Benzo(a)pyrene inhibits the role of the bioturbator Tubifex tubifex in river sediment biogeochemistry

Abstract

The interactions between invertebrates and micro-organisms living in streambed sediments often play key roles in the regulation of nutrient and organic matter fluxes in aquatic ecosystems. However, benthic sediments also constitute a privileged compartment for the accumulation of persistent organic pollutants such as PAHs or PCBs that may affect the diversity, abundance and activity of benthic organisms. The objective of this study was to quantify the impact of sediment contamination with the PAH benzo(a)pyrene on the interaction between micro-organisms and the tubificid worm, Tubifex tubifex, which has been recognized as a major bioturbator in freshwater sediments. Sedimentary microcosms (slow filtration columns) contaminated or not with benzo(a)pyrene (3 tested concentrations: 0, 1 and 5 mg kg(-1)) at the sediment surface were incubated under laboratory conditions in the presence (100 individuals) or absence of T. tubifex. Although the surface sediment contaminations with 1 mg kg(-1) and 5 mg kg(-1) of benzo(a)pyrene did not affect tubificid worm survival, these contaminations significantly influenced the role played by T. tubifex in biogeochemical processes. Indeed, tubificid worms stimulated aerobic respiration, denitrification, dehydrogenase and hydrolytic activities of micro-organisms in uncontaminated sediments whereas such effects were inhibited in sediments polluted with benzo(a)pyrene. This inhibition was due to contaminant-induced changes in bioturbation (and especially bio-irrigation) activities of worms and their resulting effects on microbial processes. This study reveals the importance of sublethal concentrations of a contaminant on ecological processes in river sediments through affecting bioturbator-microbe interactions. Since they affect microbial processes involved in water purification processes, such impacts of sublethal concentrations of pollutants should be more often considered in ecosystem health assessment.

Legacy effects on sediments in river corridors

“…As with other contaminants, biotic interactions with sediments can influence the form and distribution of PAHs in rivers. Mermillod-Blondin et al (2013), for example, document how lower concentrations of the PAH benzo(a)pyrene do not limit the survival of a tubifex worm that bioturbates river sediment, but the PAH does inhibit worm activity and the associated microbial processes that reduce contaminant concentrations.…”

“…Biotic activities can also alter the distribution of contaminants via processes such as bioturbation or the chemical form of the contaminant via processes such as microbial reactions (Mermillod-Blondin et al, 2013).…”

Structure of hydrocarbonoclastic nitrate-reducing bacterial communities in bioturbated coastal marine sediments

“…Oxygen inhibits enzymes involved on denitrification but also stimulates sedimentary nitrification that usually provides the major source of nitrate for denitrification (Herbert, ). Bioturbation can promote microbial activities (Kogure and Wada, ; Satoh et al ., ; Mermillod‐Blondin et al ., ) and modify microbial communities structures (Laverock et al ., ) associated with different aerobic processes and anaerobic organic matter degradation (Berthe‐Corti and Höpner, ; Grossi et al ., ; Papaspyrou et al ., ) as also demonstrated by 16S rRNA gene‐based studies in hydrocarbon‐, oil‐ or pesticide‐contaminated sediments (Cuny et al ., ; Monard et al ., ). To the best of our knowledge, only one study revealed the concomitant effect of oil and bioturbation (Gilbert et al ., ).…”

Effects of flatworm predators on sediment communities and ecosystem functions: a microcosm approach

“…Many marine species rework sediment and thus play a key role in benthic ecosystems by shaping local geochemical gradients and resource distribution (e.g., Aller, 1982;Solan et al, 2004;Meysman et al, 2006). By contrast, in freshwaters, the bioturbation ability of only a few species or taxonomic groups, including tubificids, chironomids, and clams, has been investigated (Fisher et al, 1980;Matisoff & Xiaosong, 1998;Ciutat et al, 2005;Stief & de Beer, 2006;Lagauzère et al, 2009;Mermillod-Blondin et al, 2013;Majdi et al, 2014a). Yet, the recent work of De Nadaï- Monoury et al (2013Monoury et al ( , 2014 has provided a wider overview of bioturbator diversity in freshwater ecosystems.…”