Skip to main content
Log in

Bacterial community composition and biogeochemical heterogeneity in PAH-contaminated riverbank sediments

  • SEDIMENTS, SEC 4 • SEDIMENT-ECOLOGY INTERACTIONS • RESEARCH ARTICLE
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

Predicting response of microbial communities to pollution requires an underlying understanding of the linkage between microbial community structure and geochemical conditions. Yet, there is scarce information about microbial communities in polycyclic aromatic hydrocarbons (PAH)-contaminated riverbank sediments. The aim of this study was to characterize bacterial communities in highly PAH-contaminated sediments and establish correlations between bacterial communities and environmental geochemistry of the sediments.

Materials and methods

Sediment core samples were collected from a highly PAH-contaminated site for (1) analysis of geochemical parameters including total nitrogen, total organic matter, moisture, total carbon, sulfate, pH, and PAH concentrations and (2) bacterial enumeration, 16S rDNA-based terminal restriction fragment length polymorphism analysis and sequencing.

Results and discussion

Non-metric dimensional scaling analyses revealed that bacterial community composition was strongly influenced by PAH concentration. Sulfate, organic matter, pH, and moisture were also related to community composition. A diverse microbial community was identified by the large number of operational taxonomic units recovered and by phylogenetic analyses. δ-Proteobacteria, firmicutes, and bacteriodetes were the dominant groups recovered. We also observed a high number of phylotypes associated with sulfate-reducing bacteria, some of which have been previously described as important in PAH degradation.

Conclusions

Our study suggests that, despite intense pollution, bacterial community composition did exhibit temporal and spatial variations and were influenced by sediment geochemistry. Significant relationships between bacterial community composition and PAHs suggest that, potentially, extant microbial communities may contribute to natural attenuation and/or bioremediation of PAHs.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Acosta-Gonzalez R-M, Marques S (2013) Characterization of the anaerobic microbial community in oil-polluted subtidal sediments: aromatic biodegradation potential after the Prestige oil spill. Environ Microbiol 15:77–92

    Article  CAS  Google Scholar 

  • Almeida R, Mucha A, Teixeira C, Bordalo A, Almeida M (2013) Biodegradation of petroleum hydrocarbons in estuarine sediments: metal influence. Biodegradation 24:111–123

    Article  CAS  Google Scholar 

  • Amin I, Jacobs A (2013) A study of the contaminated banks of the Mahoning River, Northeastern Ohio, USA: characterization of the contaminated bank sediments and river water-groundwater interactions. Env Earth Sci 70:3237–3244

    Article  CAS  Google Scholar 

  • Bamforth S, Singleton I (2005) Bioremediation of polycyclic aromatic hydrocarbons: current knowledge and future directions. J Chem Technol Biotech 80:723–736

    Article  CAS  Google Scholar 

  • Baniulyte D, Favila E, Kelly J (2009) Shifts in microbial community composition following surface application of dredged river sediments. Microb Ecol 57:160–169

    Article  CAS  Google Scholar 

  • Barns S, Cain E, Sommerville L, Kuske C (2007) Acidobacteria phylum sequences in uranium-contaminated subsurface sediments greatly expand the known diversity within the phylum. Appl Environ Microbiol 73:3113–3116

    Article  CAS  Google Scholar 

  • Bastiaens L, Springael D, Wattiau P, Harms H, deWatcher R, Verachert H, Diels L (2000) Isolation of adherent polycyclic aromatic hydrocarbon (PAH)-degrading bacteria using PAH-sorbing carriers. Appl Environ Microbiol 66:1834–1843

    Article  CAS  Google Scholar 

  • Bernhard A, Colbert D, McManus J, Field K (2005) Microbial community dynamics based on 16S rRNA gene profiles in a Pacific Northwest estuary and its tributaries. FEMS Microb Ecol 52:115–128

    Article  CAS  Google Scholar 

  • Buckley C, Hynes S, Mechan S (2012) Supply of an ecosystem service—farmers’ willingness to adopt riparian buffer zones in agricultural catchments. Environ Sci Pol 24:101–109

    Article  Google Scholar 

  • Cao Z, Liu J, Luan Y, Li Y, Ma M, Xu J, Han S (2010) Distribution and ecosystem risk assessment of polycyclic aromatic hydrocarbons in the Luan River, China. Ecotoxicology 19:827–837

    Article  CAS  Google Scholar 

  • Cardenas E, Wu W, Leigh M, Carley J, Carroll S, Gentry T, Luo J, Watson D, Gu B, Ginder-Vogel M, Kitanidis P, Jardine P, Zhou J, Criddle C, Marsh T, Tiedje J (2008) Microbial communities in contaminated sediments, associated with bioremediation of uranium to submicromolar levels. Appl Environ Microbiol 74:3718–3729

    Article  CAS  Google Scholar 

  • Carter M (2000) Soil sampling and methods of analysis. Carter M, Gregorich E (eds). Florida, Canadian Society of Soil Science

  • Christen B, Dalgaard T (2013) Buffers for biomass production in temperature European agriculture: a review and synthesis on function, ecosystem services and implementation. Biomass Bioenergy 55:53–67

    Article  Google Scholar 

  • Cleary DFR, Oliveira V, Lillebø AI, Gomes NCM, Pereira A, Henriques I, Marques B, Almeida A, Cunha A, Correia A, Lillebo A (2012) Impact of plant species on local environmental conditions, microbiological parameters and microbial composition in a historically Hg-contaminated salt marsh. Mar Pollut Bull 64:263–271

    Article  CAS  Google Scholar 

  • Dell’Anno A, Beolchini F, Gabellini M, Rocchetti L, Pusceddu A, Danovaro R (2009) Bioremediation of petroleum hydrocarbons in anoxic marine sediments: consequences on the speciation of heavy metals. Mar Pollut Bull 58:1808–1814

    Article  Google Scholar 

  • Edlund A, Jansson JK (2006) Changes in active bacterial communities before and after dredging of highly polluted Baltic Sea sediments. Appl Environ Microbiol 72:6800–6807

    Article  CAS  Google Scholar 

  • Eggleton J, Thomas K (2004) A review of factors affecting the release and bioavailability of contaminants during sediment disturbance events. Environ Inter 30:973–980

    Article  CAS  Google Scholar 

  • Feris K, Frazar P, Rillig C, Moore M, Gannon J, Holben WE (2004) Seasonal dynamics of shallow-hyporheic-zone microbial community structure along a heavy-metal contamination gradient. Appl Environ Microbiol 70:2323–2331

    Article  CAS  Google Scholar 

  • Gieg L, Fowler SJ, Berdugo-Clavijo C (2014) Syntrophic biodegradation of hydrocarbon contaminants. Curr Opin Biotech 26:21–29

    Article  Google Scholar 

  • Gomes N, Flocco C, Costa R, Junca H, Vilchez R, Piepe D, Krögerrecklenfort E, Pranhos R, Mendoça-Hagler L, Smalla K (2013) Mangrove microniches determine the structural and functional diversity of enriched petroleum hydrocarbon-degrading consortia. FEMS Ecol 74:276–290

    Article  Google Scholar 

  • Gudasz C, Bastiviken D, Prenme K, Steger K, Tranvik L (2012) Constrained microbial processing of allochthonous organic carbon in boreal lake sediments. Limnol Oceanogr 57:163–175

    Article  CAS  Google Scholar 

  • Guo W, He M, Yang Z, Lin C, Quan X, Wang H (2007) Distribution of polycyclic aromatic hydrocarbons in water, suspended particular matter and sediment from Daliao River watershed, China. Chemosphere 68:93–104

    Article  CAS  Google Scholar 

  • Haller L, Onolla M, Zopfi J, Peduzzi R, Wildi W, Pote J (2011) Composition of bacterial and archaeal communities in freshwater sediments with different contamination levels (Lake Geneva, Switzerland). Water Res 45:1213–1228

    Article  CAS  Google Scholar 

  • Ho Y, Jackson M, Yang Y, Mueller J, Pritchard P (2000) Characterization of fluoranthene and pyrene degrading bacteria isolated from PAH-contaminated soils and sediments. J Ind Microbiol Biotechnol 24:100–112

    Article  CAS  Google Scholar 

  • Holland M (2008) Non metric multidimensional scaling (MDS) University of Georgia, Department of Geology. http://strata.uga.edu/software/pdf/mdsTutorial.pdf

  • Hullar M, Kaplan L, Stahl D (2006) Recurring seasonal dynamics of microbial communities in stream habitats. Appl Environ Microbiol 72:713–722

    Article  CAS  Google Scholar 

  • Jiang L, Zheng Y, Peng X, Zhou H, Zhang C, Xiao X, Wang F (2009) Vertical distribution and diversity of sulfate-reducing prokaryotes in the Pearl River estuarine sediments, Southern China. FEMS Microbiol Ecol 70:249–262

    Article  CAS  Google Scholar 

  • Johnsen A, Karlson U (2004) Evaluation of bacterial strategies to promote the bioavailability of polycyclic aromatic hydrocarbons. Appl Microbiol Biotechnol 63:452–459

    Article  CAS  Google Scholar 

  • Johnsen A, Wick L, Harms H (2005) Principles of microbial PAH degradation in soil. Environ Pollut 133:71–84

    Article  CAS  Google Scholar 

  • Johnston C, Johnston G (2012) Bioremediation of polycyclic aromatic hydrocarbons. In: Arora R (ed) Microbial biotechnology. Energy and Environment, UK, pp 279–296

    Chapter  Google Scholar 

  • Kadnikov V, Loakina A, Likhoshvai A, Gorshkov A, Pogodaeva T, Beletsky A, Mardanov A, Zemskaya T, Ravin N (2013) Composition of the microbial communities of bituminous constructions at natural oil seeps at the bottom of Lake Baikal. Microbiology 82:373–382

    Article  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  CAS  Google Scholar 

  • Lemke M, Leff L (2006) Culturability of stream bacteria assessed at the assemblage and population levels. Microb Ecol 51:365–374

    Article  Google Scholar 

  • Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658–1659

    Article  CAS  Google Scholar 

  • Li C, Zhou H, Wong S, Tam N (2009) Vertical distribution and anaerobic biodegradation of polycyclic aromatic hydrocarbons in mangrove sediments in Hong Kong, South China. Sci Total Environ 407:5772–5779

    Article  CAS  Google Scholar 

  • Liu W, Marsh T, Cheng H, Forney L (1997) Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl Environ Microbiol 63:4516–4522

    CAS  Google Scholar 

  • Lors C, Ryngaert A, Périé F, Diels L, Damidot D (2010) Evolution of bacterial community during bioremediation of PAHs in a coal tar contaminated soil. Chemosphere 81:1263–1271

    Article  CAS  Google Scholar 

  • Machado A, Magalhaes C, Mucha A, Almeida C, Bordalo A (2012) Microbial communities within saltmarsh sediments: composition, abundance and pollution constraints. Est Coast Shelf Sci 99:145–152

    Article  CAS  Google Scholar 

  • Miletto M, Loy A, Antheunisse M, Loeb R, Bodelier P, Laanbroek H (2008) Biogeography of sulfate-reducing prokaryotes in river floodplains. FEMS Microbiol Ecol 64:395–406

    Article  CAS  Google Scholar 

  • Mosher J, Findlay R, Johnston C (2006) Physical and chemical factors affecting microbial biomass and activity in contaminated subsurface sediment. Can J Microbiol 52:397–403

    Article  CAS  Google Scholar 

  • Pies C, Hoffmann P, Petrowsky J, Yang Y, Ternes T, Hofmann T (2008) Characterization and source identification of polycyclic aromatic hydrocarbons (PAHs) in river bank soils. Chemosphere 72:1594–1601

    Article  CAS  Google Scholar 

  • Porat I, Vishnivetskaya T, Mosher J, Brandt C, Yang S, Brooks S, Liang L, Drake M, Podar M, Brown S, Palumbo A (2010) Characterization of the archaeal community in contaminated and uncontaminated surface stream sediments. Microb Ecol 60:784–795

    Article  Google Scholar 

  • Pratt B, Riesen R, Johnston CG (2012) PLFA analyses of microbial communities associated with PAH-contaminated riverbank sediment. Microb Ecol 64:680–691

    Article  CAS  Google Scholar 

  • Rogers S, Ong S, Moorman T (2007) Mineralization of PAHs in coal–tar impacted aquifer sediments and associated microbial community structure investigated with FISH. Chemosphere 69:1563–1573

    Article  CAS  Google Scholar 

  • Shen J, Shao X (2005) A comparison of accelerated solvent extraction, Soxhlet extraction, and ultrasonic-assisted extraction for analysis of terpenoids and sterols in tobacco. Anal Bioanal Chem 6:1003–1008

    Article  Google Scholar 

  • Shi W, Bischoff M, Turco R, Konopka A (2005) Microbial catabolic diversity in soils contaminated with hydrocarbons and heavy metals. Environ Sci Technol 39:1974–1979

    Article  CAS  Google Scholar 

  • Smoot J, Findlay R (2001) Spatial and seasonal variation in a reservoir sedimentary microbial community as determined by phospholipid analysis. Microb Ecol 42:350–358

    Article  CAS  Google Scholar 

  • Sponseller R, Heffernan J, Fisher S (2013) On the multiple ecological roles of water in river networks. Ecosphere 4(art17):1–17. doi:10.1890/ES12-00225.1

    Google Scholar 

  • Suárez-Suárez A, Lopez-Lopez A, Tovar-Sanchez A, Yarza P, Orfila A, Terrados J, Arnds J, Marques S, Niehmann H, Schmitt-Kopplin P, Amann R, Rossello-Mora R (2011) Response of sulfate-reducing bacteria to an artificial oil-spill in a coastal marine sediment. Environ Microbiol 13:1488–1499

    Article  Google Scholar 

  • Sun M, Dafforn K, Johnston E, Brown M (2013) Core sediment bacteria drive community response to anthropogenic contamination over multiple environmental gradients. Environ Microbiol 15:2517–2531

    Article  Google Scholar 

  • United States Army Corps of Engineers (USACE) (1999) Mahoning River Environmental Dredging Reconnaissance Study, USACE Publications

  • United States Army Corps of Engineers (USACE) (2001) Lower Mahoning River, Pennsylvania Environmental Dredging Reconnaissance Study. U.S. Army Corps of Engineers Pittsburgh District Final Report

  • United States Environmental Protection Agency (USEPA) (1996) Test methods for evaluation of solid waste, SW-846, Method 3540C, Soxhlet Extraction Revision 3. USEPA, http://www.epa.gov/osw/hazard/testmethods/sw846/pdfs/3540c.pdf

  • United States Environmental Protection Agency (USEPA) (2007) Test methods for evaluation of solid waste, SW-846, method 8270D, semivolatile organic compounds by gas chromatography/mass spectrometry (GCMS) Revision 4. USEPA, http://www.epa.gov/osw/hazard/testmethods/sw846/pdfs/8270d.pdf

  • United States Environmental Protection Agency (USEPA) (2012) Selected analytical methods for environmental remediation and recovery (SAM)-2012. Office of Research and Development National Homeland Security Research Center http://cfpub.epa.gov/…/si_public_file_download

  • Vishnivetskaya T, Mosher J, Castro H, Palumbo A, Podar M, Brown S, Elias D, Drake M, Gilmour C, Wall J, Brandt C (2011) Mercury and other heavy metals influence bacterial community structure in contaminated Tennessee streams. Appl Environ Microbiol 77:302–311

    Article  CAS  Google Scholar 

  • Wang Y, Tam N (2012) Natural attenuation of contaminated marine sediments from an old floating dock part II: changes of sediment microbial community structure and its relationship with environmental variables. Sci Total Environ 324:95–103

    Google Scholar 

  • Wentzel A, Ellingsen T, Kotlar H, Zotchev S, Throne-Holst M (2007) Bacterial metabolism of long-chain n-alkanes. Appl Microb Biotechnol 76:1209–1221

    Article  CAS  Google Scholar 

  • Zeinali M, Vossoughi M, Ardestani S (2007) Characterization of a moderate thermophilic Nocardia species able to grow on polycyclic aromatic hydrocarbons. Lett Appl Microbiol 45:622–628

    Article  CAS  Google Scholar 

  • Zhang W, Ki J, Qian P (2008) Microbial diversity in polluted harbor sediments I: bacterial community assessment based on four clone libraries of 16S rDNA. Est Coast Shelf Sci 76:668–681

    Article  Google Scholar 

Download references

Acknowledgments

G. Johnston was supported by the National Science Foundation Integrated Graduate Education and Research Training grant DGE 0904560. This research was funded by the Art and Margaret Herrick Aquatic Ecology Research Facility Student Research Grant at Kent State University. We thank Dr. Thomas Diggins, Youngstown State University, for considerable assistance with the statistical analyses, Dr. Kurt Smemo, Holden Arboretum Cleveland, for his technical assistance, Dr. David Lineman for GC-MS analysis, and Mr. Daniel Lisko, Youngstown State University, for field and technical support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gloria P. Johnston.

Additional information

Responsible editor: John R. Lawrence

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Johnston, G.P., Leff, L.G. Bacterial community composition and biogeochemical heterogeneity in PAH-contaminated riverbank sediments. J Soils Sediments 15, 225–239 (2015). https://doi.org/10.1007/s11368-014-1005-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-014-1005-2

Keywords

Navigation