Skip to main content

Advertisement

SpringerLink
Log in

Influence of PAHs among other coastal environmental variables on total and PAH-degrading bacterial communities

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

We evaluated the relative impact of anthropogenic polycyclic aromatic hydrocarbons (PAHs) among biogeochemical variables on total, metabolically active, and PAH bacterial communities in summer and winter in surface microlayer (SML) and subsurface seawaters (SSW) across short transects along the NW Mediterranean coast from three harbors, one wastewater effluent, and one nearshore observatory reference site. At both seasons, significant correlations were found between dissolved total PAH concentrations and PAH-degrading bacteria that formed a gradient from the shore to nearshore waters. Accumulation of PAH degraders was particularly high in the SML, where PAHs accumulated. Harbors and wastewater outfalls influenced drastically and in a different way the total and active bacterial community structure, but they only impacted the communities from the nearshore zone (<2 km from the shore). By using direct multivariate statistical analysis, we confirmed the significant effect of PAH concentrations on the spatial and temporal dynamic of total and active communities in this area, but this effect was putted in perspective by the importance of other biogeochemical variables.

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
Fig. 5

Similar content being viewed by others

References

  • Agogué H, Casamayor EO, Bourrain M, Obernosterer I, Joux F, Herndl GJ, Lebaron P (2005) A survey on bacteria inhabiting the sea surface microlayer of coastal ecosystems. FEMS Microbiol Ecol 54:269–280

    Article  Google Scholar 

  • Ben Said O, Goñi-Urriza M, El Bour M, Aissa P, Duran R (2010) Bacterial community structure of sediments of the Bizerte Lagoon (Tunisia), a southern Mediterranean coastal anthropized lagoon. Microb Ecol 59:445–456

    Article  Google Scholar 

  • Berdjeb L, Ghiglione J-F, Jacquet S (2011) Bottom-up versus top-down control of hypo-and epilimnion free-living bacterial community structures in two neighboring freshwater lakes. Appl Environ Microbiol 77:3591–3599

    Article  CAS  Google Scholar 

  • Birpinar ME, Talu GF, Gönençgil B (2009) Environmental effects of maritime traffic on the Istanbul Strait. Environ Monit Assess 152:13–23

    Article  Google Scholar 

  • Cappello S, Denaro R, Genovese M, Giuliano L, Yakimov MM (2007) Predominant growth of Alcanivorax during experiments on “oil spill bioremediation” in mesocosms. Microbiol Res 162:185–190

    Article  CAS  Google Scholar 

  • Céa B et al. (2014) An annual survey of bacterial production, respiration and ectoenzyme activity in coastal NW Mediterranean waters: temperature and resource controls. Environ Sci Pollut Res. doi:10.1007/s11356-014-3500-9

  • Cebron A, Norini MP, Beguiristain T, Leyval C (2008) Real-time PCR quantification of PAH-ring hydroxylating dioxygenase (PAH-RHDα) genes from gram positive and gram negative bacteria in soil and sediment samples. J Microbiol Methods 73:148–159

    Article  CAS  Google Scholar 

  • Cunliffe M, Harrison E, Salter M, Schaefer H, Upstill-Goddard RC, Murrell JC (2009) Comparison and validation of sampling strategies for the molecular microbial analysis of surface microlayers. Aquat Microb Ecol 57:69–77

    Article  Google Scholar 

  • Cunliffe M, Upstill Goddard RC, Murrell JC (2011) Microbiology of aquatic surface microlayers. FEMS Microbiol Rev 35:233–246

    Article  CAS  Google Scholar 

  • Del Giorgio PA, Bouvier TC (2002) Linking the physiologic and phylogenetic successions in free‐living bacterial communities along an estuarine salinity gradient. Limnol Oceanogr 47:471–486

    Article  Google Scholar 

  • Delille D, Pelletier E, Rodriguez-Blanco A, Ghiglione JF (2009) Effects of nutrient and temperature on degradation of petroleum hydrocarbons in sub-antarctic coastal seawater. Polar Biol 32:1521–1528

    Article  Google Scholar 

  • Ducklow HW, Myers KMS, Erickson M, Ghiglione JF, Murray AE (2011) Response of a summertime Antarctic marine bacterial community to glucose and ammonium enrichment. Aquat Microb Ecol 64:205–220

    Article  Google Scholar 

  • Durrieu de Madron X, Guieu C, Sempéré R, Conan P, Cossa D, D’Ortenzio F, Estournel C et al (2011) Marine ecosystems responses to climatic and anthropogenic forcings in the Mediterranean. Prog Oceanogr 91:97–166

    Article  Google Scholar 

  • Fernandes MB, Sicre MA, Broyelle I, Lorre A, Pont D (1999) Contamination by polycyclic aromatic hydrocarbons (PAHs) in French and European rivers. Hydrobiologia 410:343–348

    Article  CAS  Google Scholar 

  • Franklin MP, McDonald IR, Bourne DG, Owens NJP, Upstill Goddard RC, Murrell JC (2005) Bacterial diversity in the bacterioneuston (sea surface microlayer): the bacterioneuston through the looking glass. Environ Microbiol 7:723–736

    Article  CAS  Google Scholar 

  • Garrett WD (1965) Collection of slick-forming materials from the sea surface. Limnol Oceanogr 10:602–605

  • Gertler C, Gerdts G, Timmis KN, Golyshin PN (2009) Microbial consortia in mesocosm bioremediation trial using oil sorbents, slow-release fertilizer and bioaugmentation. FEMS Microbiol Ecol 69:288–300

    Article  CAS  Google Scholar 

  • Ghiglione J, Murray A (2012) Pronounced summer to winter differences and higher wintertime richness in coastal Antarctic marine bacterioplankton. Environ Microbiol 14:617–629

    Article  CAS  Google Scholar 

  • Ghiglione JF, Philippot L, Normand P, Lensi R, Potier P (1999) Disruption of narG, the gene encoding the catalytic subunit of respiratory nitrate reductase, also affects nitrite respiration in pseudomonas fluorescens YT101. J Bacteriol 181:5099–5102

    CAS  Google Scholar 

  • Ghiglione JF, Larcher M, Lebaron P (2005) Spatial and temporal scales of variation in bacterioplankton community structure in the NW Mediterranean Sea. Aquat Microb Ecol 40:229–240

    Article  Google Scholar 

  • Ghiglione JF, Palacios C, Marty JC, Mével G, Labrune C, Conan P, Pujo-Pay M, Garcia N, Goutx M (2008) Role of environmental factors for the vertical distribution (0–1000 m) of marine bacterial communities in the NW Mediterranean Sea. Biogeosciences 5:1751–1764

    Article  CAS  Google Scholar 

  • Ghiglione JF, Conan P, Pujo-Pay M (2009) Diversity of total and active free-living vs. particle-attached bacteria in the euphotic zone of the NW Mediterranean Sea. FEMS Microbiol Lett 299:9–21

    Article  CAS  Google Scholar 

  • Ghiglione JF, Galand PE, Pommier T, Pedrós-Alió C, Maas EW, Bakker K, Bertilson S, Kirchman DL, Lovejoy C, Yager PL, Murray AE (2012) Pole-to-pole biogeography of surface and deep marine bacterial communities. Proc Natl Acad Sci U S A 109:17633–17638

    Article  CAS  Google Scholar 

  • Gomez F (2003) The role of the exchanges through the strait of Gibraltar on the budget of elements in the western Mediterranean Sea: consequences of human-induced modifications. Mar Pollut Bull 46:685–694

    Article  CAS  Google Scholar 

  • Guerin WF (1989) Phenanthrene degradation by estuarine surface microlayer and bulk water microbial populations. Microb Ecol 17:89–104

    Article  CAS  Google Scholar 

  • Guigue C, Tedetti M, Giorgi S, Goutx M (2011) Occurrence and distribution of hydrocarbons in the surface microlayer and subsurface water from the urban coastal marine area off Marseilles, northwestern Mediterranean Sea. Mar Pollut Bull 62:2741–2752

    Article  CAS  Google Scholar 

  • Guigue C, Tedetti M, Ferretto N, Garcia N, Méjanelle L, Goutx M (2014) Spatial and seasonal variabilities of dissolved hydrocarbons in surface waters from the northwestern Mediterranean Sea: results from 1 year intensive sampling. Sci Total Environ 466:650–662

    Article  Google Scholar 

  • Guitart C, García-Flor N, Miquel JC, Fowler SW, Albaigés J (2010) Effect of the accumulation of polycyclic aromatic hydrocarbons in the sea surface microlayer on their coastal air-sea exchanges. J Mar Syst 79:210–217

    Article  Google Scholar 

  • Hardy JT (1982) The sea surface microlayer: biology, chemistry and anthropogenic enrichment. Prog Oceanogr 11:307–328

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Holmes RM, Aminot A, Kérouel R, Hooker BA, Peterson BJ (1999) A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Can J Fish Aquat Sci 56:1801–1808

    Article  CAS  Google Scholar 

  • Johnsen AR, Henriksen S (2009) Microplate MPN-enumeration of monocyclic-and dicyclic-aromatic hydrocarbon degraders via substrate phase-partitioning. Biodegradation 20:581–589

    Article  CAS  Google Scholar 

  • Kennish MJ (1992) Polynuclear aromatic hydrocarbons. Ecology of estuaries: anthropogenic effects. CRC Press, Boca Raton, pp 133–181

    Google Scholar 

  • Kérouel R, Aminot A (1997) Fluorometric determination of ammonia in sea and estuarine waters by direct segmented flow analysis. Mar Chem 57:265–275

  • Lami R, Ghiglione JF, Desdevises Y, West NJ, Lebaron P (2009) Annual patterns of presence and activity of marine bacteria monitored by 16S rDNA–16S rRNA fingerprints in the coastal NW Mediterranean Sea. Aquat Microb Ecol 54:199–210

    Article  Google Scholar 

  • Lee DH, Zo YG, Kim SJ (1996) Nonradioactive method to study genetic profiles of natural bacterial communities by PCR-single-strand-conformation polymorphism. Appl Environ Microbiol 62:3112–3120

    CAS  Google Scholar 

  • Lekunberri I et al (2010) Changes in bacterial activity and community composition caused by exposure to a simulated oil spill in microcosm and mesocosm experiments. Aquat Microb Ecol 59:169–183

    Article  Google Scholar 

  • Lim L, Wurl O, Karuppiah S, Obbard JP (2007) Atmospheric wet deposition of PAHs to the sea-surface microlayer. Mar Pollut Bull 54:1212–1219

    Article  CAS  Google Scholar 

  • Mével G, Vernet M, Goutx M, Ghiglione JF (2008) Seasonal to hour variation scales in abundance and production of total and particle-attached bacteria in the open NW Mediterranean Sea (0–1000 m). Biogeosciences 5:1573–1586

    Article  Google Scholar 

  • Mille G, Asia L, Guiliano M, Malleret L, Doumenq P (2007) Hydrocarbons in coastal sediments from the Mediterranean Sea (Gulf of Fos area, France). Mar Pollut Bull 54:566–575

    Article  CAS  Google Scholar 

  • Moeseneder MM, Winter C, Herndl GJ (2001) Horizontal and vertical complexity of attached and free-living bacteria of the eastern Mediterranean Sea, determined by 16S rDNA and 16S rRNA fingerprints. Limnol Oceanogr 46:95–107

    Article  CAS  Google Scholar 

  • Ortega-Retuerta E, Joux F, Jeffrey WH, Ghiglione J-F (2013) Spatial variability of particle-attached and free-living bacterial diversity in surface waters from the Mackenzie river to the Beaufort Sea (Canadian arctic). Biogeosciences 10:2747–2759

    Article  Google Scholar 

  • Pairaud I, Gatti J, Bensoussan N, Verney R, Garreau P (2011) Hydrology and circulation in a coastal area off Marseille: validation of a nested 3D model with observations. J Mar Syst 88:20–33

    Article  Google Scholar 

  • Pérez-de-Mora A, Schulz S, Schloter M (2010) MPN-and real-time-based PCR methods for the quantification of alkane monooxygenase homologous genes (alkB) in environmental samples. Methods Mol Biol (Clifton, NJ) 599:59–68

    Article  Google Scholar 

  • Poulsen LK, Ballard G, Stahl DA (1993) Use of rRNA fluorescence in situ hybridization for measuring the activity of single cells in young and established biofilms. Appl Environ Microbiol 59:1354–1360

    CAS  Google Scholar 

  • Rabouille C, Mackenzie FT, Ver LM (2001) Influence of the human perturbation on carbon, nitrogen, and oxygen biogeochemical cycles in the global coastal ocean. Geochim Cosmochim Acta 65:3615–3641

    Article  CAS  Google Scholar 

  • Rodríguez-Blanco A, Ghiglione JF, Catala P, Casamayor EO, Lebaron P (2009) Spatial comparison of total vs. active bacterial populations by coupling genetic fingerprinting and clone library analyses in the NW Mediterranean Sea. FEMS Microbiol Ecol 67:30–42

    Article  Google Scholar 

  • Rodríguez-Blanco A, Antoine V, Pelletier E, Delille D, Ghiglione JF (2010) Effects of temperature and fertilization on total vs. active bacterial communities exposed to crude and diesel oil pollution in NW Mediterranean Sea. Environ Pollut 158:663–673

    Article  Google Scholar 

  • Rodríguez-Blanco A, Duval A, Pelletier E, Delille D, Ghiglione JF (2013) Effects of temperature and fertilization on the structure of total versus active bacterial communities from sub-Antarctic seawater exposed to crude oil and diesel fuel. Polar Res 32:18521–18531

    Article  Google Scholar 

  • Sapp M, Wichels A, Wiltshire KH, Gerdts G (2007) Bacterial community dynamics during the winter–spring transition in the North Sea. FEMS Microbiol Ecol 59:622–637

    Article  CAS  Google Scholar 

  • Sauret C, Christaki U, Moutsaki P, Hatzianestis I, Gogou A, Ghiglione JF (2012) Influence of pollution history on the response of coastal bacterial and nanoeukaryote communities to crude oil and biostimulation assays. Mar Environ Res 79:70–78

    Article  CAS  Google Scholar 

  • Sauret C et al (2014) Rare biosphere bacteria as key phenanthrene degraders in coastal seawaters. Environ Pollut 194:246–253

    Article  CAS  Google Scholar 

  • Singh KP, Mohan D, Sinha S, Dalwani R (2004) Impact assessment of treated/untreated wastewater toxicants discharged by sewage treatment plants on health, agricultural, and environmental quality in the wastewater disposal area. Chemosphere 55:227–255

    Article  CAS  Google Scholar 

  • Sogin ML et al (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci U S A 103:12115–12120

    Article  CAS  Google Scholar 

  • Sohrin R, Sempéré R (2005) Seasonal variation in total organic carbon in the northeast Atlantic in 2000–2001. J Geophys Res 110:C10S90

    Google Scholar 

  • Tedetti M, Guigue C, Goutx M (2010) Utilization of a submersible UV fluorometer for monitoring anthropogenic inputs in the Mediterranean coastal waters. Mar Pollut Bull 60:350–362

    Article  CAS  Google Scholar 

  • Ulses C, Grenz C, Marsaleix P, Schaaff E, Estournel C, Meulé S, Pinazo C (2005) Circulation in a semi-enclosed bay under influence of strong freshwater input. J Mar Syst 56:113–132

    Article  Google Scholar 

  • Van Wambeke F, Ghiglione JF, Nedoma J, Mével G, Raimbault P (2009) Bottom up effects on bacterioplankton growth and composition during summer-autumn transition in the open NW Mediterranean Sea. Biogeosciences 6:705–720

    Article  Google Scholar 

  • Wurl O, Obbard JP (2004) A review of pollutants in the sea-surface microlayer (SML): a unique habitat for marine organisms. Mar Pollut Bull 48:1016–1030

    Article  CAS  Google Scholar 

  • Zhang R, Liu B, Lau SCK, Ki JS, Qian PY (2007) Particle-attached and free-living bacterial communities in a contrasting marine environment: Victoria Harbor, Hong Kong. FEMS Microbiol Ecol 61:496–508

    Article  CAS  Google Scholar 

  • Zhang R, Lau SCK, Ki JS, Thiyagarajan V, Qian PY (2009) Response of bacterioplankton community structures to hydrological conditions and anthropogenic pollution in contrasting subtropical environments. FEMS Microbiol Ecol 69:449–460

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to the crew and officials of R/V Antédon II, as well as the Service d’Observation of the MIO, and especially Aria Carame and Mpavjs Guigui for their excellent cooperation. This study is part of a research project “IBISCUS” (Indicateurs Biologiques et chImiques de Contaminations UrbaineS) from Université Aix-Marseille2/CNRS-INSU, which aims at developing observation tools for pollution assessment in urban coastal marine environment and funded by (1) the Continental and Coastal Ecosphere (EC2CO) program from CNRS and the Institut des Sciences de l’Univers (INSU) and (2) “ANR-ECOTECH 09-ECOT-009-01,” Agence Nationale de la Recherche (ANR)—Ademe/Ecotechnologies program, both labeled by the Competitivity Cluster “Pôle Mer PACA.”

Conflict of interest

The authors declare that they have no competing interests.

Author information

Authors and Affiliations

  1. UPMC Univ Paris 06, CNRS, Laboratoire d’Océanographie Microbienne (LOMIC), Observatoire Océanologique, Sorbonne Universités, F-66650, Banyuls/mer, France

    Caroline Sauret, Chloé Dumas, Raphaël Lami, Mireille Pujo-Pay, Pascal Conan & Jean-François Ghiglione

  2. Aix Marseille Université, CNRS, Université de Toulon, IRD, MIO UM 110, 13288, Marseille, France

    Marc Tedetti, Catherine Guigue & Madeleine Goutx

Authors
  1. Caroline Sauret
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marc Tedetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Catherine Guigue
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chloé Dumas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Raphaël Lami
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mireille Pujo-Pay
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Pascal Conan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Madeleine Goutx
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jean-François Ghiglione
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jean-François Ghiglione.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sauret, C., Tedetti, M., Guigue, C. et al. Influence of PAHs among other coastal environmental variables on total and PAH-degrading bacterial communities. Environ Sci Pollut Res 23, 4242–4256 (2016). https://doi.org/10.1007/s11356-015-4768-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-015-4768-0

Keywords

Search

Navigation