Research Article: The effect of bio-irrigation by the polychaete Lanice conchilega on active denitrifiers: Distribution, diversity and composition of nosZ gene

Date Published: February 6, 2018

Publisher: Public Library of Science

Author(s): Maryam Yazdani Foshtomi, Frederik Leliaert, Sofie Derycke, Anne Willems, Magda Vincx, Jan Vanaverbeke, Kay C. Vopel.

http://doi.org/10.1371/journal.pone.0192391

Abstract

The presence of large densities of the piston-pumping polychaete Lanice conchilega can have important consequences for the functioning of marine sediments. It is considered both an allogenic and an autogenic ecosystem engineer, affecting spatial and temporal biogeochemical gradients (oxygen concentrations, oxygen penetration depth and nutrient concentrations) and physical properties (grain size) of marine sediments, which could affect functional properties of sediment-inhabiting microbial communities. Here we investigated whether density-dependent effects of L. conchilega affected horizontal (m-scale) and vertical (cm-scale) patterns in the distribution, diversity and composition of the typical nosZ gene in the active denitrifying organisms. This gene plays a major role in N2O reduction in coastal ecosystems as the last step completing the denitrification pathway. We showed that both vertical and horizontal composition and richness of nosZ gene were indeed significantly affected when large densities of the bio-irrigator were present. This could be directly related to allogenic ecosystem engineering effects on the environment, reflected in increased oxygen penetration depth and oxygen concentrations in the upper cm of the sediment in high densities of L. conchilega. A higher diversity (Shannon diversity and inverse Simpson) of nosZ observed in patches with high L. conchilega densities (3,185–3,440 ind. m-2) at deeper sediment layers could suggest a downward transport of NO3− to deeper layers resulting from bio-irrigation as well. Hence, our results show the effect of L. conchilega bio-irrigation activity on denitrifying organisms in L. conchilega reefs.

Partial Text

Denitrification is a key process in the biogeochemical cycling of nitrogen. It is a primary loss mechanism for nitrogen in the nitrogen budget of coastal ecosystems [1]. It is a four-step respiratory process, in which nitrate (NO3−) is reduced sequentially to nitrite (NO2−), nitric oxide (NO), nitrous oxide (N2O), and nitrogen gas (N2), and is mediated by a taxonomically diverse group of microorganisms, mainly bacteria [2]. Denitrification counteracts eutrophication by removing N2, but it can contribute to global warming and ozone depletion due to the release of NO and N2O [3–5].

In the current study, we investigated the denitrifying community in L. conchilega aggregations at the intertidal zone by focusing on expression of the gene encoding nitrous-oxide reductase (nosZ), the enzyme catalysing the final step of denitrification. We investigated typical nosZ genes, which play the major role in N2O reduction in coastal ecosystems [25]. The denitrifiers with a complete pathway were identified as the dominant community [25].

This study improves our understanding of the effects of bio-irrigation on the nosZ gene. Our results reveal that large densities of L. conchilega (>3000 ind. m-2) affect composition, structure and diversity indices of the active nosZ community both vertically and horizontally in the sediment. These patterns can be linked with heterogeneity in geochemical environments in the sediment that are affected by allogenic ecosystem engineering effects of L. conchilega. The piston-pumping activity of the polychaete transports oxygen rich waters to the deeper layers of the sediment. This could also provide higher availability of NO3− at depth by increasing the surface for coupled nitrification-denitrification in the sediment along the tube.

 

Source:

http://doi.org/10.1371/journal.pone.0192391

 

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