Mapping the centimeter-scale spatial variability of PAHs and microbial populations in the rhizosphere of two plants

PLoS ONE

Volumn 10, Issue 11, 2015, Pages

  Bourceret, Amélia ^a,b   Leyval, Corinne ^a,b   De Fouquet, Chantal ^c   Cébron, Aurélie ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ DE LORRAINE   (France)

^c CENTRE DE GÉOSCIENCES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE; POLYCYCLIC AROMATIC HYDROCARBON; SOIL; SOIL POLLUTANT;

ALFALFA; ARTICLE; BACTERIUM; BIOMASS; BIOREMEDIATION; CONTROLLED STUDY; FUNGUS; GRAM POSITIVE BACTERIUM; INCUBATION TIME; KRIGING; LOLIUM; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; MICROBIAL DEGRADATION; MICROORGANISM; NONHUMAN; PLANT EXUDATION; PLANT GROWTH; POPULATION ABUNDANCE; RHIZOSPHERE; ROOT DEVELOPMENT; RYEGRASS; SOIL ACIDITY; SOIL POLLUTION; ANALYSIS; CHEMISTRY; METABOLISM; MICROBIOLOGY; PLANT ROOT; PRINCIPAL COMPONENT ANALYSIS; SOIL; SOIL POLLUTANT;

BACTERIA; CARBOHYDRATES; FUNGI; LOLIUM; MEDICAGO SATIVA; PLANT ROOTS; POLYCYCLIC AROMATIC HYDROCARBONS; PRINCIPAL COMPONENT ANALYSIS; RHIZOSPHERE; SOIL; SOIL POLLUTANTS;

EID: 84958012353     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0142851     Document Type: Article

References (72)

1. Villanneau E, Saby NA, Orton T, Jolivet C, Boulonne L, Caria G, et al. First evidence of large-scale PAH trends in French soils. Environ Chem Lett. 2013; 11: 99-104. doi: 10.1007/s10311-013-0401-y
2. De Fouquet C. From exploratory data analysis to geostatistical estimation: examples from the analysis of soil pollutants. Eur J Soil Sci. 2011; 62: 454-466.
3. Hybholt TK, Aamand J, Johnsen AR. Quantification of centimeter-scale spatial variation in PAH, glucose and benzoic acid mineralization and soil organic matter in road-side soil. Adapt For Ecosyst Air Pollut Clim Change. 2011; 159: 1085-1091. doi: 10.1016/j.envpol.2011.02.028
4. Amellal N, Portal J-M, Vogel T, Berthelin J. Distribution and location of polycyclic aromatic hydrocarbons (PAHs) and PAH-degrading bacteria within polluted soil aggregates. Biodegradation. 2001; 12: 49-57. doi: 10.1023/A:1011909107858 PMID: 11693295
5. Cornelissen G, Gustafsson Ö, Bucheli TD, Jonker MTO, Koelmans AA, van Noort PCM. Extensive Sorption of Organic Compounds to Black Carbon, Coal, and Kerogen in Sediments and Soils: Mechanisms and Consequences for Distribution, Bioaccumulation, and Biodegradation. Environ Sci Technol. 2005; 39: 6881-6895. doi: 10.1021/es050191b PMID: 16201609
6. Choudhary VR, Mantri K. Adsorption of Aromatic Hydrocarbons on Highly Siliceous MCM-41. Langmuir. 2000; 16: 7031-7037. doi: 10.1021/la991714u
7. Styrishave B, Björklund E, Johnsen A, Halling-Sørensen B. The Spatial Heterogeneity of Polycyclic Aromatic Hydrocarbons in Soil Depends on Their Physico-chemical Properties. Water Air Soil Pollut. 2012; 223: 969-977. doi: 10.1007/s11270-011-0916-4
8. Tunega D, Gerzabek MH, Haberhauer G, Totsche KU, Lischka H. Model study on sorption of polycyclic aromatic hydrocarbons to goethite. J Colloid Interface Sci. 2009; 330: 244-249. doi: 10.1016/j.jcis. 2008.10.056 PMID: 18996540
9. Kumar R, Pandey S, Pandey A. Plant roots and carbon sequestration. Curr Sci. 2006; 91: 885-890.
10. Vančura V, Hovadik A. Root exudates of plants: II. Composition of root exudates of some vegetables. Plant Soil. 1965; 21-32.
11. Chaudhry Q, Blom-Zandstra M, Gupta SK, Joner E. Utilising the Synergy between Plants and Rhizosphere Microorganisms to Enhance Breakdown of Organic Pollutants in the Environment (15 pp). Environ Sci Pollut Res. 2005; 12: 34-48. doi: 10.1065/espr2004.08.213
12. Joner EJ, Corgié SC, Amellal N, Leyval C. Nutritional constraints to degradation of polycyclic aromatic hydrocarbons in a simulated rhizosphere. Soil Biol Biochem. 2002; 34: 859-864. doi: 10.1016/S0038-0717(02)00018-4
13. Joner EJ, Leyval C. Rhizosphere gradients of polycyclic aromatic hydrocarbon (PAH) dissipation in two industrial soils and the impact of arbuscular mycorrhiza. Environ Sci Technol. 2003; 37: 2371-2375. PMID: 12831019
14. Sun B, Ling W, Wang Y. Can root exudate components influence the availability of pyrene in soil? J Soils Sediments. 2013; 13: 1161-1169. doi: 10.1007/s11368-013-0712-4
15. Kuiper I, Lagendijk EL, Bloemberg GV, Lugtenberg BJ. Rhizoremediation: a beneficial plant-microbe interaction. Mol Plant Microbe Interact. 2004; 17: 6-15. PMID: 14714863
16. Gerhardt KE, Huang X-D, Glick BR, Greenberg BM. Phytoremediation and rhizoremediation of organic soil contaminants: Potential and challenges. Plant Sci. 2009; 176: 20-30. doi: 10.1016/j.plantsci.2008. 09.014
17. Cébron A, Louvel B, Faure P, France-Lanord C, Chen Y, Murrell JC, et al. Root exudates modify bacterial diversity of phenanthrene degraders in PAH-polluted soil but not phenanthrene degradation rates. Environ Microbiol. 2011; 13: 722-736. doi: 10.1111/j.1462-2920.2010.02376.x PMID: 21087382
18. Storey S, Ashaari MM, McCabe G, Harty M, Dempsey R, Doyle O, et al. Microbial community structure during fluoranthene degradation in the presence of plants. J Appl Microbiol. 2014; 117: 74-84. doi: 10.1111/jam.12518 PMID: 24712542
19. Liste H-H, Alexander M. Plant-promoted pyrene degradation in soil. Chemosphere. 2000; 40: 7-10. doi: 10.1016/S0045-6535(99)00216-7 PMID: 10665438
20. Binet P, Portal JM, Leyval C. Application of GC-MS to the study of anthracene disappearance in the rhizosphere of ryegrass. Org Geochem. 2001; 32: 217-222. doi: 10.1016/S0146-6380(00)00168-6
21. Chiapusio G, Pujol S, Toussaint ML, Badot PM, Binet P. Phenanthrene toxicity and dissipation in rhizosphere of grassland plants (Lolium perenne L. and Trifolium pratense L.) in three spiked soils. Plant Soil. 2007; 294: 103-112. doi: 10.1007/s11104-007-9234-4
22. Tejeda-Agredano MC, Gallego S, Vila J, Grifoll M, Ortega-Calvo JJ, Cantos M. Influence of the sunflower rhizosphere on the biodegradation of PAHs in soil. Soil Biol Biochem. 2013; 57: 830-840. doi: 10.1016/j.soilbio.2012.08.008
23. Louvel B, Cébron A, Leyval C. Root exudates affect phenanthrene biodegradation, bacterial community and functional gene expression in sand microcosms. Int Biodeterior Biodegrad. 2011; 65: 947-953. doi: 10.1016/j.ibiod.2011.07.003
24. Liste H-H, Prutz I. Plant performance, dioxygenase-expressing rhizosphere bacteria, and biodegradation of weathered hydrocarbons in contaminated soil. Chemosphere. 2006; 62: 1411-1420. doi: 10.1016/j.chemosphere.2005.05.018 PMID: 15996713
25. Hinsinger P, Gobran GR, Gregory PJ, Wenzel WW. Rhizosphere geometry and heterogeneity arising from root-mediated physical and chemical processes. New Phytol. 2005; 168: 293-303. doi: 10.1111/j. 1469-8137.2005.01512.x PMID: 16219069
26. Shann JR, Boyle J. Influence of plant species on in situ rhizosphere degradation. 1994;
27. Marschner P, Yang C-H, Lieberei R, Crowley D. Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biol Biochem. 2001; 33: 1437-1445. doi: 10.1016/S0038-0717(01) 00052-9
28. Anderson TA, Guthrie EA, Walton BT. Bioremediation. EST. 1993; 27: 2631-2636.
29. D'Orazio V, Ghanem A, Senesi N. Phytoremediation of pyrene contaminated soils by different plant species. CLEAN-Soil Air Water. 2013; 41: 377-382.
30. Phillips LA, Germida JJ, Farrell RE, Greer CW. Hydrocarbon degradation potential and activity of endophytic bacteria associated with prairie plants. Soil Biol Biochem. 2008; 40: 3054-3064.
31. Corgié SC, Joner EJ, Leyval C. Rhizospheric degradation of phenanthrene is a function of proximity to roots. Plant Soil. 2003; 257: 143-150. doi: 10.1023/A:1026278424871
32. Corgié S, Beguiristain T, Leyval C. Spatial distribution of bacterial communities and phenanthrene degradation in the rhizosphere of Lolium perenne L. Appl Environ Microbiol. 2004; 70: 3552-3557. PMID: 15184156
33. Ma B, Wang J, Xu M, He Y, Wang H, Wu L, et al. Evaluation of dissipation gradients of polycyclic aromatic hydrocarbons in rice rhizosphere utilizing a sequential extraction procedure. Environ Pollut. 2012; 162: 413-421. doi: 10.1016/j.envpol.2011.10.034 PMID: 22243893
34. Ling W, Dang H, Liu J. In situ gradient distribution of polycyclic aromatic hydrocarbons (PAHs) in contaminated rhizosphere soil: a field study. J Soils Sediments. 2013; 13: 677-685.
35. Hafner S, Wiesenberg GB, Stolnikova E, Merz K, Kuzyakov Y. Spatial distribution and turnover of rootderived carbon in alfalfa rhizosphere depending on top- and subsoil properties and mycorrhization. Plant Soil. 2014; 380: 101-115. doi: 10.1007/s11104-014-2059-z
36. Demougeot-Renard H, de Fouquet C, Renard P. Forecasting the number of soil samples required to reduce remediation cost uncertainty. J Environ Qual. 2004; 33: 1694-1702. PMID: 15356229
37. Demougeot-Renard H, De Fouquet C. Geostatistical approach for assessing soil volumes requiring remediation: Validation using lead-polluted soils underlying a former smelting works. Environ Sci Technol. 2004; 38: 5120-5126. PMID: 15506207
38. De Fouquet C, Benoit Y, Carpentier C, Fricaudet B. Uncertainties on the Extension of a Polluted Zone. American Society of Mechanical Engineers; 2011. pp. 1307-1312.
39. Faucheux C, Lefebvre E, De Fouquet C, Benoit Y, Fricaudet B, Carpentier C, et al. Characterisation of a hydrocarbon polluted soil by an intensive multi-scale sampling. 2008. pp. 961-970.
40. De Fouquet C, Benoit Y, Carpentier C, Faucheux C, Fricaudet B. On site survey of organic pollutions: some results of the LOQUAS project. Proceedings Consoil, Salzburg; 2010.
41. Bengtsson G, Törneman N. A spatial approach to environmental risk assessment of PAH contamination. Risk Anal. 2009; 29: 48-61. doi: 10.1111/j.1539-6924.2008.01128.x PMID: 18808392
42. Bengtsson G, Törneman N, Yang X. Spatial uncoupling of biodegradation, soil respiration, and PAH concentration in a creosote contaminated soil. Environ Pollut. 2010; 158: 2865-2871. doi: 10.1016/j. envpol.2010.06.010 PMID: 20630638
43. Bengtsson G, Törneman N, Lipthay J, Sørensen S. Microbial Diversity and PAH Catabolic Genes Tracking Spatial Heterogeneity of PAH Concentrations. Microb Ecol. 2013; 65: 91-100. doi: 10.1007/s00248-012-0112-0 PMID: 22940734
44. Johnsen AR, Styrishave B, Aamand J. Quantification of small-scale variation in the size and composition of phenanthrene-degrader populations and PAH contaminants in traffic-impacted topsoil. FEMS Microbiol Ecol. 2014; 88: 84-93. doi: 10.1111/1574-6941.12272 PMID: 24344982
45. Törneman N, Yang X, Bååth E, Bengtsson G. Spatial covariation of microbial community composition and polycyclic aromatic hydrocarbon concentration in a creosote-polluted soil. Environ Toxicol Chem. 2008; 27: 1039-1046. doi: 10.1897/07-440.1 PMID: 18419193
46. Mukherjee S, Juottonen H, Siivonen P, Lloret Quesada C, Tuomi P, Pulkkinen P, et al. Spatial patterns of microbial diversity and activity in an aged creosote-contaminated site. ISME J. 2014; 8: 2131-2142. doi: 10.1038/ismej.2014.151 PMID: 25105905
47. Ouvrard S, Barnier C, Bauda P, Beguiristain T, Biache C, Bonnard M, et al. In Situ Assessment of Phytotechnologies for Multicontaminated Soil Management. Int J Phytoremediation. 2011; 13: 245-263. doi: 10.1080/15226514.2011.568546 PMID: 22046763
48. Cébron A, Faure P, Lorgeoux C, Ouvrard S, Leyval C. Experimental increase in availability of a PAH complex organic contamination from an aged contaminated soil: Consequences on biodegradation. Environ Pollut. 2013; 177: 98-105. doi: 10.1016/j.envpol.2013.01.043 PMID: 23500046
49. Reid BJ, Stokes JD, Jones KC, Semple KT. Nonexhaustive cyclodextrin-based extraction technique for the evaluation of PAH bioavailability. Environ Sci Technol. 2000; 34: 3174-3179.
50. Keith LH, Telliard WA. Priority pollutants I-a perspective view. Environ Sci Technol. 1979; 13: 416-423.
51. α) genes from Gram positive and Gram negative bacteria in soil and sediment samples. J Microbiol Methods. 2008; 73: 148-159. doi: 10.1016/j.mimet.2008.01.009 PMID: 18329116
52. Thion C, Cébron A, Beguiristain T, Leyval C. Long-term in situ dynamics of the fungal communities in a multi-contaminated soil are mainly driven by plants. FEMS Microbiol Ecol. 2012; 82: 169-181. doi: 10.1111/j.1574-6941.2012.01414.x PMID: 22587649
53. Lueders T, Wagner B, Claus P, Friedrich MW. Stable isotope probing of rRNA and DNA reveals a dynamic methylotroph community and trophic interactions with fungi and protozoa in oxic rice field soil. Environ Microbiol. 2004; 6: 60-72. doi: 10.1046/j.1462-2920.2003.00535.x PMID: 14686942
54. Felske A, Akkermans ADL, De Vos WM. Quantification of 16S rRNAs in Complex Bacterial Communities by Multiple Competitive Reverse Transcription-PCR in Temperature Gradient Gel Electrophoresis Fingerprints. Appl Environ Microbiol. 1998; 64: 4581-4587. PMID: 9797325
55. Chilès J-P, Delfiner P. Geostatistics: Modeling spatial uncertainty. 2nd edition. 2nd edition. Wiley; 2012.
56. Hinsinger P, Plassard C, Tang C, Jaillard B. Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: A review. Plant Soil. 2003; 248: 43-59. doi: 10.1023/A:1022371130939
57. Rousk J, Baath E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, et al. Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J. 2010; 4: 1340-1351. doi: 10.1038/ismej. 2010.58 PMID: 20445636
58. Walker TS, Bais HP, Grotewold E, Vivanco JM. Root exudation and rhizosphere biology. Plant Physiol. 2003; 132: 44-51. PMID: 12746510
59. Yang C-H, Crowley DE. Rhizosphere Microbial Community Structure in Relation to Root Location and Plant Iron Nutritional Status. Appl Environ Microbiol. 2000; 66: 345-351. doi: 10.1128/AEM.66.1.345-351.2000 PMID: 10618246
60. Baudoin E, Benizri E, Guckert A. Impact of growth stage on the bacterial community structure along maize roots, as determined by metabolic and genetic fingerprinting. Appl Soil Ecol. 2002; 19: 135-145. doi: 10.1016/S0929-1393(01)00185-8
61. Broeckling CD, Broz AK, Bergelson J, Manter DK, Vivanco JM. Root Exudates Regulate Soil Fungal Community Composition and Diversity. Appl Environ Microbiol. 2008; 74: 738-744. PMID: 18083870
62. Haichar Fel Z, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J, et al. Plant host habitat and root exudates shape soil bacterial community structure. ISME J. 2008; 2: 1221-1230. doi: 10.1038/ismej.2008.80 PMID: 18754043
63. Vos M, Wolf AB, Jennings SJ, Kowalchuk GA. Micro-scale determinants of bacterial diversity in soil. FEMS Microbiol Rev. 2013; 37: 936-954. doi: 10.1111/1574-6976.12023 PMID: 23550883
64. Becker JM, Parkin T, Nakatsu CH, Wilbur JD, Konopka A. Bacterial activity, community structure, and centimeter-scale spatial heterogeneity in contaminated soil. Microb Ecol. 2006; 51: 220-231. PMID: 16463134
65. Oliveira V, Gomes N, Almeida A, Silva A, Simões MM, Smalla K, et al. Hydrocarbon contamination and plant species determine the phylogenetic and functional diversity of endophytic degrading bacteria. Mol Ecol. 2014; 23: 1392-1404. PMID: 24765659
66. Siciliano SD, Germida JJ, Banks K, Greer CW. Changes in Microbial Community Composition and Function during a Polyaromatic Hydrocarbon Phytoremediation Field Trial. Appl Environ Microbiol. 2003; 69: 483-489. PMID: 12514031
67. Allard A-S, Remberger M, Neilson AH. The negative impact of aging on the loss of PAH components in a creosote-contaminated soil. Int Biodeterior Biodegrad. 2000; 46: 43-49. doi: 10.1016/S0964-8305 (00)00050-0
68. Cébron A, Beguiristain T, Faure P, Norini M-P, Masfaraud J-F, Leyval C. Influence of Vegetation on the In Situ Bacterial Community and Polycyclic Aromatic Hydrocarbon (PAH) Degraders in Aged PAH-Contaminated or Thermal-Desorption-Treated Soil. Appl Environ Microbiol. 2009; 75: 6322-6330. doi: 10.1128/AEM.02862-08 PMID: 19633127
69. Khan S, Hesham AE-L, Qing G, Shuang L, He J. Biodegradation of pyrene and catabolic genes in contaminated soils cultivated with Lolium multiflorum L. J Soils Sediments. 2009; 9: 482-491.
70. Aprill W, Sims RC. Evaluation of the use of prairie grasses for stimulating polycyclic aromatic hydrocarbon treatment in soil. Chemosphere. 1990; 20: 253-265. doi: 10.1016/0045-6535(90)90100-8
71. Soleimani M, Afyuni M, Hajabbasi MA, Nourbakhsh F, Sabzalian MR, Christensen JH. Phytoremediation of an aged petroleum contaminated soil using endophyte infected and non-infected grasses. Chemosphere. 2010; 81: 1084-1090. doi: 10.1016/j.chemosphere.2010.09.034 PMID: 20961596
72. Hertenberger G, Zampach P, Bachmann G. Plant species affect the concentration of free sugars and free amino acids in different types of soil. J Plant Nutr Soil Sci. 2002; 165: 557-565.