Relative importance of macrofaunal burrows for the microbial mineralization of pyrene in marine sediments: impact of macrofaunal species and organic matter quality

Abstract

The significance of macrofaunal burrows for microbial organic matter mineralization is well recognized. However, despite the importance of marine sediments as main sinks for organic particle-reactive contaminants such as polyaromatic hydrocarbons (PAHs), the significance of biogenic structures for microbial pollutant mineralization is largely unknown. We measured microbial mineralization of the PAH pyrene in different sediment compartments (surface, burrow and reduced bulk sediments) as a function of contamination history (uncontaminated and pyrene-exposed), macrofaunal species (Amphiura filiformis and Nereis diversicolor) and sediment organic matter quality (labile Tetraselmis sp. and refractory lignin). Sediments were exposed to combinations of the 3 factors for 43 d, after which sediment samples from the 3 compartments were incubated for radio-respirometric measurements in 14 C-pyrene-coated flasks to monitor 14 CO 2 production (i.e. pyrene mineralization) for 128 d. Pyrene exposure enhanced microbial pyrene mineralization (MPM) rates by an order of magnitude in all compartments, signifying MPM as inducible. MPM rates increased successively from reduced bulk to burrow and surface sediments in uncontaminated treatments, while MPM rates were highest in burrows when exposed to pyrene. This emphasizes the oxygen dependence of MPM and pinpoints burrows as MPM hot spots. Enrichment with labile organic matter doubled MPM rates in pyrene-exposed surface sediment, likely fertilizing MPM where oxygen is readily available. Burrow sediment MPM rates were doubled with A. filiformis, suggesting species-specific stimulation of the microbial community within the burrows. In conclusion, burrow sediment appears to be at least as important as surface sediment for microbial PAH degradation in marine sediments. Furthermore, macrofaunal biodiversity, sedimentation events and the trophic state of the system should be taken into account when the fate and effects of organic contaminants are assessed in marine systems.

Effects of sediment organic matter quality on bioaccumulation, degradation, and distribution of pyrene in two macrofaunal species and their surrounding sediment

“…Its fate is therefore also determined by metabolization and mineraliz ation processes, and degradation product may subsequently be eliminated from burrow sediment with exhaust water facilitated by macrofaunal irrigation. Granberg et al (2005) found microbial pyrene mineralization rates to be 1.5-2.5 times higher in A. filiformis burrows compared to N. diversicolor burrows.…”

“…irrigation and particle mixing) is therefore an important process affecting sedimentary PAH degradation through the oxygenation of deeper sediment layers, and through the transport of contaminated particles between oxic and reduced layers (Gardner, Frez, Cichocki & Parrish, 1985, Bauer, Kerr, Bautista, Decker & Capone, 1988, Holmer, Forbes & Forbes, 1997, Kure & Forbes, 1997. and Granberg et al (2005) furthermore stress the importance of species specific bioturbation patterns for observed differences in microbial degradation and mineralization of pyrene in sediments. Although sparsely investigated, other factors suggested to affect sedimentary microbial PAH degradation are repeated PAH exposure and altered sediment organic matter (SOM) quantity and quality (ZoBell, 1946, Bauer & Capone, 1985, Cerniglia & Heitkamp, 1989.…”

“…Since sedimenting organic matter constitutes an important food source and substrate for benthic macro -and microorganisms, seasonal variations in its quantity and quality affects organism growth, production, metabolism and activity (Smetacek, 1980, Christensen & Kanneworff, 1985, Graf, 1992, Gremare, Amouroux, Charles, Dinet, RiauxGobin, Baudart et al, 1997, Granberg, Hansen & Selck, 2005. Such physiological response due to changes in food value is likely also to affect the absorption, metabolism and general fate of sediment associated contaminants.…”

Meiofauna reduces bacterial mineralization of naphthalene in marine sediment

“…These metabolites have in turn been shown to be difficult to use for PAHdegrading bacteria, thereby inhibiting mineralization rather than promoting it (Giessing and Johnsen, 2005). Despite this, the presence of fauna, such as polychaetes, is known to increase PAH mineralization (Gardner et al, 1979;Bauer et al, 1988;Granberg et al, 2005) through increased oxygen and nutrient fluxes due to bioturbation. Such stimulatory effects from fauna are likely to have occurred in all treatments, as meiofauna also is known to increase oxygen fluxes (Aller and Aller, 1992) Anaerobic mineralization of PAHs can also occur in sediments (Coates et al, 1997), although it is not likely to be important in this study due to the fact that the majority of the remaining 14 C in the sediment was present in the top centimeter of the sediment (average 78%, data not shown), and that the water column was continuously aerated.…”

Effects of the polychaetes Arenicola marina and Nereis diversicolor on microbial pyrene mineralization

“…Irrigated burrows often show enhanced activity of biogeochemical processes (Kristensen et al 1985, Mayer et al 1995, Papaspyrou et al 2006) and both bacteria and meiofauna are often more abundant in burrows and tubes compared with the surrounding sediment (Reise 1981, Papaspyrou et al 2006. The significance of burrow structures as sites of enhanced capacity for microbial PAH mineralization have also been documented (Chung & King 1999, Granberg et al 2005.…”