Abstract
In order to estimate how pollution affects the bacterial community structure and composition of sediments, chemical and molecular approaches were combined to investigate eight stations around the Bizerte lagoon. Terminal restriction fragment length polymorphism (T-RFLP) analysis of PCR-amplified 16S rRNA genes revealed that each station was characterized by a specific bacterial community structure. The combination of this data with those of chemical analysis showed a correlation between the bacterial fingerprint and the pollutant content, principally with hydrocarbon pollution. The composition of the bacterial community of two contrasted stations related to the pollution revealed sequences affiliated to α, β, γ, δ, ε subclass of the Proteobacteria, Actinobacteria, and Acidobacteria in both stations although in different extent. Gamma and delta subclass of the Proteobacteria were dominant and represent 70% of clones in the heavy-metal-contaminated station and 47% in the polyaromatic hydrocarbon (PAH)-contaminated. Nevertheless, most of the sequences found were unaffiliated to cultured bacteria. The adaptation of the bacterial community mainly to PAH compounds demonstrated here and the fact that these bacterial communities are mainly unknown suggest that the Bizerte lagoon is an interesting environment to understand the capacity of bacteria to cope with some pollutants.
Similar content being viewed by others
References
Abulencia CB, Wyborski DL, Garcia JA, Podar M, Chen W, Chang SH, Chang HW, Watson D, Brodie EL, Hazen TC, Keller M (2006) Environmental whole-genome amplification to access microbial populations in contaminated sediments. Appl Environ Microbiol 72:3291–3301
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Asami H, Aida M, Watanabe K (2005) Accelerated sulfur cycle in coastal marine sediment beneath areas of intensive shellfish aquaculture. Appl Environ Microbiol 71:2925–2933
Ben Said O, Goñi-Urriza MS, El Bour M, Dellali M, Aissa P, Duran R (2008) Characterization of aerobic polyaromatic hydrocarbon-degrading bacteria from Bizerte lagoon sediments, Tunisia. J Appl Microbiol 104:987–997
Bissett A, Bowman J, Burke C (2006) Bacterial diversity in organically-enriched fish farm sediments. FEMS Microbiol Ecol 55:48–56
Bordenave S, Fourçans A, Blanchard S, Goñi-Urriza MS, Caumette P, Duran R (2004) Structure and fonctional analyses of bacterial communities changes in microbial mats following petroleum exposure. Ophelia 58:195–203
Bordenave S, Goñi-Urriza MS, Caumette P, Duran R (2007) Effects of heavy fuel oil on the bacterial community structure of a pristine microbial mat. Appl Environ Microbiol 73:6089–6097
Bowman JP, Mccuaig RD (2003) Biodiversity, community structural shifts, and biogeography of prokaryotes within antarctic continental shelf sediment. Appl Environ Microbiol 69:2463–2483
Brown MV, Bowman JP (2001) A molecular phylogenetic survey of sea-ice microbial communities (SIMCO). FEMS Microbiol Ecol 35:267–275
Cao Y, Cherr GN, Córdova-Kreylos AL, Fan TWM, Green PG, Higashi RM, LaMontagne MG, Scow KM, Vines CA, Yuan J, Holden PA (2006) Relationships between sediment microbial communities and pollutants in two California Salt Marshes. FEMS Microbiol Ecol 52:619–633
Córdova-Kreylos AL, Cao Y, Green PG, Hwang HM, Kuivila KM, LaMontagne MG, Van De Werfhorst LC, Holden PA, Scow KM (2006) Diversity, composition, and geographical distribution of microbial communities in California Salt Marsh Sediments. Appl Environ Microbiol 72:3357–3366
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
Ford T, Ryan D (1995) Toxic metals in aquatic ecosystems: a microbiological perspective. Environ Health Perspect 103:25–28
Fourçans A, Solé A, Diestra E, Ranchou-Peyruse A, Esteve I, Caumette P, Duran R (2006) Vertical migrations of phototrophic bacterial populations in a hypersaline microbial mat from Salins-de-Giraud (Camargue, France). FEMS Microbiol Ecol 57:367–377
Gillan DC, Pernet P (2007) Adherent bacteria in heavy metal contaminated marine sediments. Biofouling 23:1–13
Goñi-Urriza MS, Point D, Amouroux D, Guyoneaud R, Donard OFX, Caumette P, Duran R (2007) Bacterial community structure along the Adour estuary (French Atlantic coast): influence of salinity gradient versus metal contamination. Aquat Microb Ecol 49:47–56
Heijs SK, Damsté JS, Forney LJ (2005) Characterization of a deep-sea microbial mat from an active cold seep at the Milano mud volcano in the Eastern Mediterranean Sea. FEMS Microbiol Ecol 54:47–56
Hernández-Raquet G, Budzinski H, Caumette P, Dabert P, Le Ménach K, Muyzer G, Duran R (2006) Molecular diversity studies of bacterial communities of oil polluted microbial mats from the Etang de Berre (France). FEMS Microbiol Ecol 58:550–562
Hewson I, Fuhrman JA (2004) Richness and diveristy of bacterioplankton along an estuarine gradient in Moreton Bay, Australia. Appl Environ Microbiol 70:3425–3433
Hunter EM, Mills HJ, Kostka JE (2006) Microbial community diversity associated with carbon and nitrogen cycling in permeable shelf sediments. Appl Environ Microbiol 72:5689–5701
Inagaki F, Suzuki M, Takai K, Oida Sakamoto T, Aoki K, Nealson KH, Horikoshi K (2003) Microbial communities associated with geological horizons in coastal subseafloor sediments from the sea of Okhotsk. Appl Environ Microbiol 69:7224–7235
Jiang SC, Paul JH (1996) Occurrence of lysogenic bacteria in marine microbial communities as determined by prophage induction. Mar Ecol Prog Ser 142:27–38
Kasai Y, Kishira H, Syutsubo K, Harayama S (2001) Molecular detection of marine bacterial populations on beaches contaminated by the Nakhodka tanker oil-spill accident. Environ Microbiol 3:246–255
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary gnenetics analysis and sequence alignement. Brief Bioinform 5:1907–1919
Lane DJ (1991) rRNA sequencing. In: Stachenbradt E, Goodfellow M (eds) Nucleic acid 527 techniques in bacterial systematics. Wiley, Chichester, pp 115–175
Li B, Zhang T, Xu Z, Fang HHP (2009) Rapid analysis of 21 antibiotics of multiple classes in municipal wastewater using ultra performance liquid chromatography-tandem mass spectrometry. Anal Chiml Acta 645(1–2):64–72
Lopez-Garcia P, Duperron S, Philippot P, Foriel J, Susini J, Moreira (2003) Bacterial diversity in hydrothermal sediment and epsilonproteobacterial dominance in experimental microcolonizers at the Mid-Atlantic Ridge. Environ Microbiol 5:961–976
Macnaughton SJ, Stephen JR, Venosa AD, Davis GA, Chang YJ, White DC (1999) Microbial population changes during bioremediation of an experimental oil spill. Appl Environ Microbiol 65:95–101
Maidak BL, Cole JR, Lilburn TG, CT P Jr, Saxman PR, Farris RJ, Garrity GM, Olsen GJ, Schmidt TM, Tiedje JM (2001) The RDP-II (Ribosomal Database Project). Nucleic Acids Res 29:173–174
Mills HJ, Hodges C, Wilson K, MacDonald IR, Sobecky PA (2003) Microbial diversity in sediments associated with surface-breaching gas hydrate mounds in the Gulf of Mexico. FEMS Microbiol Ecol 46:39–52
Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in naturel waters. Anal Chim Acta 27:31–36
Nakatsu CH, Carmosini N, Baldwin B, Beasley F, Kourtev P, Konopka A (2005) Soil microbial community responses to additions of organic carbon substrates and heavy metals (Pb and Cr). Appl Environ Microbiol 71:7679–7689
NF EN ISO 11885 (1998) Water quality-determination of 33 elements by inductively coupled plasma atomic emission spectroscopy. AFNOR, Paris
Païssé S, Coulon F, Goñi-Urriza MS, Peperzak LJ, McGenity T, Duran R (2008) Structure of bacterial communities along a hydrocarbon contamination gradient in a coastal sediment. FEMS Microbiol Ecol 66:295–305
Precigou S, Goulas P, Duran R (2001) Rapid and specific identification of nitrile hydratase (NHase)-encoding genes in soil samples by polymerase chain reaction. FEMS Microbiol Lett 204:155–161
Richards FA, Thompson TG (1952) The estimation and characterization of plankton populations by analysis. 2- a spectrophotometric method for the estimation of plankton pigment. J Mar Res 11:156–172
Röling 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
Saitou N, Nei M (1987) The neighbour-joining method: a new method for reconstructing phylogenetics trees. Mol Biol Evol 4:406–425
Singleton DR, Furlong MA, Rathbun SL, Whitman WB (2001) Quantitative comparisons of 16S rDNA sequence libraries from environmental samples. Appl Environ Microbiol 67:4373–4376
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX-Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Vrionis HA, Anderson RT, Ortiz-Bernad I, O’Neill KR, Resch CT, Peacock AD, Dayvault R, White DC, Long PE, Lovley DR (2005) Microbiological and geochemical heterogeneity in an in situ uranium bioremediation field site. Appl Environ Microbiol 71:6308–6318
Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703
Yan T, Fields MW, Wu L, Zu Y, Tiedje JM, Zhou J (2003) Molecular diversity and characterization of nitrite reductase gene fragments (nirK and nirS) from nitrate- and uranium-contaminated groundwater. Environ Microbiol 5:13–24
Yoshida M, Hamdi H, Abdulnasser I, Jedidi N (2002) Contamination of potentially toxic elements (PTEs) in Bizerte lagoon bottom sediments, surface sediment and sediment repository. In: Ghrabi A, Yoshida M (eds) Study on environmental pollution of Bizerte lagoon. INRST-JICA, Tunis, p 139
Zhang W, Ki JS, Qian PY (2008) Microbial diversity in polluted harbor sediments I: bacterial community assessment based on four clone libraries of 16S rDNA. Estuar Coast Shelf Sci 76:668–681
Acknowledgments
This research was supported by the Tunisian “Ministère de la Recherche Scientifique, de la Technologie et du Developpement des Competences” (MRSTDC). We acknowledge the financial support of the Conseil Régional d’Aquitaine and the Conseil Général des Pyrénées Atlantiques. Sequencing experiments presented in the present publication were performed at the Genotyping and Sequencing facility of Bordeaux (grants from the Aquitaine Regional Government Council no. 20030304002FA and 20040305003FA and from the European Union, FEDER no. 2003227).
Author information
Authors and Affiliations
Corresponding author
Electronic Supplementary Material
Below is the link to the electronic supplementary material.
Table 1 supplementary data
Polyaromatic hydrocarbon composition of the Bizerte lagoon sediments (DOC 161 kb)
Table 2 supplementary data
Heavy metal composition of the Bizerte lagoon sediments (DOC 144 kb)
Figure 1 supplementary data
Canonical correspondence analysis (CCA) between sediment bacterial communities characterized by T-RFLP fingerprints and some physical–chemical parameters: suspended matter (SM), dissolved oxygen (O 2 ), nitrates (NO 3 ), phosphates (PO 4 ), Salinity, total PAHs, and total heavy metals. T-RFs (in base pairs) are represented (DOC 252 kb)
Figure 2 supplementary data
Canonical correspondence analysis (CCA) between sediment bacterial communities characterized by T-RFLP fingerprints and individual PAH concentrations. All stations are represented in the insert figure. T-RFs (in base pairs) are represented. Station 1 is not considered for this analysis. N Naphthalene; ANY Acenaphtylene; ANA Acenaphtene; F Fluorine; P Phenanthrene; A Anthracene; FL Fluoranthene; PY Pyrene; C Chrysene; BA Benzo(a)anthracene; BBF+BkF Benzo[b+k]fluoranthene; BAP Benzo(a)pyrene; IN Indeno(1,2,3-)pyrene; DBA Dibenzo(a,h)anthracène; BPE Benzo(g,h,i)perylene (DOC 183 kb)
Rights and permissions
About this article
Cite this article
Ben Said, O., Goñi-Urriza, M., El Bour, M. et al. Bacterial Community Structure of Sediments of the Bizerte Lagoon (Tunisia), a Southern Mediterranean Coastal Anthropized Lagoon. Microb Ecol 59, 445–456 (2010). https://doi.org/10.1007/s00248-009-9585-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-009-9585-x