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Effects of the Inoculant Strain Pseudomonas sp. SPN31 nah + and of 2-Methylnaphthalene Contamination on the Rhizosphere and Endosphere Bacterial Communities of Halimione portulacoides

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Abstract

The aim of this study is to evaluate the effects of the inoculation of the saltmarsh plant (Halimione portulacoides) with Pseudomonas sp. SPN31 nah+ combined with exposure to 2-methylnaphthalene (2-MtN) on the plant rhizosphere and endosphere bacterial communities as well as on plant health. To achieve this goal, microcosm experiments were set up. Denaturing gradient gel electrophoresis (DGGE) profiles and statistical analysis showed that rhizosphere and endosphere bacterial communities had distinct responses to plant inoculation and/or exposure to 2-MtN. PCR-sequencing analysis of nah genes encoding for 2-MtN degrading enzymes suggested the presence of Pseudomonas sp. SPN31 nah+ in the endosphere of H. portulacoides with 2-MtN contamination. Moreover, a significant effect in the photosynthetic performance of inoculated plants was detected. To conclude, despite the potential beneficial effect of plant inoculation with Pseudomonas sp. SPN31 nah+ endophytic bacteria may have on plant health, no significant effect on the removal of MtN was detected for the level of contamination used in the study.

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References

  1. Afzal M, Yousaf S, Reichenauer TG, Kuffner M, Sessitsch A (2011) Soil type affects plant colonization, activity and catabolic gene expression of inoculated bacterial strains during phytoremediation of diesel. J Hazard Mater 186:1568–1575

    Article  CAS  PubMed  Google Scholar 

  2. Andreolli M, Lampis S, Poli M, Gullner G, Biró B, Vallini G (2013) Endophytic Burkholderia fungorum DBT1 can improve phytoremediation efficiency of polycyclic aromatic hydrocarbons. Chemosphere 92:688–694

    Article  CAS  PubMed  Google Scholar 

  3. Andreote FD, Da Rocha UN, Araújo WL, Azevedo JL, van Overbeek LS (2010) Effect of bacterial inoculation, plant genotype and developmental stage on root-associated and endophytic bacterial communities in potato (Solanum tuberosum). Antonie Van Leeuwenhoek 97:389–399

    Article  PubMed  PubMed Central  Google Scholar 

  4. Anjum NA, Ahmad I, Válega M et al (2013) Salt marsh halophyte services to metal-metalloid remediation: assessment of the processes and underlying mechanisms. Crit Rev Environ Sci Technol 44:2038–2106.

    Article  Google Scholar 

  5. Barac T, Taghavi S, Borremans B et al (2004) Engineered endophytic bacteria improve phytoremediation of water-soluble, volatile, organic pollutants. Nat Biotechnol 22:583–588

    Article  CAS  PubMed  Google Scholar 

  6. Brannock JM (2004) Charaterization of root endophytic bacteria. Doctoral Thesis, University of Cincinnati, pp. 87

  7. Cébron A, Norini MP, Beguiristain T, Leyval C (2008) Real-Time PCR quantification of PAH-ring hydroxylating dioxygenase (PAH-RHDalpha) genes from Gram positive and Gram negative bacteria in soil and sediment samples. J Microbiol Methods 73:148–159

    Article  PubMed  Google Scholar 

  8. Coelho FJ, Sousa S, Santos L, Santos AL, Almeida A, Gomes N, Cunha  (2011) Exploring hydrocarbonoclastic bacterial communities in the estuarine surface microlayer. Aquat Microb Ecol 64:185–195

    Article  Google Scholar 

  9. Couto M, Basto M, Vasconcelos M (2011) Suitability of different salt marsh plants for petroleum hydrocarbons remediation. Chemosphere 84:1052–1057

    Article  CAS  PubMed  Google Scholar 

  10. Dubinsky EA, Conrad ME, Chakraborty R et al (2013) Succession of hydrocarbon-degrading bacteria in the aftermath of the Deepwater Horizon oil spill in the Gulf of Mexico. Environ Sci Technol 47:10860–10867

    Article  CAS  PubMed  Google Scholar 

  11. Escalante-Espinosa E, Gallegos-Martínez M, Favela-Torres E, Gutiérrez-Rojas M (2005) Improvement of the hydrocarbon phytoremediation rate by Cyperus laxus Lam. inoculated with a microbial consortium in a model system. Chemosphere 59:405–413

    Article  CAS  PubMed  Google Scholar 

  12. Fodelianakis S, Antoniou E, Mapelli F et al (2015) Allochthonous bioaugmentation in ex situ treatment of crude oil-polluted sediments in the presence of an effective degrading indigenous microbiome. J Hazard Mater 287:78–86

    Article  CAS  PubMed  Google Scholar 

  13. Gaiero JR, McCall CA, Thompson KA, Day NJ, Best AS, Dunfield KE (2013) Inside the root microbiome: bacterial root endophytes and plant growth promotion. Am J Bot 100:1738–1750

    Article  PubMed  Google Scholar 

  14. Gao Y, Zhu L (2004) Plant uptake, accumulation and translocation of phenanthrene and pyrene in soils. Chemosphere 55:1169–1178

    Article  CAS  PubMed  Google Scholar 

  15. Germaine KJ, Keogh E, Ryan D, Dowling DN (2009) Bacterial endophyte-mediated naphthalene phytoprotection and phytoremediation. FEMS Microbiol Lett 296:226–234

    Article  CAS  PubMed  Google Scholar 

  16. Glick BR (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28:367–374

    Article  CAS  PubMed  Google Scholar 

  17. Gomes NCM, Kosheleva IA, Abraham WR, Smalla K (2005) Effects of the inoculant strain Pseudomonas putida KT2442 (pNF142) and of naphthalene contamination on the soil bacterial community. FEMS Microbiol Ecol 54:21–33

    Article  CAS  PubMed  Google Scholar 

  18. Gomes NCM, Borges LR, Paranhos R, Pinto FN, Mendonca-Hagler LC, Smalla K (2008) Exploring the diversity of bacterial communities in sediments of urban mangrove forests. FEMS Microbiol Ecol 66:96–109

    Article  CAS  Google Scholar 

  19. Gurska J, Wang W, Gerhardt KE et al (2009) Three year field test of a plant growth promoting rhizobacteria enhanced phytoremediation system at a land farm for treatment of hydrocarbon waste. Environ Sci Technol 43:4472–4479

    Article  CAS  PubMed  Google Scholar 

  20. Heuer H, Krsek M, Baker P, Smalla K, Wellington E (1997) Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl Environ Microbiol 63:3233–3241

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Heuer H, Wieland G, Schönfeld J, Schönwälder A, Gomes NCM, Smalla K (2001) Bacterial community profiling using DGGE or TGGE analysis. Environ Mol Microbiol: Protoc Appl 9:177–190

    Google Scholar 

  22. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. California Agric Exp Stn Circ 347

  23. Jones RK, Sun WH, Tang C-S, Robert FM (2004) Phytoremediation of petroleum hydrocarbons in tropical coastal soils II. microbial response to plant roots and contaminant. Environ Sci Pollut R 11:340–346

    Article  CAS  Google Scholar 

  24. Leahy JG, Colwell RR (1990) Microbial degradation of hydrocarbons in the environment. Microbiol Res 54:305–315

    CAS  Google Scholar 

  25. Lin Q, Shen KL, Zhao HM, Li WH (2008) Growth response of Zea mays L. in pyrene–copper co-contaminated soil and the fate of pollutants. J Hazard Mater 150:515–521

    Article  CAS  PubMed  Google Scholar 

  26. Ma Y, Wang L, Shao Z (2006) Pseudomonas, the dominant polycyclic aromatic hydrocarbon-degrading bacteria isolated from Antarctic soils and the role of large plasmids in horizontal gene transfer. Environ Microbiol 8:455–465

    Article  CAS  PubMed  Google Scholar 

  27. Maldonado-González MM, Prieto P, Mercado-Blanco J (2015) Endophytic colonization and biocontrol performance of Pseudomonas fluorescens PICF7 in olive (Olea europaea L.) are determined neither by pyoverdine production nor swimming motility. Environ Microbiol 17:3139–3153

    Article  PubMed  Google Scholar 

  28. Mansur AA, Adetutu EM, Makadia T, Morrison PD, Ball AS (2015) Assessment of the hydrocarbon degrading abilities of three Bioaugmentation agents for the bioremediation of crude oil tank bottom sludge Contaminated Libyan soil. Int J Environ Bioremed Biodegradation 3:1–9

    Article  Google Scholar 

  29. Nedbal L, Trtìlek M, Herppich W (2000) Methods and equipment for fluorescence imaging on plant material. Bornimer Agrartechn Ber 25:127–135

    Google Scholar 

  30. Nie M, Wang Y, Yu J et al (2011) Understanding plant-microbe interactions for phytoremediation of petroleum-polluted soil. PloS One 6:e17961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Oksanen J, Blanchet FG, Kindt R et al (2011) vegan: Community Ecology Package. R package version 2.0–0

  32. Oliveira V, Gomes NCM, Cleary DF et al (2014) Halophyte plant colonization as a driver of the composition of bacterial communities in salt marshes chronically exposed to oil hydrocarbons. FEMS Microbiol Ecol 90:647–662

    Article  CAS  PubMed  Google Scholar 

  33. Oliveira V, Gomes NCM, Almeida A, Silva A, Simões MM, Smalla K, Cunha  (2014) Hydrocarbon contamination and plant species determine the phylogenetic and functional diversity of endophytic degrading bacteria. Mol Ecol 23:1392–1404

    Article  CAS  PubMed  Google Scholar 

  34. Pacwa-Płociniczak M, Płaza GA, Poliwoda A, Piotrowska-Seget Z (2014) Characterization of hydrocarbon-degrading and biosurfactant-producing Pseudomonas sp. P-1 strain as a potential tool for bioremediation of petroleum-contaminated soil. Environ Sci Pollt R 21:9385–9395

    Article  Google Scholar 

  35. Paliwal V, Raju SC, Modak A, Phale PS, Purohit HJ (2014) Pseudomonas putida CSV86: A candidate genome for genetic bioaugmentation. PloS One 9:e84000

    Article  PubMed  PubMed Central  Google Scholar 

  36. Park JW, Crowley DE (2006) Dynamic changes in nahAc gene copy numbers during degradation of naphthalene in PAH-contaminated soils. Appl Microbiol Biotechnol 72:1322–1329

    Article  CAS  PubMed  Google Scholar 

  37. Phillips LA, Greer CW, Germida JJ (2006) Culture-based and culture-independent assessment of the impact of mixed and single plant treatments on rhizosphere microbial communities in hydrocarbon contaminated flare-pit soil. Soil Biol Biochem 38:2823–2833

    Article  CAS  Google Scholar 

  38. Phillips LA, Germida JJ, Farrell RE, Greer CW (2008) Hydrocarbon degradation potential and activity of endophytic bacteria associated with prairie plants. Soil Biol Biochem 40:3054–3064

    Article  CAS  Google Scholar 

  39. Ponsin V, Coulomb B, Guelorget Y, Maier J, Höhener P (2014) In situ biostimulation of petroleum hydrocarbon degradation by nitrate and phosphate injection using a dipole well configuration. J Contam Hydrol 171:22–31

    Article  CAS  PubMed  Google Scholar 

  40. Rikalovic MG, Abdel-Mawgoud AM, Déziel E, Gojgic-Cvijovic GD, Nestorovic Z, Vrvic MM, Karadzic IM (2013) Comparative analysis of Rhamnolipids from novel environmental isolates of Pseudomonas aeruginosa. J Surfactants Deterg 16:673–682

    Article  CAS  Google Scholar 

  41. Silva I, Rocha SM, Coimbra MA, Marriott PJ (2010) Headspace solid-phase microextraction combined with comprehensive two-dimensional gas chromatography time-of-flight mass spectrometry for the determination of volatile compounds from marine salt. J Chromatogr A 1217:5511–5521

    Article  CAS  PubMed  Google Scholar 

  42. Singer AC, Crowley DE, Thompson IP (2003) Secondary plant metabolites in phytoremediation and biotransformation. Trends Biotechnol 21:123–130

    Article  CAS  PubMed  Google Scholar 

  43. Sun T-R, Cang L, Wang Q-Y, Zhou D-M, Cheng J-M, Xu H (2010) Roles of abiotic losses, microbes, plant roots, and root exudates on phytoremediation of PAHs in a barren soil. J Hazard Mater 176:919–925

    Article  CAS  PubMed  Google Scholar 

  44. Taghavi S, Barac T, Greenberg B, Borremans B, Vangronsveld J, van der Lelie D (2005) Horizontal gene transfer to endogenous endophytic bacteria from poplar improves phytoremediation of toluene. Appl Environ Microbiol 71:8500–8505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Top EM, Springael D (2003) The role of mobile genetic elements in bacterial adaptation to xenobiotic organic compounds. Curr Opin Biotechnol 14:262–269

    Article  CAS  PubMed  Google Scholar 

  46. Top EM, Springael D, Boon N (2002) Catabolic mobile genetic elements and their potential use in bioaugmentation of polluted soils and waters. FEMS Microbiol Ecol 42:199–208

    Article  CAS  PubMed  Google Scholar 

  47. Wasi S, Tabrez S, Ahmad M (2013) Use of Pseudomonas spp. for the bioremediation of environmental pollutants: a review. Environ Monit Assess 185:8147–8155

    Article  PubMed  Google Scholar 

  48. Wilson MS, Bakermans C, Madsen EL (1999) In situ, real-time catabolic gene expression: extraction and characterization of naphthalene dioxygenase mRNA transcripts from groundwater. Appl Environ Microbiol 65:80–87

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Yousaf S, Andria V, Reichenauer TG, Smalla K, Sessitsch A (2010) Phylogenetic and functional diversity of alkane degrading bacteria associated with Italian ryegrass (Lolium multiflorum) and Birdsfoot trefoil (Lotus corniculatus) in a petroleum oil-contaminated environment. J Hazard Mater 184:523–532

    Article  CAS  PubMed  Google Scholar 

  50. Yousaf S, Afzal M, Reichenauer TG, Brady CL, Sessitsch A (2011) Hydrocarbon degradation, plant colonization and gene expression of alkane degradation genes by endophytic Enterobacter ludwigii strains. Environ Pollut 159:2675–2683

    Article  CAS  PubMed  Google Scholar 

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Funding

The funding was provided by Fundação para a Ciência e a Tecnologia, Fundação para a Ciência e Tecnologia—FCT and Programa Operacional Factores de Competitividade.

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Correspondence to Ângela Cunha.

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Oliveira, V., Gomes, N.C.M., Santos, M. et al. Effects of the Inoculant Strain Pseudomonas sp. SPN31 nah + and of 2-Methylnaphthalene Contamination on the Rhizosphere and Endosphere Bacterial Communities of Halimione portulacoides . Curr Microbiol 74, 575–583 (2017). https://doi.org/10.1007/s00284-017-1197-y

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