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Variation in pickleweed root-associated microbial communities at different locations of a saline solid waste management unit contaminated with petroleum hydrocarbons


Autoři: Abdur Rahim Khan aff001;  L. G. Reichmann aff001;  J. C. Ibal aff002;  J. H. Shin aff002;  Y. Liu aff001;  H. Collins aff003;  B. LePage aff004;  N. Terry aff001
Působiště autorů: Department of Plant and Microbial Biology, University of California, Berkeley, CA, United States of America aff001;  School of Applied Biosciences, College of Agriculture and Life Sciences, Kyungpook National University, Daegu, Republic of Korea aff002;  USDA-ARS Grassland Soil and Water Research Laboratory, Temple, TX, United States of America aff003;  Pacific Gas and Electric Company, San Ramon, CA, United States of America aff004;  The Academy of Natural Science, Philadelphia, PA, United States of America aff005
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0222901

Souhrn

The main purpose of this study was to explore the potential influences of pickleweed vegetation on the abundance, diversity and metabolic activities of microbial communities in four distinct areas of a petroleum-contaminated solid waste management unit (SWMU) located in Contra Costa County, northern California. The four areas sampled include two central areas, one of which is central vegetated (CV) and one unvegetated (UV), and two peripheral vegetated areas, one of which is located to the west side of the SWMU (V-West) and one located to the east side (V-East). Measurements were made of total petroleum hydrocarbons (TPH), polyaromatic hydrocarbons (PAH), soil physicochemical properties, and various aspects of microbial communities including metabolic activities, microbial abundances (PLFAs), diversity and composition based on amplicon sequencing. The peripheral V-East and V-West sites had 10-times lower electrical conductivity (EC) than that of the CV and UV sites. The high salinity levels of the CV and UV sites were associated with significant reductions in bacterial and fungal abundances (PLFA) when compared to V-East but not when compared to V-West. TPH levels of CV and UV were not significantly different from those of V-West but were substantially lower than V-East TPH (19,311 mg/kg of dry soil), the high value of which may have been associated with a pipeline that ran through the area. Microbial activities (in terms of soil respiration and the activities of three soil enzymes, i.e., urease, lipase, and phosphatase) were greatest in the vegetated sites compared to the UV site. The prokaryotic community was not diverse as revealed by the Shannon index with no significant variation among the four groups of samples. However, the fungal community of the peripheral sites, V-East and V-West had significantly higher OTU richness and Shannon index. Structure of prokaryotic communities inhabiting the rhizosphere of pickleweed plants at the three sites differed significantly and were also different from those found in the UV region of the central site according to pairwise, global PERMANOVA and ANOSIM analyses. The differences in OTU-based rhizosphere-associated bacterial and fungal communities’ composition were explained mainly by the changes in soil EC and pH. The results suggest that saline TPH-contaminated areas that are vegetated with pickleweed are likely to have increased abundances, diversity and metabolic activities in the rhizosphere compared to unvegetated areas, even in the presence of high salinity.

Klíčová slova:

Fungi – Bacteria – Fungal structure – Rhizosphere – Community structure – Salinity – Hydrocarbons – Petroleum


Zdroje

1. Gkorezis P, Daghio M, Franzetti A, Van Hamme JD, Sillen W, Vangronsevld J. The Interaction between Plants and Bacteria in the Remediation of Petroleum Hydrocarbons: An Environmental Perspective. Frontiers in microbiology. 2016;7. doi: 10.3389/fmicb.2016.00007

2. Brassington KJ, Hough RL, Paton GI, Semple KT, Risdon GC, Crossley J, et al. Weathered Hydrocarbon Wastes: A Risk Management Primer. Critical Reviews in Environmental Science and Technology. 2017; 37: 199–232. doi: 10.1080/10643380600819625

3. Cocârţă DM, Stoian MA, Karademir A. Crude Oil Contaminated Sites: Evaluation by Using Risk Assessment Approach. Sustainability. 2017; 9: 1365.

4. dos Santos JJ, Maranho LT. Rhizospheric microorganisms as a solution for the recovery of soils contaminated by petroleum: A review. Journal of Environmental Management. 2018; 210: 104–113. doi: 10.1016/j.jenvman.2018.01.015 29331851

5. Gremion F, Chatzinotas A, Kaufmann K, von Sigler W, Harms H. Impacts of Heavy Metal Contamination and Phytoremediation on A Microbial Community During A Twelve-Month Microcosm Experiment. FEMS Microbiology Ecology. 2004; 48 (2):273–283. doi: 10.1016/j.femsec.2004.02.004 19712410

6. Shahi A, Aydin S, Ince B, Ince O. Reconstruction of bacterial community structure and variation for enhanced petroleum hydrocarbons degradation through biostimulation of oil contaminated soil. Chemical Engineering Journal. 2016; 306: 60–66. doi: 10.1016/j.cej.2016.07.016

7. Varjani SJ. Microbial degradation of petroleum hydrocarbons. Bioresource Technology. 2017; 223: 277–286. doi: 10.1016/j.biortech.2016.10.037 27789112

8. Correa-García S, Pande P, Séguin A, St-Arnaud M, Yergeau E. Rhizoremediation of petroleum hydrocarbons: a model system for plant microbiome manipulation. Microbial Biotechnology. 2018; 11: 819–832. doi: 10.1111/1751-7915.13303 30066464

9. Kuiper I, Lagendijk EL, Bloemberg GV, Lugtenberg BJ. Rhizoremediation: a beneficial plant-microbe interaction. Molecular Plant-Microbe Interactions: MPMI. 2004; 17: 6–15. doi: 10.1094/MPMI.2004.17.1.6 14714863

10. Cai B, Ma J, Yan G, Dai X, Li M, Guo S. Comparison of phytoremediation, bioaugmentation and natural attenuation for remediating saline soil contaminated by heavy crude oil. Biochemical Engineering Journal. 2016; 112: 170–177. https://doi.org/10.1016/j.bej.2016.04.018

11. Ebadi A, Khoshkholgh Sima NA, Olamaee M, Hashemi M, Ghorbani Nasrabadi R. Remediation of saline soils contaminated with crude oil using the halophyte Salicornia persica in conjunction with hydrocarbon-degrading bacteria. Journal of Environmental Management. 2018; 219: 260–268. doi: 10.1016/j.jenvman.2018.04.115 29751257

12. Sousa AI, Caçador I, Lillebø AI, Pardal MA. Heavy metal accumulation in Halimione portulacoides: Intra- and extra-cellular metal binding sites. Chemosphere. 2008; 70: 850–857. https://doi.org/10.1016/j.chemosphere.2007.07.012

13. Bourceret A, Leyval C, de Fouquet C, Cebron A. Mapping the Centimeter-Scale Spatial Variability of PAHs and Microbial Populations in the Rhizosphere of Two Plants. PloS One. 2015; 10: e0142851. doi: 10.1371/journal.pone.0142851 26599438

14. Chaudhary DR, Rathore AP, Kumar R, Jha B. Spatial and halophyte-associated microbial communities in intertidal coastal region of India. International Journal of Phytoremediation. 2017; 19: 478–489. doi: 10.1080/15226514.2016.1244168 27739867

15. Xia Mingqian, Liu Y Alicia AT, Fu Dafang, Khan AR Norman Terry. Crude oil depletion by bacterial strains isolated from a petroleum hydrocarbon impacted solid waste management site in California, International Biodeterioration & Biodegradation. 2017; 123: 70–77 https://doi.org/10.1016/j.ibiod.2017.06.003

16. Mukherjee S, Sipilä T, Pulkkinen P, Yrjälä K. Secondary successional trajectories of structural and catabolic bacterial communities in oil-polluted soil planted with hybrid poplar. Molecular Ecology. 2015; 24: 628–642. doi: 10.1111/mec.13053 25545194

17. Weatherburn MJAc. Phenol-hypochlorite reaction for determination of ammonia. Analytical Chemistry. 1967; 39: 971–974.

18. Doane TA, Horwáth WR. Spectrophotometric Determination of Nitrate with a Single Reagent,Analytical Letters. 2003; 36:12, 2713–2722, doi: 10.1081/AL-120024647

19. Jarrell WM, Armstrong DE, Grigal DF, Kelly EF, Monger HC, Wedin DA. Soil Water and Temperature Status. 1999. In: Robertson G. P., Coleman D. C., Bledsoe C. S., and Sollins P. Standard Soil Methods for Long-Term Ecological Research. Oxford University Press. pp 55–73.

20. Mishra S, Jyot J, Kuhad RC, Lal BJA. Evaluation of inoculum addition to stimulate in situ bioremediation of oily-sludge-contaminated soil. Applied and Environmental Microbiology. 2001; 67: 1675–1681 doi: 10.1128/AEM.67.4.1675-1681.2001 11282620

21. Cheng F, Peng X, Zhao P, Yuan J, Zhong C, Cheng Y, et al. Soil Microbial Biomass, Basal Respiration and Enzyme Activity of Main Forest Types in the Qinling Mountains. PLOS ONE. 2013; 8: e67353. doi: 10.1371/journal.pone.0067353 23840671

22. Margesin R, Feller G, Hämmerle M, Stegner U, Schinner F. A colorimetric method for the determination of lipase activity in soil. Biotechnology Letters. 2002; 24: 27–33. doi: 10.1023/A:1013801131553

23. Kandeler E, Gerber H. Short-term assay of soil urease activity using colorimetric determination of ammonium. Biology and Fertility of Soils. 1988; 6: 68–72. doi: 10.1007/BF00257924

24. Eivazi F, Tabatabai MJSBB. Phosphatases in Soils. 1977; 9: 167–172.

25. Buyer JS, Sasser M. High throughput phospholipid fatty acid analysis of soils. Applied Soil Ecology. 2012; 61: 127–130. https://doi.org/10.1016/j.apsoil.2012.06.005

26. Vancov T, Keen B. Amplification of soil fungal community DNA using the ITS86F and ITS4 primers. FEMS Microbiol Letters. 2009; 296: 91–96. doi: 10.1111/j.1574-6968.2009.01621.x 19459948

27. Ren G, Ren W, Teng Y, Li Z. Evident bacterial community changes but only slight degradation when polluted with pyrene in a red soil. Frontiers in Microbiology. 2015; 6: 22. doi: 10.3389/fmicb.2015.00022 25688237

28. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014; 30: 2114–2120. doi: 10.1093/bioinformatics/btu170 24695404

29. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nature Methods. 2010; 7: 335–336. doi: 10.1038/nmeth.f.303 20383131

30. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology. 2009; 75: 7537–7541. doi: 10.1128/AEM.01541-09 19801464

31. Hammer Ø, Harper D, Ryan P. PAST: Palaeontological statistics software package for education and data analysis. Palaeontologia Electronica. 2008; 4: 9–17.

32. Chen L, Luo S, Chen J, Wan Y, Li X, Lui C, et al. A comparative analysis of endophytic bacterial communities associated with hyperaccumulators growing in mine soils. Environmental Science and Pollution Research. 2014; 21: 7538–7547. doi: 10.1007/s11356-014-2670-9 24595752

33. Cundy AB, Bardos RP, Puschenreiter M, Mench M, Bert V, Friesl HW, et al. Brownfields to green fields: Realising wider benefits from practical contaminant phytomanagement strategies. Journal of Environmental Management. 2016; 184: 67–77. doi: 10.1016/j.jenvman.2016.03.028 27068275

34. Ferrari BC, Zhang C, van Dorst J. Recovering Greater Fungal Diversity from Pristine and Diesel Fuel Contaminated Sub-Antarctic Soil Through Cultivation Using Both a High and a Low Nutrient Media Approach. Frontiers in Microbiology. 2011; 2: 217. doi: 10.3389/fmicb.2011.00217 22131985

35. Tardif S, Yergeau É, Tremblay J, Legendre P, Whyte LG, Greer CW. The Willow Microbiome Is Influenced by Soil Petroleum-Hydrocarbon Concentration with Plant Compartment-Specific Effects. Frontiers of Microbiology. 2016; 7. doi: 10.3389/fmicb.2016.01363 27660624

36. Oliveira V, Gomes NCM, Cleary DFR, Almeida A, Silva AMS, et al. Halophyte plant colonization as a driver of the composition of bacterial communities in salt marshes chronically exposed to oil hydrocarbons. FEMS Microbiology Ecology. 2014; 90: 647–662. doi: 10.1111/1574-6941.12425 25204351

37. Yergeau E, Tremblay J, Joly S, Labrecque M, Maynard C. Soil contamination alters the willow root and rhizosphere metatranscriptome and the root–rhizosphere interactome. The ISME Journal. 2018; 12: 869–884. doi: 10.1038/s41396-017-0018-4 29330533

38. Mitter EK, de Freitas JR, Germida JJ. Bacterial Root Microbiome of Plants Growing in Oil Sands Reclamation Covers. Frontiers Microbiology. 2017; 8. doi: 10.3389/fmicb.2017.00849 28559882

39. Yang Y, Dong M, Cao Y, Wang J, Tang M, Ban Y. Comparisons of Soil Properties, Enzyme Activities and Microbial Communities in Heavy Metal Contaminated Bulk and Rhizosphere Soils of Robinia pseudoacacia L. in the Northern Foot of Qinling Mountain. Forests. 2017; 8(11), 430; https://doi.org/10.3390/f8110430

40. Puglisi E, Del Re A, Rao M, Gianfreda LJSB. Development and validation of numerical indexes integrating enzyme activities of soils. Soil Biology and Biochemistry. 2006; 38: 1673–1681.

41. Bell TH, El-Din Hassan S, Lauron-Moreau A, Al-Otaibi F, Hijri M, Yergeau E, et al. Linkage between bacterial and fungal rhizosphere communities in hydrocarbon-contaminated soils is related to plant phylogeny. The ISME Journal. 2014; 8: 331–343. doi: 10.1038/ismej.2013.149 23985744

42. 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 Microbiology Ecology. 2012; 82: 169–181. doi: 10.1111/j.1574-6941.2012.01414.x 22587649

43. Harms H, Schlosser D, Wick LY. Untapped potential: exploiting fungi in bioremediation of hazardous chemicals. Nature Reviews Microbiology. 2011; 9: 177. doi: 10.1038/nrmicro2519 https://www.nature.com/articles/nrmicro2519#supplementary-information 21297669

44. Allen JP, Atekwana EA, Atekwana EA, Duris JW, Werkema DD, Rossbach S, et al. The Microbial Community Structure in Petroleum-Contaminated Sediments Corresponds to Geophysical Signatures Applied and Environmental Microbiology. 2007; 73: 2860–2870. doi: 10.1128/AEM.01752-06%J

45. Dendooven L, Alcántara-Hernández RJ, Valenzuela-Encinas C, Luna-Guido M, Perez-Guevara F, Marsch R. Dynamics of carbon and nitrogen in an extreme alkaline saline soil: A review. Soil Biology and Biochemistry. 2010; 42: 865–877. https://doi.org/10.1016/j.soilbio.2010.02.014

46. Qin X, Tang J, Li D, Zhang M. Effect of the salt contentin soil on bioremediation of soil by contaminated petroleum. Letters in Applied Microbiology. 2013; 55, 210–217. doi: 10.1111/j.1472-765X.2012.03280.x 22725670

47. Abed RMM, Al-Kindi S, Al-Kharusi S. Diversity of Bacterial Communities Along a Petroleum Contamination Gradient in Desert Soils. 2015; 69: 95–105. doi: 10.1007/s00248-014-0475-5 25103912

48. Oren A. Microbial life at high salt concentrations: phylogenetic and metabolic diversity. Saline Systems. 2008; 4: 2–2. doi: 10.1186/1746-1448-4-2 18412960

49. Xia J, Xie ZH, Dunlap CA, Rooney AP, Du ZJ. Rhodohalobacter halophilus gen. nov., sp. nov., a moderately halophilic member of the family Balneolaceae. International Journal of Systematic and Evolutionary Microbiology. 2017; 67: 1281–1287. doi: 10.1099/ijsem.0.001806 28109207

50. Bergman B, Rai AN, Rasmussen U. Cyanobacterial Associations. In: Elmerich C, Newton WE(eds.) Associative and Endophytic Nitrogen-fixing Bacteria and Cyanobacterial Associations. Springer Netherlands, Dordrecht. 2007; pp. 257–301

51. Fountoulakis MS, Terzakis S, Kalogerakis N, Manios T. Removal of polycyclic aromatic hydrocarbons and linear alkylbenzene sulfonates from domestic wastewater in pilot constructed wetlands and a gravel filter. Ecological Engineering. 2009; 35: 1702–1709. https://doi.org/10.1016/j.ecoleng.2009.06.011

52. Ben-David EA, Zaady E, Sher Y, Nejidat A. Assessment of the spatial distribution of soil microbial communities in patchy arid and semi-arid landscapes of the Negev Desert using combined PLFA and DGGE analyses. FEMS Microbiology Ecology. 2011; 76: 492–503. doi: 10.1111/j.1574-6941.2011.01075.x 21401693

53. Ebadi A, Khoshkholgh Sima NA, Olamaee M, HM, Ghorbani NR. Effective bioremediation of a petroleum-polluted saline soil by a surfactant-producing Pseudomonas aeruginosa consortium. Journal of Advanced Research. 2017; 8: 627–633. doi: 10.1016/j.jare.2017.06.008 28831308

54. Mille G, Almallah M, Bianchi M, van Wambeke F, Bertrand JC. Effect of salinity on petroleum biodegradation. Fresenius' Journal of Analytical Chemistry. 1991; 339: 788–791. doi: 10.1007/bf00321746

55. Rhykerd RL, Weaver RW, McInnes KJ. Influence of salinity on bioremediation of oil in soil. Environmental Pollution. 1995; 90: 127–130. doi: 10.1016/0269-7491(94)00087-t 15091510

56. Ulrich AC, Guigard SE, Foght JM, Semple KM, Pooley K, Armstron JE, et al. Effect of salt on aerobic biodegradation of petroleum hydrocarbons in contaminated groundwater. Biodegradation. 2009; 20: 27–38. doi: 10.1007/s10532-008-9196-0 18437506

57. Yergeau E, Sanschagrin S, Maynard C, St-Arnaud M, Greer CW. Microbial expression profiles in the rhizosphere of willows depend on soil contamination. The ISME Journal. 2014; 8: 344–358. doi: 10.1038/ismej.2013.163 24067257


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