Abstract
Colonization by polycyclic aromatic hydrocarbon (PAH)-degrading endophytic bacteria (PAHDEB) can reduce the PAH contamination risk in plant. However, little information is available on the impact of PAHDEB colonization on the endophytic bacterial community of inner plant tissues. A phenanthrene-degrading endophytic bacterium (PDEB), Massilia sp. Pn2, was inoculated onto the roots of wheat and subjected to greenhouse container experiments. The endophytic bacterial community structure in wheat was investigated using high-throughput sequencing technology. The majority of endophytic bacteria in wheat were Proteobacteria, and the dominant genus was Pseudomonas. Phenanthrene contamination clearly increased the diversity of endophytic bacteria in wheat. The cultivable endophytic bacteria counts in wheat decreased with increasing the level of phenanthrene contamination; the endophytic bacterial community structure changed correspondingly, and the bacterial richness first increased and then decreased. Inoculation of strain Pn2 reduced the phenanthrene contamination in wheat, enlarged the biomass of wheat roots, changed the bacterial community structure and enhanced the cell counts, diversity and richness of endophytic bacteria in phenanthrene-contaminated wheat in a contamination level-dependent manner. The findings of this investigation provide insight into the responses of endophytic bacterial community in plant to external PAH contamination and PAHDEB colonization.
Similar content being viewed by others
References
Afzal M, Khan QM, Sessitsch A (2014) Endophytic bacteria: prospects and applications for the phytoremediation of organic pollutants. Chemosphere 117:232–242
Ahmed AS, Sánchez CP, Candela ME (2000) Evaluation of induction of systemic resistance in pepper plants (Capsicum annuum) to Phytophthora capsici using Trichoderma harzianum and its relation with capsidiol accumulation. Eur J Plant Pathol 106:817–824
Amato KR, Yeoman CJ, Kent A, Righini N, Carbonero F, Estrada A, Gaskins HR, Stumpf RM, Yildirim S, Torralba M, Gillis M, Wilson BA, Nelson KE, White BA, Leigh SR (2013) Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. The ISME J 7:1344–1353
Araújo WL, Marcon J, Maccheroni W, Elsas JD, Vuurde JW, Azevedo JL (2002) Diversity of endophytic bacterial populations and their interaction with Xylella fastidiosa in citrus plants. Appl Environ Microbiol l68:4906–4914
Campbell BJ, Polson SW, Hanson TE, Mack MC, Schuur EA (2010) The effect of nutrient deposition on bacterial communities in Arctic tundra soil. Environ Microbiol 12:1842–1854
Cheema SA, Khana MI, Shen C, Tang X, Farooq M, Chen L, Zhang C, Chen Y (2010) Degradation of phenanthrene and pyrene in spiked soils by single and combined plants cultivation. J Hazard Mater 177:384–389
Chelius MK, Triplett EW (2001) The diversity of Archaea and Bacteria in association with the roots of Zea mays L. Microb Ecol 41:252–263
Chen H, Boutros PC (2011) VennDiagram: a package for the generation of highly-customizable Venn and Euler diagrams in R. BMC Bioinformatics 12(1):35
Collins CD, Fryer M, Grosso A (2006) Plant uptake of non-ionic organic chemicals. Environ Sci Technol 40:45–52
Compant S, Clement C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461
Gao YZ, Zhu LZ (2004) Plant uptake, accumulation and translocation of phenanthrene and pyrene in soils. Chemosphere 55:1169–1178
Gao YZ, Zhang Y, Liu J, Kong HL (2013) Metabolism and subcellular distribution of anthracene in tall fescue (Festuca arundinacea Schreb.) Plant Soil 365:171–182
Gao YZ, Hu XJ, Zhou ZY, Zhang W, Wang YZ, Sun BQ (2017) Phytoavailability and mechanism of bound PAH residues in filed contaminated soils. Environ Pollut. doi:10.1016/j.envpol.2016.11.076
Garbeva P, Overbeek VL, Vuurde VJ, Elsas VJ (2001) Analysis of endophytic bacterial communities of potato by plating and denaturing gradient gel electrophoresis (DGGE) of 16S rDNA based PCR fragments. Microb Ecol 41:369–383
Gardner JM, Feldman AW, Zablotowicz M (1982) Identity and behavior of xylem-residing bacteria in rough lemon roots of Florida citrus trees. Appl Environ Microbiol 43:1335–1342
Germaine KJ, Keogh E, Ryan D, Dowling DN (2009) Bacterial endophyte-mediated naphthalene phytoprotection and phytoremediation. FEMS Microbiol Lett 296:226–234
Glick BR (2003) Phytoremediation: synergistic use of plants and bacteria to clean up the environment. Biotechnol Adv 21:383–393
Gotelli NJ, Colwell RK (2011) Estimating species richness. In: Magurran AE, McGill BJ (eds) Biological diversity: frontiers in measurement and assessment. Oxford University Press, Oxford, pp 39–54
Hallmann J, Quadt-Hallmann A, Mahafee WF, Kloepper JW (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43:895–914
Harish S, Kavino M, Kumar N, Saravanakumar D, Soorianathasundaram K, Samiyappan R (2008) Biohardening with plant growth promoting rhizosphere and endophytic bacteria induces systemic resistance against banana bunchy top virus. Appl Soil Ecol 39:187–200
Ho YN, Shih CH, Hsiao SC, Huang CC (2009) A novel endophytic bacterium, Achromobacter xylosoxidans, helps plants against pollutant stress and improves phytoremediation. J Biosci Bioeng 108:S75–S95
Hung PQ, Annapurna K (2004) Isolation and characterization of endophytic bacteria in soybean (Glycine sp.) Omonrice 12:92–101
Huse SM, Dethlefsen L, Huber JA, Mark WD, Relman DA, Sogin ML (2008) Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet 4:e1000255
Hwang S, Cutright TJ (2002) Biodegradability of aged pyrene and phenanthrene in a natural soil. Chemosphere 47:891–899
Johnsen AR, Wick LY, Harms H (2005) Principles of microbial PAH-degradation in soil. Environ Pollut 133:71–84
Khan Z, Doty S (2011) Endophyte-assisted phytoremediation. Curr Top Plant Biol 12:97–105
Khan Z, Roman D, Kintz T, delas Alas M, Yap R, Doty S (2014) Degradation, phytoprotection and phytoremediation of phenanthrene by endophyte Pseudomonas putida, PD1. Environ Sci Technol 48:12221–12228
Kim KH, Jahan SA, Kabir E, Brown RJ (2013) A review of airborne polycyclic aromatic hydrocarbons (PAHs) and their human health effects. Environ Inter 60:71–80
Liengme BV (2015) Guide to Microsoft Excel 2013 for scientists and engineers. Academic Press, London
Liu J, Liu S, Sun K, Sheng YH, Gu YJ, Gao YZ (2014) Colonization on root surface by a phenanthrene-degrading endophytic bacterium and its application for reducing plant phenanthrene contamination. PLoS One 9:e108249
Lodewyckx C, Vangronsveld J, Porteous F, Moore ER, Taghavi S, Mezgeay M, der Lelie DV (2002) Endophytic bacteria and their potential applications. Crit Rev Plant Sci 21:583–606
Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R (2011) UniFrac: an effective distance metric for microbial community comparison. ISME J 5:169
Ministry of Environmental Protection and Ministry of Land and Resource of the People’s Republic of China (MEP and MLR) (2014) The bulletin of nationwide soil pollution status survey April 14. Index No. 000014672/2014–00351
Moore FP, Barac T, Borremans B, Oeyen L, Vangronsveld J, van der Lelie D, Campbell CD, Moore ER (2006) Endophytic bacterial diversity in poplar trees growing on a BTEX-contaminated site: the characterisation of isolates with potential to enhance phytoremediation. Syst Appl Microbiol 29:539–556
Morrissey JP, Dow JM, Mark GL (2004) Are microbes at the root of a solution to world food production? EMBO Rep 5:922–926
Oliveira V, Gomes N, 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
Peng A, Liu J, Gao YZ, Chen ZY (2013) Distribution of endophytic bacteria in Alopecurus aequalis Sobol and Oxalis corniculata L. from soils contaminated by polycyclic aromatic hydrocarbons. PLoS One 8:e83054
Phillips LA, Germida JJ, Farrell RE (2008) Hydrocarbon degradation potential and activity of endophytic bacteria associated with prairie plants. Soil Biol Biochem 40:3054–3064
Qing W, Zhao X, Zhao SY (2006) Application of PCR-DGGE in research of bacterial diversity in drinking water. Biomed Environ Sci 19:371–374
R Development Core Team (2013) R: a language and environment for statistical computing. Available on line at: http://www.r-project.org/
Rajkumar M, Ae N, Freitas H (2009) Endophytic bacteria and their potential to enhance heavy metal phytoextraction. Chemosphere 77:153–160
Reysenbach A, Pace N (1995) Reliable amplification of hyperthermophilic archaeal 16S rRNA genes by the polymerase chain reaction. In: Robb F (ed) Archaea: a laboratory manual. Cold Spring Harbor Laboratory Press, New York, pp p101–p107
Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Sahl JW (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541
Sheng XF, Gong JX (2006) Increased degradation of phenanthrene in soil by Pseudomonas sp. GF3 in the presence of wheat. Soil Biol Biochem 38:2587–2592
Siciliano SD, Fortin N, Mihoc A, Wisse G, Labelle S, Beaumier D, Schwab P (2001) Selection of specific endophytic bacterial genotypes by plants in response to soil contamination. Appl Environ Microbiol 67:2469–2475
Sobral JK, Araujo WL, Mendes R, Kleiner AAP, Joao LA (2005) Isolation and characterization of endophytic bacteria from soybean (Glycine max) grown in soil treated with glyphosate herbicide. Plant Soil 273:91–99
Spellerberg IF (2008) Shannon–Wiener index. Lincoln University Press, Lincoln, pp 3249–3252
Sun L, Qiu F, Zhang X, Dai X, Dong X, Song W (2008) Endophytic bacterial diversity in rice (Oryza sativa L.) roots estimated by 16S rDNA sequence analysis. Microb Ecol 55:415–424
Sun K, Liu J, Jin L, Gao YZ (2014) Utilizing pyrene-degrading endophytic bacteria to reduce the risk of plant pyrene contamination. Plant Soil 374:251–262
Tanprasert P, Reed BM (1997) Detection and identification of bacterial contaminants from strawberry runner explants. In Vitro Cell Dev Biol 33:221–226
Weyens N, van der Lelie D, Taghavi S, Newman L, Vangronsveld J (2009a) Exploiting plant-microbe partnerships to improve biomass production and remediation. Trends Biotechnol 27:591–598
Weyens N, van der Lelie D, Taghavi S, Vangronsveld J (2009b) Phytoremediation: plant-endophyte partnerships take the challenge. Curr Opin Biotechnol 20:248–254
Xie WY, Su JQ, Zhu YG (2015) Phyllosphere bacterial community of floating macrophytes in paddy soil environments as revealed by Illumina high-throughput sequencing. Appl Environ Microbiol 81:522–532
Yaws CL (1999) Chemical properties handbook. McGraw-Hill, New York
Acknowledgements
This work was supported by the Major State Basic Research Development Program of China (973 Program, 2015CB150505), the Fundamental Research Funds for the Central Universities (KYZ201516), the Natural Science Foundation of Jiangsu Province (BK20161454), the Special Fund for Agro-Scientific Research in Public Interest, China (201503107) and a project funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethical statement
This article does not contain any studies with human participants or animals performed by any of the authors.
Conflict of interest
The authors declared that they have no conflict of interest.
Additional information
Juan Liu and Yanbing Xiang contribute equality to this paper.
Electronic supplementary material
ESM 1
(PDF 420 kb)
Rights and permissions
About this article
Cite this article
Liu, J., Xiang, Y., Zhang, Z. et al. Inoculation of a phenanthrene-degrading endophytic bacterium reduces the phenanthrene level and alters the bacterial community structure in wheat. Appl Microbiol Biotechnol 101, 5199–5212 (2017). https://doi.org/10.1007/s00253-017-8247-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-017-8247-z