Skip to main content
Log in

Pinewood Nematode Alters the Endophytic and Rhizospheric Microbial Communities of Pinus massoniana

  • Host Microbe Interactions
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Pinewood nematode, Bursaphelenchus xylophilus, is one of the greatest threats to pine trees and is spreading all over the world. During the nematode’s pathogenesis, plant microorganisms play important roles. However, many microbial communities, such as that in Pinus massoniana, a major host of B. xylophilus that is widely distributed in China, are not well studied, especially the fungal communities. Here, the endophytic and rhizospheric bacterial and fungal communities associated with healthy and B. xylophilus–infected P. massoniana were analyzed. The results showed that 7639 bacterial and 3108 fungal OTUs were annotated from samples of P. massoniana, the rhizosphere, and B. xylophilus. There were significant diversity differences of endophytic microbes between healthy and infected P. massoniana. The abundances of endophytic bacteria Paenibacillus, unidentified_Burkholderiaceae, Serratia, Erwinia, and Pseudoxanthomonas and fungi Penicillifer, Zygoascus, Kirschsteiniothelia, Cyberlindnera, and Sporothrix in infected pines were greater than those in healthy pines, suggesting an association of particular microbial abundances with the pathogenesis of B. xylophilus in pines. Meanwhile, the abundances of microbes of unidentified_Burkholderiaceae, Saitozyma, and Pestalotiopsis were greater and Acidothermus and Trichoderma were lower in the rhizosphere under infected pines than those under healthy pines and the differences might be caused by B. xylophilus–induced weakening of the health of pines. Our study explored the endophytic and rhizospheric microbial community changes potentially caused by B. xylophilus infection of pines.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Nickle W, Golden A, Mamiya Y, Wergin W (1981) On the taxonomy and morphology of the pine wood nematode, Bursaphelenchus xylophilus (Steiner & Buhrer 1934) Nickle 1970. J Nematol 13:385

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Cheng H, Lin M, Li W, Fang Z (1983) The occurrence of a pine wilting disease caused by a nematode found in Nanjing. For Pest Dis 4:1–5

    Google Scholar 

  3. Mota MM, Braasch H, Bravo MA, Penas AC, Burgermeister W, Metge K, Sousa E (1999) First report of Bursaphelenchus xylophilus in Portugal and in Europe. Nematology 1:727–734

    Google Scholar 

  4. Yi CK, Byun BH, Park JD, Yang S, Chang KH (1989) First finding of the pine wood nematode, Bursaphelenchus xylophilus (Steiner et Buhrer) Nickle and its insect vector in Korea. Research Reports of the Forestry Research Institute (Seoul): 141-149

  5. Zamora P, Rodriguez V, Renedo F, Sanz AV, Dominguez JC, Perez-Escolar G, Miranda J, Alvarez B, Gonzalez-Casas A, Mayor E, Duenas M, Miravalles A, Navas A, Robertson L, Martin AB (2015) First report of Bursaphelenchus xylophilus causing pine wilt disease on Pinus radiata in Spain. Plant Dis 99:1449–1449

    Google Scholar 

  6. Zhao LL, Wei W, Kang L, Sun JH (2007) Chemotaxis of the pinewood nematode, Bursaphelenchus xylophilus, to volatiles associated with host pine, Pinus massoniana, and its vector Monochamus alternatus. J Chem Ecol 33:1207–1216

    CAS  PubMed  Google Scholar 

  7. Ichihara Y, Fukuda K, Suzuki K (2000) Early symptom development and histological changes associated with migration of Bursaphelenchus xylophilus in seedling tissues of Pinus thunbergii. Plant Dis 84:675–680

    CAS  PubMed  Google Scholar 

  8. Shi J, Chen F, Luo YQ, Wang Z, Xie BY, Sturrock RN (2012) First isolation of pine wood nematode from Pinus tabuliformis forests in China. For Pathol 43:59–66

    Google Scholar 

  9. Zhao B, Futai Kazuyoshi, Sutherland J, Takeuchi Yuko (2008) Pine wilt disease. Springer Japan

  10. Guo Q, Guo D, Zhao B, Xu J, Li R (2007) Two cyclic dipeptides from Pseudomonas fluorescens GcM5-1A carried by the pine wood nematode and their toxicities to Japanese black pine suspension cells and seedlings in vitro. J Nematol 39:243–247

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Han Z, Hong Y, Zhao B (2003) A study on pathogenicity of bacteria carried by pine wood nematodes. J Phytopathol 151:683–689

    Google Scholar 

  12. Vicente CSL, Ikuyo Y, Mota M, Hasegawa K (2013) Pinewood nematode-associated bacteria contribute to oxidative stress resistance of Bursaphelenchus xylophilus. BMC Microbiol 13:299

    PubMed  PubMed Central  Google Scholar 

  13. Oku H, Shiraishi T, Ouchi S, Kurozumi S, Ohta H (1980) Pine wilt toxin, the metabolite of a bacterium associated with a nematode. Naturwissenschaften 67:198–199

    CAS  Google Scholar 

  14. Dang QL, Choi GJ, Kim J-C, Cheon H-M, Jang KS, Son SW, Choi YH, Lim CH (2011) Pyochelin isolated from Burkholderia arboris KRICT1 carried by pine wood nematodes exhibits phytotoxicity in pine callus 13:521

  15. Han ZM, Han SF, Wang HL, Zhao BG (2003) Distribution and pathogenicity of bacteria species carried by Bursaphelenchus xylophilus in China. Nematology 5:899–906

    Google Scholar 

  16. Kawazu K, Zhang H, Kanzaki H (1996) Accumulation of benzoic acid in suspension cultured cells of Pinus thunbergii Parl. in response to phenylacetic acid administration. Biosci Biotechnol Biochem 60:1410–1412

    CAS  PubMed  Google Scholar 

  17. Vicente CSL, Nascimento FX, Espada M, Barbosa P, Hasegawa K, Mota M, Oliveira S (2013) Characterization of bacterial communities associated with the pine sawyer beetle Monochamus galloprovincialis, the insect vector of the pinewood nematode Bursaphelenchus xylophilus. FEMS Microbiol Lett 347:130–139

    CAS  PubMed  Google Scholar 

  18. Kwon SJ, Jin HC, Lee S, Nam MH, Chung JH, Kwon SI, Ryu C-M, Park OK (2009) GDSL lipase-like 1 regulates systemic resistance associated with ethylene signaling in Arabidopsis. Plant J 58:235–245

    CAS  PubMed  Google Scholar 

  19. Raffaele S, Leger A, Roby D (2009) Very long chain fatty acid and lipid signaling in the response of plants to pathogens. Plant Signal Behav 4:94–99

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Wang Z, Zhang Y, Wang C, Wang Y, Sung C (2017) Esteya vermicola controls the pinewood nematode, Bursaphelenchus xylophilus, in pine seedlings. J Nematol 49:86–91

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Maehara N (2008) Reduction of Bursaphelenchus xylophilus (Nematoda: Parasitaphelenchidae) population by inoculating Trichoderma spp. into pine wilt-killed trees. Biol Control 44:61–66

    Google Scholar 

  22. Alves M, Pereira A, Vicente C, Matos P, Henriques J, Lopes H, Nascimento F, Mota M, Correia A, Henriques I (2018) The role of bacteria in pine wilt disease: insights from microbiome analysis. FEMS Microbiol Ecol 94:fiy077

    CAS  Google Scholar 

  23. Bal A, Anand R, Berge O, Chanway CP (2012) Isolation and identification of diazotrophic bacteria from internal tissues of Pinus contorta and Thuja plicata. Can J For Res 42:807–813

    CAS  Google Scholar 

  24. Izumi H, Anderson IC, Killham K, Moore ERB (2008) Diversity of predominant endophytic bacteria in European deciduous and coniferous trees. Can J Microbiol 54:173–179

    CAS  PubMed  Google Scholar 

  25. Carper DL, Carrell AA, Kueppers LM, Frank AC (2018) Bacterial endophyte communities in Pinus flexilis are structured by host age, tissue type, and environmental factors. Plant Soil 428:335–352

    CAS  Google Scholar 

  26. Ma Y, Qu Z-L, Liu B, Tan J-J, Asiegbu FO, Sun H (2020) Bacterial community structure of Pinus thunbergii naturally infected by the nematode Bursaphelenchus xylophilus. Microorganisms 8:307

    CAS  PubMed Central  Google Scholar 

  27. Pirttila AM, Laukkanen H, Pospiech H, Myllyla R, Hohtola A (2000) Detection of intracellular bacteria in the buds of Scotch pine (Pinus sylvestris L.) by in situ hybridization. Appl Environ Microbiol 66:3073–3077

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Feng YH, Yang ZQ, Wang J, Luo QF, Li HG (2014) Development and characterization of SSR markers from Pinus massoniana and their transferability to P. elliottii, P. caribaea and P. yunnanensis. Genet Mol Res 13:1508–1513

    CAS  PubMed  Google Scholar 

  29. Guo Y, Lin Q, Chen L, Carballar-Lejarazú R, Zhang A, Shao E, Liang G, Hu X, Wang R, Xu L, Zhang F, Wu S (2020) Characterization of bacterial communities associated with the pinewood nematode insect vector Monochamus alternatus Hope and the host tree Pinus massoniana. BMC Genomics:21

  30. Fu Y-M, Liu H-B, Wu X-Q (2020) Diversity and function of endo-bacteria in Bursaphelenchus xylophilus from Pinus massoniana Lamb. in different regions. Forests:11

  31. Plomion C, Bahrman N, Durel CE, O’Malley DM (1995) Genomic mapping in Pinus pinaster (maritime pine) using RAPD and protein markers. Heredity 74:661–668

    CAS  Google Scholar 

  32. Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963

    PubMed  PubMed Central  Google Scholar 

  33. Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, Mills DA, Caporaso JG (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10:57–59

    CAS  PubMed  Google Scholar 

  34. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, Ciulla D, Tabbaa D, Highlander SK, Sodergren E, Methé B, DeSantis TZ, Consortium THM, Petrosino JF, Knight R, Birren BW (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21:494–504

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998

    CAS  PubMed  Google Scholar 

  37. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2012) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596

    PubMed  PubMed Central  Google Scholar 

  38. Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM, Douglas B, Drenkhan T, Eberhardt U, Dueñas M, Grebenc T, Griffith GW, Hartmann M, Kirk PM, Kohout P, Larsson E, Lindahl BD, Lücking R, Martín MP, Matheny PB, Nguyen NH, Niskanen T, Oja J, Peay KG, Peintner U, Peterson M, Põldmaa K, Saag L, Saar I, Schüßler A, Scott JA, Senés C, Smith ME, Suija A, Taylor DL, Telleria MT, Weiss M, Larsson K-H (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277

    PubMed  Google Scholar 

  39. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Kobayashi DY, Crouch JA (2009) Bacterial/fungal interactions: from pathogens to mutualistic endosymbionts. Annu Rev Phytopathol 47:63–82

    CAS  PubMed  Google Scholar 

  41. Lodewyckx C, Vangronsveld J, Porteous F, Moore ERB, Taghavi S, Mezgeay M, der Lelie D (2002) Endophytic bacteria and their potential applications. Crit Rev Plant Sci 21:583–606

    Google Scholar 

  42. Proença DN, Grass G, Morais PV (2017) Understanding pine wilt disease: roles of the pine endophytic bacteria and of the bacteria carried by the disease-causing pinewood nematode. MicrobiologyOpen 6:e00415

    Google Scholar 

  43. Li L, Tan J, Chen F (2018) Bacillus pumilus strain LYMC-3 shows nematicidal activity against Bursaphelenchus xylophilus via the production of a guanidine compound. Biocontrol Sci Tech 28:1128–1139

    Google Scholar 

  44. Proenca DN, Santo CE, Grass G, Morais PV (2012) Draft genome sequence of Serratia sp. strain M24T3, isolated from pinewood disease nematode Bursaphelenchus xylophilus. J Bacteriol 194:3764–3764

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Prescott CE, Grayston SJ (2013) Tree species influence on microbial communities in litter and soil: current knowledge and research needs. For Ecol Manag 309:19–27

    Google Scholar 

  46. Finkel OM, Burch AY, Lindow SE, Post AF, Belkin S (2011) Geographical location determines the population structure in phyllosphere microbial communities of a salt-excreting desert tree. Appl Environ Microbiol 77:7647–7655

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Coulon F, McKew BA, Osborn AM, McGenity TJ, Timmis KN (2007) Effects of temperature and biostimulation on oil-degrading microbial communities in temperate estuarine waters. Environ Microbiol 9:177–186

    CAS  PubMed  Google Scholar 

  48. Bardgett RD, Lovell RD, Hobbs PJ, Jarvis SC (1999) Seasonal changes in soil microbial communities along a fertility gradient of temperate grasslands. Soil Biol Biochem 31:1021–1030

    CAS  Google Scholar 

  49. Belnap CP, Pan C, Denef VJ, Samatova NF, Hettich RL, Banfield JF (2011) Quantitative proteomic analyses of the response of acidophilic microbial communities to different pH conditions. ISME J 5:1152–1161

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Zhang W, Zhao L, Zhou J, Yu H, Zhang C, Lv Y, Lin Z, Hu S, Zou Z, Sun J (2019) Enhancement of oxidative stress contributes to increased pathogenicity of the invasive pine wood nematode. Philos Trans Royal Soc B Biol Sci 374:20180323

    CAS  Google Scholar 

  51. Wingfield MJ (1987) Fungi associated with the pine wood nematode, Bursaphelenchus Xylophilus, and cerambycid beetles in Wisconsin. Mycologia 79:325–328

    Google Scholar 

  52. Zhang B, Zhang W, Lu M, Ahmad F, Tian H, Ning J, Liu X, Zhao L, Sun J (2017) Chemical signals of vector beetle facilitate the prevalence of a native fungus and the invasive pinewood nematode. J Nematol 49:341–347

    PubMed  PubMed Central  Google Scholar 

  53. Yang Z, Yu Z, Lei L, Xia Z, Shao L, Zhang K, Li G (2012) Nematicidal effect of volatiles produced by Trichoderma sp. J Asia-Pacif Entomol 15:647–650

    CAS  Google Scholar 

  54. Proenca DN, Francisco R, Kublik S, Schoeler A, Vestergaard G, Schloter M, Morais PV (2017) The microbiome of endophytic, wood colonizing bacteria from pine trees as affected by pine wilt disease. Sci Rep 7:4205

    PubMed  PubMed Central  Google Scholar 

  55. Vorholt JA (2012) Microbial life in the phyllosphere. Nat Rev Microbiol 10:828–840

    CAS  PubMed  Google Scholar 

Download references

Funding

This work was funded by the National Key R&D Program of China (2018YFC1200400) and the National Natural Science Foundation of China (NSFC 31901315).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yongxia Li.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, W., Wang, X., Li, Y. et al. Pinewood Nematode Alters the Endophytic and Rhizospheric Microbial Communities of Pinus massoniana. Microb Ecol 81, 807–817 (2021). https://doi.org/10.1007/s00248-020-01619-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-020-01619-1

Keywords

Navigation