen N, Xie BY (2013) Metagenomic analysis of the pinewood nematode microbiome reveals a symbiotic relationship critical for xenobiotics degradation. Sci Rep 3:1–10CrossRefGoogle Scholar
  9. 9.
    Paiva G, Proença DN, Francisco R et al (2013) Nematicidal bacteria associated to pinewood nematode produce extracellular proteases. PLoS ONE 8:e79705CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Nascimento FX, Hasegawa K, Mota M, Vicente CSL (2015) Bacterial role in pine wilt disease development—review and future perspectives. Environ Microbiol Rep 7:51–63CrossRefPubMedGoogle Scholar
  11. 11.
    Proença DN, Francisco RCV, Lopes A, Fonseca L, Abrantes IMO, Morais PV (2010) Diversity of bacteria associated with Bursaphelenchus xylophilus and other nematodes isolated from Pinus pinaster trees with pine wilt disease. PloS ONE 5:e15191CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Vicente CSL, Nascimento F, Espada M, Mota M, Oliveira S (2011) Bacteria associated with the pinewood nematode Bursaphelenchus xylophilus collected in Portugal. Ant Van Leeuwenhoek 100:477–481CrossRefGoogle Scholar
  13. 13.
    Grimont F, Grimont P (2006) The genus Serratia. Prokaryotes 6:219–244Google Scholar
  14. 14.
    Euzéby T (2015) List of Prokaryotic names with standing in nomenclature. Accessed in 2 of December 2015.Google Scholar
  15. 15.
    Iguchi A, Nagaya Y, Pradel E et al (2014) Genome evolution and plasticity of Serratia marcescens, an important multidrug-resistant nosocomial pathogen. Genome Biol Evol 6:2096–2110CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Flyg C, Kenne K, Boman HG (1980) Insect pathogenic properties of Serratia marcescens: phage-resistant mutants with a decreased resistance to Cecropia immunity and a decreased virulence to Drosophila. J Gen Microbiol 120:173–181PubMedGoogle Scholar
  17. 17.
    Gillis A, Rodríguez M, Santana MA (2014) Serratia marcescens associated with bell pepper (Capsicum annuum L.) soft-rot disease under greenhouse conditions. Eur J Plant Pathol 138:1–8CrossRefGoogle Scholar
  18. 18.
    Vicente CSL, Nascimento F, Espada M, Barbosa P, Mota M, Glick BR, Oliveira S (2012) Characterization of bacteria associated with pinewood Nematode Bursaphelenchus xylophilus. PLoS ONE 7:e46661CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Brenner S (1974) The genetics of the nematode Caenorhabditis elegans. Genetics 77:71–94PubMedPubMedCentralGoogle Scholar
  20. 20.
    Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9:671–675CrossRefPubMedGoogle Scholar
  21. 21.
    Takemoto S (2008) Population ecology of Bursaphelenchus xylophilus. In Pine Wilt Disease. Zhao BG, Futai K, Sutherland JR, Takeuchi Y. Kato Bunmeisha: Springer. pp. 105-122.Google Scholar
  22. 22.
    Barbosa PB, Ima ASL, Ieira PV, Ias LSD, Inoco MTT, Arroso JGB, Edro LGP (2010) Nematicidal activity of essential oils and volatiles derived from Portuguese aromatic flora against the pinewood nematode, Bursaphelenchus xylophilus. Nematol 42:8–16Google Scholar
  23. 23.
    Futai K, Furuno T (1979) The variety of resistances among pine species to pine wood nematode, Bursaphelenchus lignicolus. Bull Kyoto Univ For 51:23–36Google Scholar
  24. 24.
    Fang ZD (1998) Methods in research of plant disease. Chinese Agricultural Publishing House, Beijing, ChinaGoogle Scholar
  25. 25.
    Margulies M, Egholm M, Altman W et al (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376–380PubMedPubMedCentralGoogle Scholar
  26. 26.
    Chevreux B, Wetter T, Suhai S (1999) Genome sequence assembly using trace signals and additional sequence information. Computer Science and Biology: Proceedings of the German Conference on Bioinformatics (GCB) 99:45–56Google Scholar
  27. 27.
    Berlin K, Koren S, Chin CS, Drake JP, Landolin JM, Phillippy AM (2015) Assembling large genomes with single-molecule sequencing and locality- sensitive hashing. Nat Biotechnol 33:623–630CrossRefPubMedGoogle Scholar
  28. 28.
    Chin CS, Alexander DH, Marks P et al (2013) Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nature Methods 10:563–569CrossRefPubMedGoogle Scholar
  29. 29.
    Darling ACE, Mau B, Blattner FR, Perna NT (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14:1394–1403CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Seeman T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069CrossRefGoogle Scholar
  31. 31.
    Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676CrossRefPubMedGoogle Scholar
  32. 32.
    Moriya Y, Itoh M, Okuda S, Yoshizawa A, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35:W182–W185CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B (2000) Artemis: sequence visualization and annotation. Bioinformatics 16:944–945CrossRefPubMedGoogle Scholar
  34. 34.
    Alikhan NF, Petty NK, Zakour NLB, Beatson SA (2011) BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genom 12:402CrossRefGoogle Scholar
  35. 35.
    Tatusova T, Ciufo S, Fedorov B, O’Neill K, Tolstoy I (2014) RefSeq microbial genomes database: new representation and annotation strategy. Nuclei Acids Res 42:D553–D559CrossRefGoogle Scholar
  36. 36.
    Aylward FO, Tremmel DM, Starrett GJ et al (2013) Complete genome of Serratia sp. strain associated with leaf-cutter ant fungus gardens. Genome Announc 1:e0023912PubMedGoogle Scholar
  37. 37.
    Chung WC, Chen LL, Lo WS, Kuo PA, Tu J, Kuo CH (2013) Complete genome sequence of Serratia marcescens WW4. Genome Announc 2:e00126123Google Scholar
  38. 38.
    Sandner-Miranda L, Vinuesa P, Soberón-Chávez G, Morales-Espinosa R (2016) Complete genome sequence of Serratia marcescens SmUNAM836, a nonpigmented multidrug-resistant strain isolated from a Mexican patient with obstructive pulmonary disease. Genome Announc 4:e01417-15CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Dhillon BK, Laird MR, Shay JA et al (2015) IslandViewer 3: more flexible, interactive genomic island discovery, visualization and analysis. Nucleic Acids Res 43:W104–W108CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106:19126–19131CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Emms DM, Kelly S (2015) OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol 16:157CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224CrossRefPubMedGoogle Scholar
  43. 43.
    Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 1–12.Google Scholar
  44. 44.
    Shinya R, Morisaka H, Takeuchi Y, Ueda M, Futai K (2010) Comparison of the surface coat proteins of the pine wood nematode appeared during host pine infection and in vitro culture by a proteomic approach. Phytopathol 100:1289–1297CrossRefGoogle Scholar
  45. 45.
    Shintani M, Sanchez ZK, Kimbara K (2015) Genomics of microbial plasmids classification and identification based on replication and transfer systems and host taxonomy. Front Microbiol 6:242CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Smillie C, Garcillán-Barcia MP, Francia MV, Rocha EP, de la Cruz F (2010) Mobility of plasmids. Microbiol Mol Biol Rev 74:434–452CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Hayes F (2003) Toxins-antitoxins: plasmid maintenance, programmed cell death, and cell cycle arrest. Science 301:1496–1499CrossRefPubMedGoogle Scholar
  48. 48.
    Mitter B, Petric A, Shin MW, Chain PSG, Hauberg-Lotte L, Reinhold-Hurek B et al (2013) Comparative genome analysis of Burkholderia phytofirmans PsJN reveals a wide spectrum of endophytic lifestyles based on interaction strategies with host plants. Front Plant Sci 4:1–15CrossRefGoogle Scholar
  49. 49.
    Darmon E, Leach DRF (2014) Bacterial genome instability. Microbiol Mol Biol Rev 78:1–39CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Ternan NG, McGrath JW, McMullan G, Quinn JP (1998) Organophosphonates: occurrence, synthesis and biodegradation by microorganisms. World J Microbiol Biotechnol 14:635–647CrossRefGoogle Scholar
  51. 51.
    Reith ME, Singh RK, Curtis B et al (2008) The genome of Aeromonas salmonicida subsp. salmonicida A449: insights into the evolution of a fish pathogen. BMC Genomics 9:427CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Zhao BG, Lin F, Guo D, Li R, Li SN, Kulinich O, Ryss A (2009) Pathogenic roles of the bacteria carried by Bursaphelenchus mucronatus. J Nematol 41:11–16PubMedPubMedCentralGoogle Scholar
  53. 53.
    Ali S, Duan J, Charles TC, Glick BR (2014) A bioinformatics approach to the determination of genes involved in endophytic behavior in Burkholderia spp. J Theor Biol 343:193–198CrossRefPubMedGoogle Scholar
  54. 54.
    Wu X, Monchy S, Taghavi S, Zhu W, Ramos J, van der Lelie D (2010) Comparative genomics and functional analysis of niche-specific adaptation in Pseudomonas putida. FEMS Microbiol Rev 35:299–323CrossRefPubMedCentralGoogle Scholar
  55. 55.
    Couillault C, Ewbank JJ (2002) Diverse bacteria are pathogens of Caenorhabditis elegans. Infect Immun 70:4705–4707CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Sato K, Yoshiga T, Hasegawa K (2014) Activated and inactivated immune responses in Caenorhabditis elegans against Photorhabdus luminescens TT01. SpringerPlus 3:274CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Tripathi LP, Sowdhamini R (2008) Genome-wide survey of prokaryotic serine proteases: analysis of distribution and domain architectures of five serine protease families. BMC Genomics 9:549CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Vicente CSL, Nascimento FX, Ikuyo Y, Cock PJA, Mota M, Hasegawa K (2016) The genome and genetics of a high oxidative stress tolerant Serratia sp. LCN16 isolated from the plant parasitic nematode Bursaphelenchus xylophilus. BMC Genomics 17:301CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Berg G (2009) Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 84:11–18CrossRefPubMedGoogle Scholar
  60. 60.
    Taghavi S, Van der Lelie D, Hoffman A, Zhang YB, Walla MD, Vangronsveld J et al (2010) Genome sequence of the plant growth promoting endophytic bacterium Enterobacter sp. 638. PLoS Genet 6:e1000943CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Hardoim PR, van Overbeek LS, van Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471CrossRefPubMedGoogle Scholar
  62. 62.
    Friesen ML, Porter SS, Stark SC, Von Wettberg EJ, Sachs JL, Martinez-Romero E (2011) Microbially mediated plant functional traits. Annu Rev Ecol Evol Syst 42:23–46CrossRefGoogle Scholar
  63. 63.
    Frank AC (2011) The genomes of endophytic bacteria. In Endophytes of Forest Trees: Biology and Applications. Pirttilä AM, Frank AC (eds). Springer Science+Business Media. pp. 107-136.Google Scholar
  64. 64.
    Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signalling. J Exp Bot 65:1229–1240CrossRefPubMedGoogle Scholar
  65. 65.
    Fones H, Preston GM (2012) Reactive oxygen and oxidative stress tolerance in plant pathogenic Pseudomonas. FEMS Microbiol Lett 327:1–8CrossRefPubMedGoogle Scholar
  66. 66.
    Kim J, Park W (2014) Oxidative stress response in Pseudomonas putida. Appl Microbiol Biotechnol 98:6933–6946CrossRefPubMedGoogle Scholar
  67. 67.
    Chiang SM, Schellhorn HE (2012) Regulators of oxidative stress response genes in Escherichia coli and their functional conservation in bacteria. Arch Biochem Biophys 525:161–169CrossRefPubMedGoogle Scholar
  68. 68.
    Zeidler D, Zahringer U, Gerber I et al (2004) Innate immunity in Arabidopsis thaliana: lipopolysaccharides activate nitric oxide synthase (NOS) and induce defence genes. Proc Nat Acad Sci USA 44:15811–15816CrossRefGoogle Scholar
  69. 69.
    Li K, Chen WH, Bruner ST (2015) Structure and mechanism of siderophore-interacting protein from the fuscachelin gene cluster of Thermobifida fusca. Biochem 54:3989–4000CrossRefGoogle Scholar
  70. 70.
    Taghavi S, Garafola C, Monchy S et al (2009) Genome survey and characterization of endophytic bacteria exhibiting a beneficial effect on growth and development of poplar trees. Appl Environ Microbiol 75:748–757CrossRefPubMedGoogle Scholar
  71. 71.
    Martin VJJ, Yu Z, Mohn MW (1999) Recent advances in understanding resin acid biodegradation: microbial diversity and metabolism. Arch Microbiol 172:131–138CrossRefPubMedGoogle Scholar
  72. 72.
    Adams AS, Aylward FO, Adams SM et al (2013) Mountain pine beetles colonizing historical and naïve host trees are associated with a bacterial community highly enriched in genes contributing to terpene metabolism. App Environ Microbiol 79:3468CrossRefGoogle Scholar
  73. 73.
    Kende H (1993) Ethylene biosynthesis. Annu. Annu Rev Plant Physiol Plant Mol Biol 44:283–307CrossRefGoogle Scholar
  74. 74.
    Ryu CM, Farag MA, Hu CH et al (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Nat Acad Sci USA 100:4927–4932CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Huang M, Oppermann-Sanio FB, Steinbuchel A (1999) Biochemical and molecular characterization of the Bacillus subtilis acetoin catabolic pathway. J Bacteriol 181:3837–3841PubMedPubMedCentralGoogle Scholar
  76. 76.
    Choi O, Kim J, Kim JG et al (2008) Pyrroloquinoline quinone is a plant growth promotion factor produced by Pseudomonas fluorescens B16. Plant Physiol 146:657–668CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Redondo-Nieto M, Barret M, Morrissey J et al (2013) Genome sequence reveals that Pseudomonas fluorescens F113 possesses a large and diverse array of systems for rhizosphere function and host interaction. BMC Genomics 14:54CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Purushotham P, Sai Arun PVP, Prakash JSS, Podile AR (2012) Chitin binding proteins act synergistically with chitinases in Serratia proteamaculans 568. PloS ONE 7:e36714CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Wang T, Si M, Song Y et al (2015) Type VI secretion system transports Zn2+ to combat multiple stresses and host immunity. PloS Pathogens 11:e1005020CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Proença DN, Espírito-Santo C, Grass G, Morais PV (2012) Draft genome sequence of Pseudomonas sp. strain M47T1, carried by Bursaphelenchus xylophilus isolated from Pinus pinaster. J Bacteriol 194:4789–4790CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Proença DN, Espírito-Santo C, Grass G, Morais PV (2012) Draft genome sequence of Serratia sp. strain M24T3, isolated from pinewood disease nematode Bursaphelenchus xylophilus. J Bacteriol 194:3764CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Feng K, Li R, Chen Y, Zhao B, Yin T (2015) Sequencing and analysis of the Pseudomonas fluorescens GcM5-1A genome: a pathogen living in the surface coat of Bursaphelenchus xylophilus. PloS ONE 10:e0141515CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Cláudia S. L. Vicente
    • 1
    • 2
    Email author
  • Francisco X. Nascimento
    • 1
    • 3
  • Pedro Barbosa
    • 1
  • Huei-Mien Ke
    • 4
    • 5
  • Isheng J. Tsai
    • 4
  • Tomonori Hirao
    • 6
  • Peter J. A. Cock
    • 7
  • Taisei Kikuchi
    • 8
  • Koichi Hasegawa
    • 2
  • Manuel Mota
    • 1
    • 9
  1. 1.NemaLab/ICAAM—Institute of Mediterranean Agricultural and Environmental Sciences, Biology DepartmentUniversity of ÉvoraÉvoraPortugal
  2. 2.Department of Environmental BiologyChubu UniversityKasugaiJapan
  3. 3.Departamento de Microbiologia, Laboratório de Microbiologia do SoloUniversidade Federal de Santa CatarinaFlorianópolisBrazil
  4. 4.Biodiversity Research Center, Academia SinicaTaipeiTaiwan
  5. 5.Ph.D. Program in Microbial GenomicsNational Chung Hsing University and Academia SinicaTaichungTaiwan
  6. 6.Forest Tree Breeding Center, Forestry and Forest Products Research InstituteIbarakiJapan
  7. 7.Information and Computer Sciences group, The James Hutton InstituteDundeeUK
  8. 8.Division of Parasitology, Faculty of MedicineUniversity of MiyazakiMiyazakiJapan
  9. 9.Departamento de Ciências da VidaUniversidade Lusófona de Humanidades e TecnologiasLisbonPortugal

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