Abstract
In estuarine ecosystems, metallic and organic contaminants are mainly associated with fine grain sediments which settle on mudflats. Over time, the layers of sediment accumulate and are then transformed by diagenetic processes mainly controlled by microbial activity, recording the history of the estuary’s chemical contamination. In an environment of this specific type, we investigated the evolution of the chemical contamination and the structure of both total and active microbial communities, based on PhyloChip analysis of a 4.6-m core corresponding to a 40-year sedimentary record. While the archaeal abundance remained constant along the core, a decrease by one order of magnitude in the bacterial abundance was observed with depth. Both total and active microbial communities were dominated by Proteobacteria, Actinobacteria, and Firmicutes in all sediment samples. Among Proteobacteria, alpha-Proteobacteria dominated both total (from 37 to 60 %) and metabolically active (from 19.7 to 34.6 %) communities, including the Rhizobiales, Rhodobacter, Caulobacterales, and Sphingomonadales orders. Co-inertia analysis revealed a relationship between polycyclic aromatic hydrocarbons, zinc and some polychlorobiphenyls concentrations, and the structure of total and active microbial communities in the oldest and most contaminated sediments (from 1970 to 1975), suggesting that long-term exposure to chemicals shaped the structure of the microbial community.





Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Abou-Shanab RAI, Van Berkum P, Angle JS (2007) Heavy metal resistance and genotypic analysis of metal resistance genes in gram-positive and gram-negative bacteria present in Ni-rich serpentine soil and in the rhizosphere of Alyssum murale. Chemosphere 68:360–367
Akob DM, Mills HJ, Kostka JE (2007) Metabolically active microbial communities in uranium-contaminated subsurface sediments. FEMS Microbiol Ecol 59:95–107
Beazley MJ, Martinez RJ, Rajan S et al (2012) Microbial community analysis of a coastal salt marsh affected by the Deepwater Horizon oil spill. PLoS One 7, e41305
Berdugo‐Clavijo C, Dong X, Soh J et al (2012) Methanogenic biodegradation of two-ringed polycyclic aromatic hydrocarbons. FEMS Microbiol Ecol 81:124–133
Berner RA (1980) Early diagenesis: a theoretical approach. Princeton University Press
Billon G, Ouddane B, Boughriet A (2001) Chemical speciation of sulfur compounds in surface sediments from three bays (Fresnaye, Seine and Authie) in northern France, and identification of some factors controlling their generation. Talanta 53:971–981
Boonyatumanond R, Wattayakorn G, Togo A, Takada H (2006) Distribution and origins of polycyclic aromatic hydrocarbons (PAHs) in riverine, estuarine, and marine sediments in Thailand. Mar Pollut Bull 52:942–956
Bouskill NJ, Barker-Finkel J, Galloway TS et al (2010) Temporal bacterial diversity associated with metal-contaminated river sediments. Ecotoxicology 19:317–328
Breuker A, Köweker G, Blazejak A, Schippers A (2011) The deep biosphere in terrestrial sediments in the Chesapeake Bay area, Virginia, USA. Front Microbiol 2
Bruce KD, Hiorns WD, Hobman JL et al (1992) Amplification of DNA from native populations of soil bacteria by using the polymerase chain reaction. Appl Environ Microbiol 58:3413–3416
Budzinski H, Jones I, Bellocq J et al (1997) Evaluation of sediment contamination by polycyclic aromatic hydrocarbons in the Gironde estuary. Mar Chem 58:85–97
Burguener GF, Maldonado MJ, Revale S et al (2014) Draft genome sequence of the polyextremophilic Halorubrum sp. strain AJ67, isolated from hyperarsenic lakes in the Argentinian Puna. Genome Announc 2:e01096–13
Cachot J, Geffard O, Augagneur S et al (2006) Evidence of genotoxicity related to high PAH content of sediments in the upper part of the Seine estuary (Normandy, France). Aquat Toxicol 79:257–267
Cachot J, Cherel Y, Larcher T et al (2013) Histopathological lesions and DNA adducts in the liver of European flounder (Platichthys flesus) collected in the Seine estuary versus two reference estuarine systems on the French Atlantic coast. Environ Sci Pollut Res 20:723–737
Canfield DE, Thamdrup B (2009) Towards a consistent classification scheme for geochemical environments, or, why we wish the term “suboxic”would go away. Geobiology 7:385–392
Carignan J, Hild P, Mevelle G et al (2001) Routine analyses of trace elements in geological samples using flow injection and low pressure on-line liquid chromatography coupled to ICP-MS: a study of geochemical reference materials BR, DR-N, UB-N, AN-G and GH. Geostand Newsl 25:187–198
Chevreuil M, Carru A-M, Chesterikoff A et al (1995) Contamination of fish from different areas of the river Seine (France) by organic (PCB and pesticides) and metallic (Cd, Cr, Cu, Fe, Mn, Pb and Zn) micropollutants. Sci Total Environ 162:31–42
Chiffoleau J-F, Auger D, Chartier E et al (2001) Spatiotemporal changes in cadmium contamination in the Seine estuary (France). Estuaries 24:1029–1040
Choudhury R, Srivastava S (2001) Mechanism of zinc resistance in Pseudomonas putida strain S4. World J Microbiol Biotechnol 17:149–153
Copard Y, Di-Giovanni C, Martaud T et al (2006) Using Rock-Eval 6 pyrolysis for tracking fossil organic carbon in modern environments: implications for the roles of erosion and weathering. Earth Surf Process Landf 31:135–153
Coulon F, Chronopoulou P-M, Fahy A et al (2012) Central role of dynamic tidal biofilms dominated by aerobic hydrocarbonoclastic bacteria and diatoms in the biodegradation of hydrocarbons in coastal mudflats. Appl Environ Microbiol 78:3638–3648
Cravo-Laureau C, Duran R (2014) Marine coastal sediments microbial hydrocarbon degradation processes: contribution of experimental ecology in the Omics’ era. Name Front Microbiol 5:39
Dash HR, Mangwani N, Chakraborty J et al (2013) Marine bacteria: potential candidates for enhanced bioremediation. Appl Microbiol Biotechnol 97:561–571
Dell’Anno A, Fabiano M, Duineveld GCA et al (1998) Nucleic acid (DNA, RNA) quantification and RNA/DNA ratio determination in marine sediments: comparison of spectrophotometric, fluorometric, and highperformance liquid chromatography methods and estimation of detrital DNA. Appl Environ Microbiol 64:3238–3245
Dhote M, Juwarkar A, Kumar A et al (2010) Biodegradation of chrysene by the bacterial strains isolated from oily sludge. World J Microbiol Biotechnol 26:329–335
Dolédec S, Chessel D (1994) Co‐inertia analysis: an alternative method for studying species–environment relationships. Freshw Biol 31:277–294
Dray S, Dufour A-B (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20
Feris K, Ramsey P, Frazar C et al (2003) Differences in hyporheic-zone microbial community structure along a heavy-metal contamination gradient. Appl Environ Microbiol 69:5563–5573
Fernandes MB, Sicre M-A, Boireau A, Tronczynski J (1997) Polyaromatic hydrocarbon (PAH) distributions in the Seine River and its estuary. Mar Pollut Bull 34:857–867
Fernández-Luqueño F, Valenzuela-Encinas C, Marsch R et al (2011) Microbial communities to mitigate contamination of PAHs in soil—possibilities and challenges: a review. Environ Sci Pollut Res 18:12–30
Gillan DC, Danis B, Pernet P et al (2005) Structure of sediment-associated microbial communities along a heavy-metal contamination gradient in the marine environment. Appl Environ Microbiol 71:679–690
Gillan DC, Baeyens W, Bechara R et al (2012) Links between bacterial communities in marine sediments and trace metal geochemistry as measured by in situ DET/DGT approaches. Mar Pollut Bull 64:353–362
Gremion F, Chatzinotas A, Harms H (2003) Comparative 16S rDNA and 16S rRNA sequence analysis indicates that Actinobacteria might be a dominant part of the metabolically active bacteria in heavy metal‐contaminated bulk and rhizosphere soil. Environ Microbiol 5:896–907
Grosbois C, Meybeck M, Lestel L et al (2012) Severe and contrasted polymetallic contamination patterns (1900–2009) in the Loire River sediments (France). Sci Total Environ 435:290–305
Grousset FE, Jouanneau JM, Castaing P et al (1999) A 70 year record of contamination from industrial activity along the Garonne River and its tributaries (SW France). Estuar Coast Shelf Sci 48:401–414
Hamzeh M, Ouddane B, El-daye M, Halwani J (2013) Profile of trace metals accumulation in core sediment from Seine river estuary (docks basin). Environ Technol 34:1107–1116
Hamzeh M, Ouddane B, Daye M, Halwani J (2014) Trace metal mobilization from surficial sediments of the Seine river estuary. Water Air Soil Pollut 225:1–15
Hernandez‐Raquet G, Budzinski H, Caumette P et al (2006) Molecular diversity studies of bacterial communities of oil polluted microbial mats from the Etang de Berre (France). FEMS Microbiol Ecol 58:550–562
Higson FK (1991) Degradation of xenobiotics by white rot fungi. Rev Environ Contam Toxicol Springer, pp 111–152
Hou L-H, Dutta SK (2000) Phylogenetic characterization of several para‐and meta‐PCB dechlorinating Clostridium species: 16s rDNA sequence analyses. Lett Appl Microbiol 30:238–243
Imfeld G, Vuilleumier S (2012) Measuring the effects of pesticides on bacterial communities in soil: a critical review. Eur J Soil Biol 49:22–30
Jones MD, Crandell DW, Singleton DR, Aitken MD (2011) Stable‐isotope probing of the polycyclic aromatic hydrocarbon‐degrading bacterial guild in a contaminated soil. Environ Microbiol 13:2623–2632
Kaci A, Petit F, Lesueur P et al (2014) Distinct diversity of the czcA gene in two sedimentary horizons from a contaminated estuarine core. Environ Sci Pollut Res Int 21:10787–10802. doi:10.1007/s11356-014-3029-y
Kim B-S, Oh H-M, Kang H et al (2004) Remarkable bacterial diversity in the tidal flat sediment as revealed by 16S rDNA analysis. J Microbiol Biotechnol 14:205–211
Kjellerup BV, Paul P, Ghosh U, et al (2012) Spatial distribution of PCB dechlorinating bacteria and activities in contaminated soil. Appl Environ Soil Sci
Köpke B, Wilms R, Engelen B et al (2005) Microbial diversity in coastal subsurface sediments: a cultivation approach using various electron acceptors and substrate gradients. Appl Environ Microbiol 71:7819–7830
Larose C, Prestat E, Cecillon S et al (2013) Interactions between snow chemistry, mercury inputs and microbial population dynamics in an arctic snowpack. PLoS One 8, e79972
Le Cloarec M-F, Bonte PH, Lestel L et al (2011) Sedimentary record of metal contamination in the Seine River during the last century. Phys Chem Earth Parts ABC 36:515–529
Leloup J, Fossing H, Kohls K et al (2009) Sulfate-reducing bacteria in marine sediment (Aarhus Bay, Denmark): abundance and diversity related to geochemical zonation. Environ Microbiol 11:1278–1291
Lesourd S, Lesueur P, Brun-Cottan JC et al (2003) Seasonal variations in the characteristics of superficial sediments in a macrotidal estuary (the Seine inlet, France). Estuar Coast Shelf Sci 58:3–16
Li C-H, Zhou H-W, Wong Y-S, Tam NF-Y (2009) Vertical distribution and anaerobic biodegradation of polycyclic aromatic hydrocarbons in mangrove sediments in Hong Kong, South China. Sci Total Environ 407:5772–5779
Liu M, Baugh PJ, Hutchinson SM et al (2000) Historical record and sources of polycyclic aromatic hydrocarbons in core sediments from the Yangtze Estuary, China. Environ Pollut 110:357–365
Looper JK, Cotto A, Kim B-Y et al (2013) Microbial community analysis of Deepwater Horizon oil-spill impacted sites along the Gulf coast using functional and phylogenetic markers. Environ Sci Process Impacts 15:2068–2079
Mai H, Cachot J, Brune J et al (2012) Embryotoxic and genotoxic effects of heavy metals and pesticides on early life stages of Pacific oyster (Crassostrea gigas). Mar Pollut Bull 64:2663–2670
Marchesi JR, Sato T, Weightman AJ, et al (1998) Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl Environ Microbiol 64:795–799
Meybeck M, Lestel L, Bonté P et al (2007) Historical perspective of heavy metals contamination (Cd, Cr, Cu, Hg, Pb, Zn) in the Seine River basin (France) following a DPSIR approach (1950–2005). Sci Total Environ 375:204–231
Mills HJ, Martinez RJ, Story S, Sobecky PA (2005) Characterization of microbial community structure in Gulf of Mexico gas hydrates: comparative analysis of DNA-and RNA-derived clone libraries. Appl Environ Microbiol 71:3235–3247
Minier C, Abarnou A, Jaouen‐Madoulet A et al (2006) A pollution‐monitoring pilot study involving contaminant and biomarker measurements in the Seine Estuary, France, using zebra mussels (Dreissena polymorpha). Environ Toxicol Chem 25:112–119
Motelay-Massei A, Ollivon D, Garban B, Chevreuil M (2002) Atmospheric deposition of toxics onto the Seine Estuary, France: example of polycyclic aromatic hydrocarbons. Atmospheric Chem Phys Discuss 2:1351–1369
Motelay-Massei A, Ollivon D, Garban B et al (2004) Distribution and spatial trends of PAHs and PCBs in soils in the Seine River basin, France. Chemosphere 55:555–565
Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700
Niepceron M, Portet‐Koltalo F, Merlin C et al (2010) Both Cycloclasticus spp. and Pseudomonas spp. as PAH‐degrading bacteria in the Seine estuary (France). FEMS Microbiol Ecol 71:137–147
Nogales B, Moore ER, Llobet-Brossa E et al (2001) Combined use of 16S ribosomal DNA and 16S rRNA to study the bacterial community of polychlorinated biphenyl-polluted soil. Appl Environ Microbiol 67:1874–1884
Nomura M, Gourse R, Baughman G (1984) Regulation of the synthesis of ribosomes and ribosomal components. Annu Rev Biochem 53:75–117
Oger C, Berthe T, Quillet L et al (2001) Estimation of the abundance of the cadmium resistance gene cadA in microbial communities in polluted estuary water. Res Microbiol 152:671–678
Peng A, Liu J, Gao Y, Chen Z (2013) Distribution of endophytic bacteria in Alopecurus aequalis sobol and Oxalis corniculata L. from soils contaminated by polycyclic aromatic hydrocarbons. PLoS One 8, e83054
Plassart P, Akpa Vinceslas M, Gangneux C et al (2008) Molecular and functional responses of soil microbial communities under grassland restoration. Agric Ecosyst Environ 127:286–293
Pratt B, Riesen R, Johnston CG (2012) PLFA analyses of microbial communities associated with PAH-contaminated riverbank sediment. Microb Ecol 64:680–691
Ramond J-B, Berthe T, Lafite R et al (2008) Relationships between hydrosedimentary processes and occurrence of mercury-resistant bacteria (merA) in estuary mudflats (Seine, France). Mar Pollut Bull 56:1168–1176
Rasmussen LD, Sørensen SJ (2001) Effects of mercury contamination on the culturable heterotrophic, functional and genetic diversity of the bacterial community in soil. FEMS Microbiol Ecol 36:1–9
Rocchetti L, Beolchini F, Hallberg KB et al (2012) Effects of prokaryotic diversity changes on hydrocarbon degradation rates and metal partitioning during bioremediation of contaminated anoxic marine sediments. Mar Pollut Bull 64:1688–1698
Savage KN, Krumholz LR, Gieg LM et al (2010) Biodegradation of low‐molecular‐weight alkanes under mesophilic, sulfate‐reducing conditions: metabolic intermediates and community patterns. FEMS Microbiol Ecol 72:485–495
Silby MW, Cerdeño-Tárraga AM, Vernikos GS et al (2009) Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens. Genome Biol 10:R51
Srivastava P, Kowshik M (2013) Mechanisms of metal resistance and homeostasis in haloarchaea. Archaea
Takai K, Horikoshi K (2000) Rapid detection and quantification of members of the archaeal community by quantitative PCR using fluorogenic probes. Appl Environ Microbiol 66:5066–5072
Toes A-CM, Finke N, Kuenen JG, Muyzer G (2008) Effects of deposition of heavy-metal-polluted harbor mud on microbial diversity and metal resistance in sandy marine sediments. Arch Environ Contam Toxicol 55:372–385
Vaalgamaa S, Conley DJ (2008) Detecting environmental change in estuaries: nutrient and heavy metal distributions in sediment cores in estuaries from the Gulf of Finland, Baltic Sea. Estuar Coast Shelf Sci 76:45–56
Van Ael E, Covaci A, Blust R, Bervoets L (2012) Persistent organic pollutants in the Scheldt estuary: environmental distribution and bioaccumulation. Environ Int 48:17–27
Van der Oost R, Beyer J, Vermeulen NP (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149
Verrhiest GJ, Clement B, Volat B et al (2002) Interactions between a polycyclic aromatic hydrocarbon mixture and the microbial communities in a natural freshwater sediment. Chemosphere 46:187–196
Vicquelin L, Leray-Forget J, Peluhet L et al (2011) A new spiked sediment assay using embryos of the Japanese medaka specifically designed for a reliable toxicity assessment of hydrophobic chemicals. Aquat Toxicol 105:235–245
Voorspoels S, Covaci A, Maervoet J, Schepens P (2004) PBDEs in marine and freshwater sediments from Belgium: levels, profiles and relations with biota. J Environ Monit 6:914–918
Vrel A, Boust D, Lesueur P et al (2013) Dating of sediment record at two contrasting sites of the Seine River using radioactivity data and hydrological time series. J Environ Radioact 126:20–31. doi:10.1016/j.jenvrad.2013.06.005
Wang Y, Wu Y, Pi N, Tam NF (2014) Investigation of microbial community structure in constructed mangrove microcosms receiving wastewater-borne polycyclic aromatic hydrocarbons (PAHs) and polybrominated diphenyl ethers (PBDEs). Environ Pollut 187:136–144
Wilms R, Sass H, Köpke B et al (2006) Specific bacterial, archaeal, and eukaryotic communities in tidal-flat sediments along a vertical profile of several meters. Appl Environ Microbiol 72:2756–2764
Wu G, Kechavarzi C, Li X et al (2013) Influence of mature compost amendment on total and bioavailable polycyclic aromatic hydrocarbons in contaminated soils. Chemosphere 90:2240–2246
Yakimov MM, Denaro R, Genovese M et al (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
Yan T, LaPara TM, Novak PJ (2006) The reductive dechlorination of 2,3,4,5‐tetrachlorobiphenyl in three different sediment cultures: evidence for the involvement of phylogenetically similar Dehalococcoides‐like bacterial populations. FEMS Microbiol Ecol 55:248–261
Yen JH, Liao WC, Chen WC, Wang YS (2009) Interaction of polybrominated diphenyl ethers (PBDEs) with anaerobic mixed bacterial cultures isolated from river sediment. J Hazard Mater 165:518–524
Zegers BN, Lewis WE, Booij K et al (2003) Levels of polybrominated diphenyl ether flame retardants in sediment cores from Western Europe. Environ Sci Technol 37:3803–3807
Zhang H, Kallimanis A, Koukkou AI, Drainas C (2004) Isolation and characterization of novel bacteria degrading polycyclic aromatic hydrocarbons from polluted Greek soils. Appl Microbiol Biotechnol 65:124–131
Zhang D-C, Mörtelmaier C, Margesin R (2012) Characterization of the bacterial archaeal diversity in hydrocarbon-contaminated soil. Sci Total Environ 421:184–196
Acknowledgments
This work was supported by the Seine-Aval scientific research program. The first author holds a research grant from the Haute-Normandie Regional council.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Philippe Garrigues
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOCX 42580 kb)
Rights and permissions
About this article
Cite this article
Kaci, A., Petit, F., Fournier, M. et al. Diversity of active microbial communities subjected to long-term exposure to chemical contaminants along a 40-year-old sediment core. Environ Sci Pollut Res 23, 4095–4110 (2016). https://doi.org/10.1007/s11356-015-4506-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-015-4506-7


