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Interactions between benthic copepods, bacteria and diatoms promote nitrogen retention in intertidal marine sediments.

Stock W, Heylen K, Sabbe K, Willems A, De Troch M - PLoS ONE (2014)

Bottom Line: Ammonium concentrations were highest in the treatments with copepods or their spent medium, whilst denitrification potential was lowest in these treatments, suggesting that copepods enhance dissimilatory nitrate reduction to ammonium over denitrification.We hypothesize that this is an indirect effect, by providing extra carbon for the bacterial community through the copepods' excretion products, thus changing the C/N ratio in favour of dissimilatory nitrate reduction.Diatoms alone had no effect on the nitrogen fluxes, but they did enhance the effect of copepods, possibly by influencing the quantity and quality of the copepods' excretion products.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Ghent University, Ghent, Belgium.

ABSTRACT
The present study aims at evaluating the impact of diatoms and copepods on microbial processes mediating nitrate removal in fine-grained intertidal sediments. More specifically, we studied the interactions between copepods, diatoms and bacteria in relation to their effects on nitrate reduction and denitrification. Microcosms containing defaunated marine sediments were subjected to different treatments: an excess of nitrate, copepods, diatoms (Navicula sp.), a combination of copepods and diatoms, and spent medium from copepods. The microcosms were incubated for seven and a half days, after which nutrient concentrations and denitrification potential were measured. Ammonium concentrations were highest in the treatments with copepods or their spent medium, whilst denitrification potential was lowest in these treatments, suggesting that copepods enhance dissimilatory nitrate reduction to ammonium over denitrification. We hypothesize that this is an indirect effect, by providing extra carbon for the bacterial community through the copepods' excretion products, thus changing the C/N ratio in favour of dissimilatory nitrate reduction. Diatoms alone had no effect on the nitrogen fluxes, but they did enhance the effect of copepods, possibly by influencing the quantity and quality of the copepods' excretion products. Our results show that small-scale biological interactions between bacteria, copepods and diatoms can have an important impact on denitrification and hence sediment nitrogen fluxes.

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Summary of the assumed interactions to explain the observed differences in N2O production rates.The assumed interactions which affect denitrification are indicated with dashed arrows. Bacteria mediated relevant reduction reactions of the nitrogen pathway and sulfur pathway are enclosed by grey boxes indicated with respectively ‘N fluxes’ and ‘S fluxes’. Copepods feed on both diatoms and bacteria, and produce excretion producs (excretions). Bacteria feed on the excretion produces and are also responsible for the reduction of SO42- to H2S and of NO3- to NH4+ (DNRA) and N2O+N2 (denitrification) in the microcosm. The produced NH4+ is assimilated by both bacteria and diatoms. Copepods affect the N2O production rate by producing excretion products which provide an extra carbon source, of which mainly the DNRA bacteria can take advantage (1) and also enhances SO42- reduction (2a), which results in more H2S. The increased H2S inhibits denitrification (2b). Diatoms have no direct effect on the N2O production rate, but do have an indirect effect by enhancing the survival of the copepods (3) and influencing the quantity and composition of the copepods' excretion products (4).
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pone-0111001-g002: Summary of the assumed interactions to explain the observed differences in N2O production rates.The assumed interactions which affect denitrification are indicated with dashed arrows. Bacteria mediated relevant reduction reactions of the nitrogen pathway and sulfur pathway are enclosed by grey boxes indicated with respectively ‘N fluxes’ and ‘S fluxes’. Copepods feed on both diatoms and bacteria, and produce excretion producs (excretions). Bacteria feed on the excretion produces and are also responsible for the reduction of SO42- to H2S and of NO3- to NH4+ (DNRA) and N2O+N2 (denitrification) in the microcosm. The produced NH4+ is assimilated by both bacteria and diatoms. Copepods affect the N2O production rate by producing excretion products which provide an extra carbon source, of which mainly the DNRA bacteria can take advantage (1) and also enhances SO42- reduction (2a), which results in more H2S. The increased H2S inhibits denitrification (2b). Diatoms have no direct effect on the N2O production rate, but do have an indirect effect by enhancing the survival of the copepods (3) and influencing the quantity and composition of the copepods' excretion products (4).

Mentions: Contrary to macrofauna, not much is known about the impact of meiofauna on nitrogen fluxes. Macrofauna seems to have its biggest impact through bioturbation (e.g. [15]). However, the oxygen penetration depth did not increase in the presence of copepods (Text S1), and consequently the effects of copepods are not related to oxygen. Since the N2O production rates of the copepod and their spent medium treatments were low, the copepods appeared to negatively impact denitrification, at least partially via their outfluxes. The outfluxes of the copepods are, apart from being an important nutrient source, a source of organic compounds and hence a substrate for bacterial growth [38]. Since organic matter loading may be one of the most important variables controlling denitrification in aquatic ecosystems [39], the impact of these carbon outfluxes should not be underestimated. The copepod outfluxes contain high amounts of labile carbon [22], which are known to stimulate DNRA over denitrification and anammox (Fig. 2, dashed arrow 1; [9]). Copepods can also indirectly stimulate labile carbon production by mechanically breaking down detrital particles [40], [41]. In addition, more organic matter results in a higher sulphate reduction rate (Fig. 2, dashed arrow 2; [42]). The main product of sulphate reduction is hydrogen sulphide, which inhibits denitrification and nitrification, but not DNRA [7]. These findings are supported by the higher final ammonium concentrations in the treatments with copepods or their spent medium. Furthermore, the NO3- reduction rate did not differ significantly between the treatments, suggesting that the reduced denitrification activity in the treatments with copepods or their spent medium was compensated by another nitrate reducing process.


Interactions between benthic copepods, bacteria and diatoms promote nitrogen retention in intertidal marine sediments.

Stock W, Heylen K, Sabbe K, Willems A, De Troch M - PLoS ONE (2014)

Summary of the assumed interactions to explain the observed differences in N2O production rates.The assumed interactions which affect denitrification are indicated with dashed arrows. Bacteria mediated relevant reduction reactions of the nitrogen pathway and sulfur pathway are enclosed by grey boxes indicated with respectively ‘N fluxes’ and ‘S fluxes’. Copepods feed on both diatoms and bacteria, and produce excretion producs (excretions). Bacteria feed on the excretion produces and are also responsible for the reduction of SO42- to H2S and of NO3- to NH4+ (DNRA) and N2O+N2 (denitrification) in the microcosm. The produced NH4+ is assimilated by both bacteria and diatoms. Copepods affect the N2O production rate by producing excretion products which provide an extra carbon source, of which mainly the DNRA bacteria can take advantage (1) and also enhances SO42- reduction (2a), which results in more H2S. The increased H2S inhibits denitrification (2b). Diatoms have no direct effect on the N2O production rate, but do have an indirect effect by enhancing the survival of the copepods (3) and influencing the quantity and composition of the copepods' excretion products (4).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4215923&req=5

pone-0111001-g002: Summary of the assumed interactions to explain the observed differences in N2O production rates.The assumed interactions which affect denitrification are indicated with dashed arrows. Bacteria mediated relevant reduction reactions of the nitrogen pathway and sulfur pathway are enclosed by grey boxes indicated with respectively ‘N fluxes’ and ‘S fluxes’. Copepods feed on both diatoms and bacteria, and produce excretion producs (excretions). Bacteria feed on the excretion produces and are also responsible for the reduction of SO42- to H2S and of NO3- to NH4+ (DNRA) and N2O+N2 (denitrification) in the microcosm. The produced NH4+ is assimilated by both bacteria and diatoms. Copepods affect the N2O production rate by producing excretion products which provide an extra carbon source, of which mainly the DNRA bacteria can take advantage (1) and also enhances SO42- reduction (2a), which results in more H2S. The increased H2S inhibits denitrification (2b). Diatoms have no direct effect on the N2O production rate, but do have an indirect effect by enhancing the survival of the copepods (3) and influencing the quantity and composition of the copepods' excretion products (4).
Mentions: Contrary to macrofauna, not much is known about the impact of meiofauna on nitrogen fluxes. Macrofauna seems to have its biggest impact through bioturbation (e.g. [15]). However, the oxygen penetration depth did not increase in the presence of copepods (Text S1), and consequently the effects of copepods are not related to oxygen. Since the N2O production rates of the copepod and their spent medium treatments were low, the copepods appeared to negatively impact denitrification, at least partially via their outfluxes. The outfluxes of the copepods are, apart from being an important nutrient source, a source of organic compounds and hence a substrate for bacterial growth [38]. Since organic matter loading may be one of the most important variables controlling denitrification in aquatic ecosystems [39], the impact of these carbon outfluxes should not be underestimated. The copepod outfluxes contain high amounts of labile carbon [22], which are known to stimulate DNRA over denitrification and anammox (Fig. 2, dashed arrow 1; [9]). Copepods can also indirectly stimulate labile carbon production by mechanically breaking down detrital particles [40], [41]. In addition, more organic matter results in a higher sulphate reduction rate (Fig. 2, dashed arrow 2; [42]). The main product of sulphate reduction is hydrogen sulphide, which inhibits denitrification and nitrification, but not DNRA [7]. These findings are supported by the higher final ammonium concentrations in the treatments with copepods or their spent medium. Furthermore, the NO3- reduction rate did not differ significantly between the treatments, suggesting that the reduced denitrification activity in the treatments with copepods or their spent medium was compensated by another nitrate reducing process.

Bottom Line: Ammonium concentrations were highest in the treatments with copepods or their spent medium, whilst denitrification potential was lowest in these treatments, suggesting that copepods enhance dissimilatory nitrate reduction to ammonium over denitrification.We hypothesize that this is an indirect effect, by providing extra carbon for the bacterial community through the copepods' excretion products, thus changing the C/N ratio in favour of dissimilatory nitrate reduction.Diatoms alone had no effect on the nitrogen fluxes, but they did enhance the effect of copepods, possibly by influencing the quantity and quality of the copepods' excretion products.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Ghent University, Ghent, Belgium.

ABSTRACT
The present study aims at evaluating the impact of diatoms and copepods on microbial processes mediating nitrate removal in fine-grained intertidal sediments. More specifically, we studied the interactions between copepods, diatoms and bacteria in relation to their effects on nitrate reduction and denitrification. Microcosms containing defaunated marine sediments were subjected to different treatments: an excess of nitrate, copepods, diatoms (Navicula sp.), a combination of copepods and diatoms, and spent medium from copepods. The microcosms were incubated for seven and a half days, after which nutrient concentrations and denitrification potential were measured. Ammonium concentrations were highest in the treatments with copepods or their spent medium, whilst denitrification potential was lowest in these treatments, suggesting that copepods enhance dissimilatory nitrate reduction to ammonium over denitrification. We hypothesize that this is an indirect effect, by providing extra carbon for the bacterial community through the copepods' excretion products, thus changing the C/N ratio in favour of dissimilatory nitrate reduction. Diatoms alone had no effect on the nitrogen fluxes, but they did enhance the effect of copepods, possibly by influencing the quantity and quality of the copepods' excretion products. Our results show that small-scale biological interactions between bacteria, copepods and diatoms can have an important impact on denitrification and hence sediment nitrogen fluxes.

Show MeSH