Elsevier

Chemosphere

Volume 144, February 2016, Pages 1060-1073
Chemosphere

Consequences of contaminant mixture on the dynamics and functional diversity of bacterioplankton in a southwestern Mediterranean coastal ecosystem

https://doi.org/10.1016/j.chemosphere.2015.09.093Get rights and content

Highlights

  • Bacterioplankton was exposed to pollutant mixture created from sediment resuspension.

  • Strong enrichment in metals, herbicides, DOC and nutrients were observed.

  • Bacterial abundance and activities were inhibited by metals and herbicides.

  • Nutrients and DOC modified the inhibitory effects of metals and herbicides.

  • Inhibitory effects were more marked in offshore waters than in lagoon waters.

Abstract

Contamination of coastal environments is often due to a complex mixture of pollutants, sometimes in trace levels, that may have significant effects on diversity and function of organisms. The aim of this study was to evaluate the short-term dynamics of bacterioplankton exposed to natural and artificial mixtures of contaminants. Bacterial communities from a southwestern Mediterranean ecosystem, lagoon and the bay (offshore) of Bizerte were exposed to i) elutriate from resuspension of contaminated sediment, and ii) an artificial mixture of metals and herbicides mimicking the contamination observed during sediment resuspension. Elutriate incubation as well as artificial spiking induced strong enrichments in nutrients (up to 18 times), metals (up to six times) and herbicides (up to 20 times) relative to the in situ concentrations in the offshore station, whereas the increases in contaminants were less marked in the lagoon station. In the offshore waters, the artificial mixture of pollutants provoked a strong inhibition of bacterial abundance, production and respiration and significant modifications of the potential functional diversity of bacterioplankton with a strong decrease of the carbohydrate utilization. In contrast, incubation with elutriate resulted in a stimulation of bacterial activities and abundances, suggesting that the toxic effects of pollutants were modified by the increase in nutrient and DOM concentrations due to the sediment resuspension. The effects of elutriate and the artificial mixture of pollutants on bacterial dynamics and the functional diversity were less marked in the lagoon waters, than in offshore waters, suggesting a relative tolerance of lagoon bacteria against contaminants.

Introduction

It is now well recognized that the risk of environmental contamination by chemical pollutants is particularly high in coastal waters (Simonich and Hites, 1995, Schwarzenbach et al., 2006) where demographic increases are amplifying the pressures in these ecosystems (James, 2002, Small and Nicholls, 2003). Most of the studies aiming to assess the consequences of contamination on marine model organisms have used artificial poisoning with toxic compounds added individually or in mixture. Particular attention is generally focused on simulating the in situ conditions observed in the polluted ecosystems as much as possible. Nevertheless, it is a great challenge to experimentally reproduce the contamination of a polluted ecosystem in experimental conditions. The contamination is rarely due to only one compound but is rather caused by a train of several pollutants, sometimes in trace levels, which may have significant effects on diversity and function (Roberts, 2012). When a contaminant is observed in the presence of other pollutants the effects can be additive, the toxicity of one being increased by the presence of another contaminant (Franklin et al., 2002). The effects can also be antagonists (Sharma et al., 1999) with the toxicity of a given element being reduced by the presence of another contaminant. For example, complex organic molecules such as polycyclic aromatic hydrocarbons (PAHs) may promote adsorption of other pollutants (e.g. metals) thereby reducing their bioavailability and hence their toxicity (Lorenzo et al., 2002). Finally, the toxicity of a contaminant may also be modified depending on environmental conditions; solar radiation, particularly ultraviolet (UV) radiation, can increase the toxicity of PAH compounds by production of secondary metabolites (Ankley et al., 1994, Woo et al., 2009). Therefore, to estimate consequences of contaminants on biological models it is necessary to consider the contamination in its entirety in order to better simulate the conditions of exposure to contaminants encountered by organisms in polluted environments (Echeveste et al., 2010). Recently, Lafabrie et al. (2013a) have observed important changes in marine phytoplankton community structure following the contamination by a natural mixture of low dose metals and PAHs with a negative impact on cyanobacteria while nanophytoplankton benefits from the reduction of cyanobacteria abundance. In contrast, Nayar et al. (2004) demonstrated that bacterioplankton can be stimulated by the release of heavy metals from sediment with an increase in abundance and production. Similarly, Rochelle-Newall et al. (2008b) have observed that a moderate Zn pollution (5 µg L−1) resulted in a shift in the balance between autotrophic production and respiration, further pushing the system towards being a carbon source rather than a sink to the atmosphere. The stimulation of heterotrophic compartment, to the detriment of phytoplankton, has major consequences on the carbon cycle by enhancing the supply of CO2 into the atmosphere (Cotner, 2000). In addition, the impact of contamination on the carbon cycle in coastal ecosystems might also be observed qualitatively with modification in the metabolism of carbon compounds by heterotrophic bacterial affecting the functional diversity of the ecosystem (Sura et al., 2012). The response to contamination depends on the adaptation mechanisms that microorganisms can develop to survive pollution according to the PICT (pollution induced-community tolerance) concept (Blanck et al., 1988). Tolerance of a toxicant can increase by three ways; physiological adaptation also known as the phenotypic plasticity of an individual, tolerant genotypes selected within a population over time, and the replacement of species with more tolerant ones within a community. These mechanisms of adaptation can be triggered by the chemical environment of the microorganisms; exposure of a community to a toxicant above its effect threshold exerts a selection pressure on sensitive species or individuals leading to their exclusion and their replacement by tolerant species. Pollution effects on functional diversity and dynamics of bacteria are largely documented in soils (e.g. Baath et al., 1998, Engelen et al., 1998, Yao et al., 2003) and freshwater ecosystems (Tiquia, 2010, Leboulanger et al., 2011), while coastal marine environments have received less attention.

The aim of this study was to assess the consequences of a complex mixture of contaminants on the dynamics and the functional diversity of bacterioplankton in a coastal southwestern Mediterranean ecosystem. For that purpose, bacterioplankton communities were incubated in microcosms for 96 h, with contaminated water obtained after resuspension of polluted sediments. Two contrasting sites, an offshore site and a lagoon site, were investigated in order to test the hypothesis that bacterial response to contamination would be different between the two sampling sites considering the possible selective pressure and the adaptation that can be triggered by the chemical environment.

Section snippets

Study sites and sampling

The study was conducted in April 2014 in southwestern Mediterranean ecosystems, lagoon and the bay of Bizerte (Fig. S1, Supplementary material). Like many Mediterranean coastal lagoons, Bizerte lagoon (Tunisia) is a polluted ecosystem subject to agriculture, urbanization and industrialization (cement works, metallurgical industry, boatyard, tire production factories) pressures, and pressures from naval and commercial shipping harbors. Runoff and discharges of urban, agricultural and industrial

Contamination level

Sediment of the Bizerte channel was clearly contaminated with heavy metals and PAHs (Table S2, Supplementary Material). The most abundant metals were Zn, Cr and Pb (228 µg g−1, 85 µg g−1 and 70 µg g−1, respectively) whereas for PAHs the highest concentrations were measured for benzo(b)fluoranthene, pyrene and fluoranthene (772 ng g−1, 696 ng g−1 and 677 ng g−1, respectively). Except for Cd, which exhibited concentrations below the “Effects Range Low” (ERL) values, all metal concentrations were

Contamination level of elutriate

In marine ecosystems, contaminants accumulate within sediments where they can impact benthic communities (Long et al., 1995). While sediments have traditionally been viewed as a sink for contaminants in marine ecosystems, they can also act as a source of contaminants when they are disturbed, moved or relocated (Latimer et al., 1999). Sediment resuspension can result in severe ecological consequences in shallow water habitats depending on i) the contamination level of the sediment and ii) the

Conclusion

Contaminated sediments represent a source of toxic chemicals that can potentially impact the functioning and the diversity of pelagic communities during hydrodynamic events. The results of this study showed that sediment resuspension provoked the release of a train of contaminants in concentrations that may alter the dynamics and the function of the bacterioplankton. However, this train of contaminants was accompanied by high concentrations in nutrients and DOM that modify the toxic effects of

Acknowledgments

This study was supported by the RISCO project which was funded by the French National Agency for Research (ANR-13-CESA-0001). This study was conducted as a part of the MERMEX-WP3/MISTRALS project and is a contribution to the international SOLAS LOICZ program. The English grammar and syntax of the manuscript have been revised by Proof-Reading-Service.com.

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