Skip to main content

Salt marsh sediment characteristics as key regulators on the efficiency of hydrocarbons bioremediation by Juncus maritimus rhizospheric bacterial community

Environmental Science and Pollution Research volume 22, pages 450–462 (2015)Cite this article

Abstract

Mitigation of petroleum hydrocarbons was investigated during a 5-month greenhouse experiment, to assess the rhizoremediation (RR) potential in sediments with different characteristics colonized by Juncus maritimus, a salt marsh plant commonly found in temperate estuaries. Furthermore, the efficiency of two bioremediation treatments namely biostimulation (BS) by the addition of nutrients, and bioaugmentation (BA) by addition of indigenous microorganisms, was tested in combination with RR. The effect of the distinct treatments on hydrocarbon degradation, root biomass weight, and bacterial community structure was assessed. Our result showed higher potential for hydrocarbon degradation (evaluated by total petroleum hydrocarbon analysis) in coarse rhizosediments with low organic matter (OM), than rhizosediments with high OM, and small size particles. Moreover, the bacterial community structure was shaped according to the rhizosediment characteristics, highlighting the importance of specific microbe-particle associations to define the structure of rhizospheric bacterial communities, rather than external factors, such as hydrocarbon contamination or the applied treatments. The potential for hydrocarbon RR seems to depend on root system development and bacterial diversity, since biodegradation efficiencies were positively related with these two parameters. Treatments with higher root biomass, and concomitantly with higher bacterial diversity yielded higher hydrocarbon degradation. Moreover, BS and BA did not enhance hydrocarbons RR. In fact, it was observed that higher nutrient availability might interfere with root growth and negatively influence hydrocarbon degradation performance. Therefore, our results suggested that to conduct appropriate hydrocarbon bioremediation strategies, the effect of sediment characteristics on root growth/exploration should be taken into consideration, a feature not explored in previous studies. Furthermore, strategies aiming for the recovery of bacterial diversity after oil spills may improve the efficiency of hydrocarbon biodegradation in contaminated salt marsh sediments.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3

References

  • Allison SD, Martiny JB (2008) Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci U S A 105(Suppl 1):11512–11519

    CAS  Article  Google Scholar 

  • Amellal N, Portal J-M, Berthelin J (2001) Effect of soil structure on the bioavailability of polycyclic aromatic hydrocarbons within aggregates of a contaminated soil. Appl Geochem 16:1611–1619

    CAS  Article  Google Scholar 

  • Amézketa E (1999) Soil aggregate stability: a review. J Sustain Agric 14:83–151

    Article  Google Scholar 

  • Andrade M, Covelo E, Vega F, Marcet P (2004) Effect of the oil spill on salt marsh soils on the Coast of Galicia (Northwestern Spain). J Environ Qual 33:2103–2110

    CAS  Article  Google Scholar 

  • Barrett JE, Virginia RA, Wall DH, Cary SC, Adams BJ, Hacker AL, Aislabie JM (2006) Co-variation in soil biodiversity and biogeochemistry in northern and southern Victoria Land, Antarctica. Antarct Sci 18:535

    Article  Google Scholar 

  • Beazley MJ, Martinez RJ, Rajan S, Powell J, Piceno YM, Tom LM, Andersen GL, Hazen TC, Van Nostrand JD, Zhou J (2012) Microbial community analysis of a coastal salt marsh affected by the Deepwater Horizon oil spill. PLoS ONE 7:e41305

    CAS  Article  Google Scholar 

  • Bengough A, Mullins C (1990) Mechanical impedance to root growth: a review of experimental techniques and root growth responses. J Soil Sci 41:341–358

    Article  Google Scholar 

  • Bradley P, Morris J (1990) Physical characteristics of salt marsh sediments: ecological implications. Mar Ecol Prog Ser 61:245–252

    Article  Google Scholar 

  • Buyer JS, Roberts DP, Russek-Cohen E (1999) Microbial community structure and function in the spermosphere as affected by soil and seed type. Can J Microbiol 45:138–144

    CAS  Article  Google Scholar 

  • Cardinale M, Brusetti L, Quatrini P, Borin S, Puglia AM, Rizzi A, Zanardini E, Sorlini C, Corselli C, Daffonchio D (2004) Comparison of different primer sets for use in automated ribosomal intergenic spacer analysis of complex bacterial communities. Appl Environ Microbiol 70:6147–6156

    CAS  Article  Google Scholar 

  • Clarke K, Gorley R (2006) Primer V6: user manual/tutorial. PRIMER-E Ltd, Plymouth

    Google Scholar 

  • Couto MN, Borges JR, Guedes P, Almeida R, Monteiro E, Almeida CMR, Basto MCP, Vasconcelos MTSD (2014) An improved method for the determination of petroleum hydrocarbons from soil using a simple ultrasonic extraction and Fourier transform infrared spectrophotometry. Pet Sci Technol 32:426–432

    CAS  Article  Google Scholar 

  • Danovaro R, Luna GM, Dell’anno A, Pietrangeli B (2006) Comparison of two fingerprinting techniques, terminal restriction fragment length polymorphism and automated ribosomal intergenic spacer analysis, for determination of bacterial diversity in aquatic environments. Appl Environ Microbiol 72:5982–5989

    CAS  Article  Google Scholar 

  • De Gryze S, Jassogne L, Bossuyt H, Six J, Merckx R (2006) Water repellence and soil aggregate dynamics in a loamy grassland soil as affected by texture. Eur J Soil Sci 57:235–246

    Article  Google Scholar 

  • Dell’Anno A, Beolchini F, Rocchetti L, Luna GM, Danovaro R (2012) High bacterial biodiversity increases degradation performance of hydrocarbons during bioremediation of contaminated harbor marine sediments. Environ Pollut 167:85–92

    Article  Google Scholar 

  • Fisher MM, Triplett EW (1999) Automated approach for ribosomal intergenic spacer analysis of microbial diversity and its application to freshwater bacterial communities. Appl Environ Microbiol 65:4630–4636

    CAS  Google Scholar 

  • Galvão TC, Mohn WW, de Lorenzo V (2005) Exploring the microbial biodegradation and biotransformation gene pool. Trends Biotechnol 23:497–506

    Article  Google Scholar 

  • Gao D, Tao Y (2011) Current molecular biologic techniques for characterizing environmental microbial community. Front Environ Sci Eng 6:82–97

    Article  Google Scholar 

  • Garbeva P, van Veen JA, van Elsas JD (2004) Microbial diversity in soil: selection microbial populations by plant and soil type and implications for disease suppressiveness. Annu Rev Phytopathol 42:243–270

    CAS  Article  Google Scholar 

  • Gerhardt KE, Huang X-D, Glick BR, Greenberg BM (2009) Phytoremediation and rhizoremediation of organic soil contaminants: potential and challenges. Plant Sci 176:20–30

    CAS  Article  Google Scholar 

  • Grötzschel S, Köster J, Abed RM, de Beer D (2002) Degradation of petroleum model compounds immobilized on clay by a hypersaline microbial mat. Biodegradation 13:273–283

    Article  Google Scholar 

  • Haines J, Wrenn B, Holder E, Strohmeier K, Herrington R, Venosa A (1996) Measurement of hydrocarbon-degrading microbial populations by a 96-well plate most-probable-number procedure. J Ind Microbiol 16:36–41

    CAS  Article  Google Scholar 

  • Head IM, Jones DM, Roling WF (2006) Marine microorganisms make a meal of oil. Nat Rev Microbiol 4:173–182

    CAS  Article  Google Scholar 

  • Hewson I, Fuhrman JA (2004) Richness and diversity of bacterioplankton species along an estuarine gradient in Moreton Bay, Australia. Appl Environ Microbiol 70:3425–3433

    CAS  Article  Google Scholar 

  • Hoagland D, Arnon D (1950) The water-culture method for growing plants without soil, California agriculture Experiment Station. The College of Agriculture Berkeley

  • Hodge A, Berta G, Doussan C, Merchan F, Crespi M (2009) Plant root growth, architecture and function. Plant Soil 321:153–187

    CAS  Article  Google Scholar 

  • Horel A, Bernard RJ, Mortazavi B (2014) Impact of crude oil exposure on nitrogen cycling in a previously impacted Juncus roemerianus salt marsh in the northern Gulf of Mexico. Environ Sci Pollut Res 21:6982–6993

    CAS  Article  Google Scholar 

  • Horn R, Taubner H, Wuttke M, Baumgartl T (1994) Soil physical properties related to soil structure. Soil Till Res 30:187–216

    Article  Google Scholar 

  • Hrynkiewicz K, Baum C (2012) The potential of rhizosphere microorganisms to promote the plant growth in disturbed soils. In: Malik A, Grohmann E (eds) Environmental protection strategies for sustainable development, strategies for sustainability. Springer, Netherlands, pp 35–64

    Chapter  Google Scholar 

  • 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 Res 11:340–346

    CAS  Article  Google Scholar 

  • Kabir M, Chotte J-L, Rahman M, Bally R, Monrozier LJ (1994) Distribution of soil fractions and location of soil bacteria in a vertisol under cultivation and perennial grass. Plant Soil 163:243–255

    CAS  Article  Google Scholar 

  • Kaimi E, Mukaidani T, Miyoshi S, Tamaki M (2006) Ryegrass enhancement of biodegradation in diesel-contaminated soil. Environ Exp Bot 55:110–119

    CAS  Article  Google Scholar 

  • Kechavarzi C, Pettersson K, Leeds-Harrison P, Ritchie L, Ledin S (2007) Root establishment of perennial ryegrass (L. perenne) in diesel contaminated subsurface soil layers. Environ Pollut 145:68–74

    CAS  Article  Google Scholar 

  • Kladivko EJ, Brown LC, Baker JL (2001) Pesticide transport to subsurface tile drains in humid regions of North America. Crit Rev Environ Sci Technol 31:1–62

    CAS  Article  Google Scholar 

  • Knezovich JP, Harrison FL, Wilhelm RG (1987) The bioavailability of sediment-sorbed organic chemicals: a review. Water Air Soil Pollut 32:233–245

    CAS  Article  Google Scholar 

  • Latour X, Philippot L, Corberand T, Lemanceau P (1999) The establishment of an introduced community of fluorescent pseudomonads in the soil and in the rhizosphere is affected by the soil type. FEMS Microbiol Ecol 30:163–170

    CAS  Article  Google Scholar 

  • López-Bucio J, Cruz-Ramírez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287

    Article  Google Scholar 

  • Lovley DR (2003) Cleaning up with genomics: applying molecular biology to bioremediation. Nat Rev Microbiol 1:35–44

    CAS  Article  Google Scholar 

  • Marschner P, Yang C-H, Lieberei R, Crowley DE (2001) Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biol Biochem 33:1437–1445

    CAS  Article  Google Scholar 

  • Martin BC, George SJ, Price CA, Ryan MH, Tibbett M (2014) The role of root exuded low molecular weight organic anions in facilitating petroleum hydrocarbon degradation: current knowledge and future directions. Sci Total Environ 472:642–653

    CAS  Article  Google Scholar 

  • McGenity TJ (2014) Hydrocarbon biodegradation in intertidal wetland sediments. Curr Opin Biotechnol 27:46–54

    CAS  Article  Google Scholar 

  • Paisse S, Goni-Urriza M, Coulon F, Duran R (2010) How a bacterial community originating from a contaminated coastal sediment responds to an oil input. Microb Ecol 60:394–405

    Article  Google Scholar 

  • Pezeshki SR, DeLaune RD (2012) Soil oxidation-reduction in wetlands and its impact on plant functioning. Biology 1:196–221

    CAS  Article  Google Scholar 

  • Ranjard L, Poly F, Lata JC, Mougel C, Thioulouse J, Nazaret S (2001) Characterization of bacterial and fungal soil communities by automated ribosomal intergenic spacer analysis fingerprints: biological and methodological variability. Appl Environ Microbiol 67:4479–4487

    CAS  Article  Google Scholar 

  • Ribeiro H, Mucha AP, Almeida CM, Bordalo AA (2011) Hydrocarbon degradation potential of salt marsh plant-microorganisms associations. Biodegradation 22:729–739

    CAS  Article  Google Scholar 

  • Ribeiro H, Almeida CMR, Mucha AP, Bordalo AA (2013a) Influence of different salt marsh plants on hydrocarbon degrading microorganisms abundance throughout a phenological cycle. Int J Phytoremediat 15:715–728

    CAS  Article  Google Scholar 

  • Ribeiro H, Almeida CMR, Mucha AP, Teixeira C, Bordalo AA (2013b) Influence of natural rhizosediments characteristics on hydrocarbons degradation potential of microorganisms associated to Juncus maritimus roots. Int Biodeterior Biodegrad 84:86–96

    CAS  Article  Google Scholar 

  • Ribeiro H, Mucha AP, Almeida CM, Bordalo AA (2013c) Bacterial community response to petroleum contamination and nutrient addition in sediments from a temperate salt marsh. Sci Total Environ 458–460:568–576

    Article  Google Scholar 

  • Ribeiro H, Mucha AP, Almeida CM, Bordalo AA (2014) Potential of phytoremediation for the removal of petroleum hydrocarbons in contaminated salt marsh sediments. J Environ Manag 137:10–15

    CAS  Article  Google Scholar 

  • Rissanen AJ, Kurhela E, Aho T, Oittinen T, Tiirola M (2010) Storage of environmental samples for guaranteeing nucleic acid yields for molecular microbiological studies. Appl Microbiol Biotechnol 88:977–984

    CAS  Article  Google Scholar 

  • Roling WFM, Milner MG, Jones DM, Lee K, Daniel F, Swannell RJP, Head IM (2002) Robust hydrocarbon degradation and dynamics of bacterial communities during nutrient-enhanced oil spill bioremediation. Appl Environ Microbiol 68:5537–5548

    CAS  Article  Google Scholar 

  • Singer AC, van der Gast CJ, Thompson IP (2005) Perspectives and vision for strain selection in bioaugmentation. Trends Biotechnol 23:74–77

    CAS  Article  Google Scholar 

  • Tate PT, Shin WS, Pardue JH, Jackson WA (2011) Bioremediation of an experimental oil spill in a Coastal Louisiana salt marsh. Water Air Soil Pollut 223:1115–1123

    Article  Google Scholar 

  • Torsvik V, Øvreås L (2002) Microbial diversity and function in soil: from genes to ecosystems. Curr Opin Microbiol 5:240–245

    CAS  Article  Google Scholar 

  • Tyagi M, da Fonseca MM, de Carvalho CC (2011) Bioaugmentation and biostimulation strategies to improve the effectiveness of bioremediation processes. Biodegradation 22:231–241

    CAS  Article  Google Scholar 

  • Wrenn BA, Venosa AD (1996) Selective enumeration of aromatic and aliphatic hydrocarbon degrading bacteria by a most-probable-number procedure. Can J Microbiol 42:252–258

    CAS  Article  Google Scholar 

  • Yakimov MM, Denaro R, Genovese M, Cappello S, D’Auria G, Chernikova TN, Timmis KN, Golyshin PN, Giluliano L (2005) Natural microbial diversity in superficial sediments of Milazzo Harbor (Sicily) and community successions during microcosm enrichment with various hydrocarbons. Environ Microbiol 7:1426–1441

    CAS  Article  Google Scholar 

  • Zhang B, Deng H, Wang H, Yin R, Hallett PD, Griffiths BS, Daniell TJ (2010) Does microbial habitat or community structure drive the functional stability of microbes to stresses following re-vegetation of a severely degraded soil? Soil Biol Biochem 42:850–859

    CAS  Article  Google Scholar 

  • Zhu X, Venosa AD, Suidan MT, Lee K (2004) Guidelines for the bioremediation of oil contaminated salt marshes. In: Agency UEP (Hrsg.), Cincinnati, OH

Download references

Acknowledgments

The Portuguese Foundation for Science and Technology (FCT) supported this research, through the research project (PTDC/AAC-AMB/113973/2009), and the PhD fellowships awarded to Hugo Ribeiro (SFRH/BD/47631/2008) co-financed by POPH/FSE. This research was partially supported by the European Regional Development Fund (ERDF) through the COMPETE-Operational Competitiveness Programme and national funds through FCT-Foundation for Science and Technology, under the project PEst-C/MAR/LA0015/2013 and through the Project ECORISK (reference NORTE-07-0124-FEDER-000054), co-financed by the North Portugal Regional Operational Programme (ON.2-O Novo Norte), under the National Strategic Reference Framework (NSRF).

Author information

Affiliations

  1. CIMAR/CIIMAR-Centro Interdisciplinar de Investigação Marinha e Ambiental, Universidade do Porto, Rua dos Bragas, 289, 4050-123, Porto, Portugal

    Hugo Ribeiro, C. Marisa R. Almeida, Catarina Magalhães, Adriano A. Bordalo & Ana P. Mucha

  2. Laboratório de Hidrobiologia e Ecologia, Instituto de Ciências Biomédicas de Abel Salazar (ICBAS-UP), Universidade do Porto, Porto, Portugal

    Adriano A. Bordalo

Authors
  1. Hugo Ribeiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. Marisa R. Almeida
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Catarina Magalhães
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Adriano A. Bordalo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ana P. Mucha
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hugo Ribeiro.

Additional information

Responsible editor: Robert Duran

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Ribeiro, H., Almeida, C.M.R., Magalhães, C. et al. Salt marsh sediment characteristics as key regulators on the efficiency of hydrocarbons bioremediation by Juncus maritimus rhizospheric bacterial community. Environ Sci Pollut Res 22, 450–462 (2015). https://doi.org/10.1007/s11356-014-3388-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-3388-4

Keywords

  • Juncus maritimus
  • Salt marsh
  • Sediment characteristics
  • Hydrocarbon bioremediation
  • Bacterial diversity