Skip to main content
SpringerLink
Log in

Hydrocarbon degradation potential of salt marsh plant–microorganisms associations

  • Original Paper
  • Published:
Biodegradation Aims and scope Submit manuscript

Abstract

Estuaries are often considered sinks for contaminants and the cleanup of salt marshes, sensitive ecosystems with a major ecological role, should be carried out by means of least intrusive approaches, such as bioremediation. This study was designed to evaluate the influence of plant–microorganisms associations on petroleum hydrocarbons fate in salt marshes of a temperate estuary (Lima River, NW Portugal). Sediments un-colonized and colonized (rhizosediments) by different plants (Juncus maritimus, Phragmites australis, Triglochin striata and Spartina patens) were sampled in four sites of the lower and middle estuary for hydrocarbon degrading microorganisms (HD), total cell counts (TCC) and total petroleum hydrocarbons (TPHs) assessment. In general, TPHs, HD and TCC were significantly higher (P < 0.05) in rhizosediments than in un-colonized sediments. Also recorded were differences on the abundance of hydrocarbon degraders among the rhizosediment of the different plants collected at the same site (J. maritimus < P. australis < T. striata), with statistically significant differences (P < 0.05) between J. maritimus and T. striata. Moreover, strong positive correlations—0.81 and 0.84 (P < 0.05), between biotic (HD) and abiotic (organic matter content) parameters and TPHs concentrations were also found. Our data clearly suggest that salt marsh plants can influence the microbial community, by fostering the development of hydrocarbon-degrading microbial populations in its rhizosphere, an effect observed for all plants. This effect, combined with the plant capability to retain hydrocarbons around the roots, points out that salt marsh plant–microorganisms associations may actively contribute to hydrocarbon removal and degradation in estuarine environments.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aichberger H, Hasinger M, Braun R, Loibner AP (2005) Potential of preliminary test methods to predict biodegradation performance of petroleum hydrocarbons in soil. Biodegradation 16:115–125

    Article  PubMed  CAS  Google Scholar 

  • Almeida CM, Mucha AP, Vasconcelos MT (2004) Influence of the sea rush Juncus maritimus on metal concentration and speciation in estuarine sediment colonized by the plant. Environ Sci Technol 38:3112–3118

    Article  PubMed  CAS  Google Scholar 

  • Andrade ML, Covelo EF, Vega FA, Marcet P (2004) Effect of the prestige oil spill on salt marsh soils on the coast of Galicia (Northwestern Spain). J Environ Qual 33:2103–2110

    Article  PubMed  CAS  Google Scholar 

  • Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266

    Article  PubMed  CAS  Google Scholar 

  • Boorman LA (1999) Salt marshes—present functioning and future change. Mang Salt Marsh 3:227–241

    Article  Google Scholar 

  • Braddock JF, Lindstrom JE, Brown EJ (1995) Distribution of hydrocarbon-degrading microorganisms in sediments from Prince William Sound, Alaska, following the Exxon Valdez oil spill. Mar Pollut Bull 30:125–132

    Article  CAS  Google Scholar 

  • Brunk BK, Jirka GH, Lion LW (1997) Effects of salinity changes and the formation of dissolved organic matter on the sorption of phenanthrene—implications for pollutant trapping in estuaries. Environ Sci Technol 31:119–125

    Article  CAS  Google Scholar 

  • Chapman P, Wang F (2001) Assessing sediment contamination in estuaries. Environ Toxicol Chem 20:3–22

    Article  PubMed  CAS  Google Scholar 

  • Clothier BE, Green SR (1997) Roots: the big movers of water and chemicals in soil. Soil Sci 162:534–543

    Article  CAS  Google Scholar 

  • Corgié SC, Joner EJ, Leyval C (2003) Rhizospheric degradation of phenanthrene is a function of proximity to roots. Plant Soil 257:143–150

    Article  Google Scholar 

  • Costanza R, d' Arge R, Groot R, Farber S, Grasso M, Hannon B, Limburg K, Naeem S, O’Neill R, Paruelo J, Raskin R, Sutton P, Belt M (1997) The value of the world’s ecosystem services and natural capital. Nature 387:253–260

    Article  CAS  Google Scholar 

  • Daane LL, Harjono I, Zylstra GJ, Häggblom MM (2001) Isolation and characterization of polycyclic aromatic hydrocarbon-degrading bacteria associated with the rhizosphere of salt marsh plants. Appl Environ Microbiol 67:2683–2691

    Article  PubMed  CAS  Google Scholar 

  • Davis LC, Castro-Diaz S, Zhang Q, Erickson LE (2002) Benefits of vegetation for soils with organic contaminants. Crit Rev Plant Sci 21:457–491

    Article  CAS  Google Scholar 

  • European Committee for Standardization (1999) Soil improvers and growing media—determination of organic matter and ash. Standard CEN EN 13039:1999 E. European Committee for Standardization, Brussels

  • Gregory ST, Shea D, Nichols EG (2005) Impact of vegetation on sedimentary organic matter composition and polycyclic aromatic hydrocarbon attenuation. Environ Sci Technol 39:5285–5292

    Article  PubMed  CAS  Google Scholar 

  • Haines JR, Wrenn BA, Holder EL, Strohmeier KL, Herrington RT, Venosa AD (1996) Measurement of hydrocarbon-degrading microbial populations by a 96-well plate most-probable-number procedure. J Ind Microbiol 16:36–41

    Article  PubMed  CAS  Google Scholar 

  • Hartmann A, Schmid M, van Tuinen D, Berg G (2009) Plant-driven selection of microbes. Plant Soil 321:235–257

    Article  CAS  Google Scholar 

  • Ho Chi-hua, Banks MK (2006) Degradation of polycyclic aromatic hydrocarbons in the rhizosphere of Festuca arundinacea and associated microbial community changes. Bioremed J 10:93–104

    Article  Google Scholar 

  • Hutchinson SL, Schwab AP, Banks MK (2003) Biodegradation of petroleum hydrocarbons in the rhizosphere. In: McCutcheon SC, Schnoor JL (eds) Phytoremediation transformation and control of contaminants. Wiley, New York, pp 355–386

    Google Scholar 

  • Ke L, Yu KSH, Wong YS, Tam NFY (2005) Spatial and vertical distribution of polycyclic aromatic hydrocarbons in mangrove sediments. Sci Total Environ 340:177–187

    Article  PubMed  CAS  Google Scholar 

  • Kepner RL Jr, Pratt JR (1994) Use of fluorochromes for direct enumeration of total bacteria in environmental samples: past and present. Microbiol Rev 58:603–615

    PubMed  CAS  Google Scholar 

  • Kim GB, Maruya KA, Lee RF, Koh CH, Tanabe SS (1999) Distribution and sources of polycyclic aromatic hydrocarbons in sediments from Kyeonggi Bay, Korea. Mar Pollut Bull 28:7–15

    Article  Google Scholar 

  • Kirk JL, Klironomos JN, Lee H, Trevors JT (2005) The effects of perennial ryegrass and alfalfa on microbial abundance and diversity in petroleum contaminated soil. Environ Pollut 133:455–465

    Article  PubMed  CAS  Google Scholar 

  • Kuiper I, Lagendijk EL, Bloemberg GV, Lugtenberg BJJ (2004) Rhizoremediation: a beneficial plant–microbe interaction. Mol Plant-Microbe Interact 17:6–15

    Article  PubMed  CAS  Google Scholar 

  • Kukkonen J, Landrum PF (1996) Distribution of organic carbon and organic xenobiotics among different particle-size fractions in sediments. Chemosphere 32:1063–1076

    Article  CAS  Google Scholar 

  • Lambers H, Mougel C, Jaillard B, Hinsinger P (2009) Plant-microbe-soil interactions in the rhizosphere: an evolutionary perspective. Plant Soil 321:83–115

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Liste HH, Alexander M (2000) Accumulation of phenanthrene and pyrene in rhizosphere soil. Chemosphere 40:11–14

    Article  PubMed  CAS  Google Scholar 

  • Liste HH, Felgentreu D (2006) Crop growth, culturable bacteria, and degradation of petrol hydrocarbons (PHCs) in a long-term contaminated field soil. Appl Soil Ecol 31:43–52

    Article  Google Scholar 

  • Martins M, Ferreira AM, Vale C (2008) The influence of Sarcocornia fruticosa on retention of PAHs in salt marsh sediments (Sado estuary, Portugal). Chemosphere 71:1599–1606

    Article  PubMed  CAS  Google Scholar 

  • Merkl N, Schultze-Kraft R, Arias M (2006) Effect of the tropical grass Brachiaria brizantha (Hochst. ex A. Rich.) Stapf on microbial population and activity in petroleum-contaminated soil. Microbiol Res 161:80–91

    Article  PubMed  CAS  Google Scholar 

  • Mikutta R, Kleber M, Kaiser K, Jahn R (2005) Organic matter removal from soils using hydrogen peroxide, sodium hypochlorite, and disodium peroxodisulfate. Soil Sci Soc Am J 69:120–135

    Article  CAS  Google Scholar 

  • Muratova AY, Turkovskaya OV, Hübner T, Kuschk P (2003) Studies of the efficacy of alfalfa and reed in the phytoremediation of hydrocarbon-polluted soil. Appl Biochem Microbiol 39:599–605

    Article  CAS  Google Scholar 

  • Nemes A, Rawls WJ (2006) Evaluation of different representations of the particle-size distribution to predict soil water retention. Geoderma 132:47–58

    Article  Google Scholar 

  • Nichols TD, Wolf DC, Rogers HB, Beyrouty CA, Reynolds CM (1997) Rhizosphere microbial populations in contaminated soils. Water Air Soil Pollut 95:165–178

    CAS  Google Scholar 

  • Olson PE, Reardon KF, Pilon-Smits EAH (2003) Ecology of rhizosphere bioremediation. In: McCutcheon SC, Schnoor JL (eds) Phytoremediation transformation and control of contaminants. Wiley, New York, pp 317–353

    Google Scholar 

  • Porter KG, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–948

    Article  Google Scholar 

  • Prosser JI, Rangel-Castro JI, Killham K (2006) Studying plant–microbe interactions using stable isotope technologies. Curr Opin Biotechnol 17:98–102

    Article  PubMed  CAS  Google Scholar 

  • Salt DE, Smith RD, Raskin I (1998) Phytoremediation. Annu Rev Plant Physiol Plant Mol Biol 49:643–668

    Article  PubMed  CAS  Google Scholar 

  • Vidali M (2001) Bioremediation. An overview. Pure Appl Chem 73:1163–1172

    Article  CAS  Google Scholar 

  • Wang XC, Zhang YX, Chen RF (2001) Distribution and partitioning of pahs in different size fractions in sediments. Mar Pollut Bull 42:1139–1149

    Article  PubMed  CAS  Google Scholar 

  • Wang J, Zhang Z, Su Y, He W, He F, Song H (2008) Phytoremediation of petroleum polluted soil. Pet Sci 5:167–171

    Article  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Xu SY, Chen YX, Wu WX, Wang KX, Lin Q, Liang XQ (2006) Enhanced dissipation of phenanthrene and pyrene in spiked soils by combined plants cultivation. Sci Total Environ 363:206–215

    Article  PubMed  CAS  Google Scholar 

  • Xu J, Yu Y, Wang P, Guo W, Dai S, Sun H (2007) Polycyclic aromatic hydrocarbons in the surface sediments from Yellow River, China. Chemosphere 67:1408–1414

    Article  PubMed  CAS  Google Scholar 

  • Yang GP (2000) Polycyclic aromatic hydrocarbons in the sediments of the South China Sea. Environ Pollut 108:2625–2632

    Article  Google Scholar 

  • Zhang J, Cai L, Yuan D, Chen M (2004) Distribution and sources of polynuclear aromatic hydrocarbons in Mangrove surficial sediments of Deep Bay. China Mar Pollut Bull 49:479–486

    Article  CAS  Google Scholar 

  • Zhu X, Venosa A, Makram T, Lee K (2004) Guidelines for the bioremediation of oil contaminated salt marshes. EPA/600/R-04/074. US Environmental Protection Agency, Cincinnati

    Google Scholar 

Download references

Acknowledgments

Authors acknowledge Paula Guedes and Jaqueline Cochofel for helping in TPHs determinations, and Paulo Alves (Botanical Department, Faculty of Sciences, University of Porto) for plant identification. This work was funded by Fundação para a Ciência e Tecnologia (FCT), Portugal, through the project PTDC/MAR/099140/2008, and the PhD fellowships awarded to H. Ribeiro (SFRH/BD/47631/2008).

Author information

Authors and Affiliations

  1. Laboratório de Hidrobiologia, Instituto de Ciências Biomédicas de Abel Salazar (ICBAS-UP), Universidade do Porto, Largo Professor Abel Salazar, no. 2, 4099-003, Porto, Portugal

    Hugo Ribeiro & Adriano A. Bordalo

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

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

Authors
  1. Hugo Ribeiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ana P. Mucha
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C. Marisa R. Almeida
    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

Corresponding author

Correspondence to Hugo Ribeiro.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ribeiro, H., Mucha, A.P., Almeida, C.M.R. et al. Hydrocarbon degradation potential of salt marsh plant–microorganisms associations. Biodegradation 22, 729–739 (2011). https://doi.org/10.1007/s10532-010-9446-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10532-010-9446-9

Keywords

Search

Navigation