Abstract

Denitrifying and anammox bacteria are involved in the nitrogen cycling in marine sediments but the environmental factors that regulate the relative importance of these processes are not well constrained. Here, we evaluated the abundance, diversity, and potential activity of denitrifying, anammox, and sulfide-dependent denitrifying bacteria in the sediments of the seasonally hypoxic saline Lake Grevelingen, known to harbor an active microbial community involved in sulfur oxidation pathways. Depth distributions of 16S rRNA gene, nirS gene of denitrifying and anammox bacteria, aprA gene of sulfur-oxidizing and sulfate-reducing bacteria, and ladderane lipids of anammox bacteria were studied in sediments impacted by seasonally hypoxic bottom waters. Samples were collected down to 5 cm depth (1 cm resolution) at three different locations before (March) and during summer hypoxia (August). The abundance of denitrifying bacteria did not vary despite of differences in oxygen and sulfide availability in the sediments, whereas anammox bacteria were more abundant in the summer hypoxia but in those sediments with lower sulfide concentrations. The potential activity of denitrifying and anammox bacteria as well as of sulfur-oxidizing, including sulfide-dependent denitrifiers and sulfate-reducing bacteria, was potentially inhibited by the competition for nitrate and nitrite with cable and/or Beggiatoa-like bacteria in March and by the accumulation of sulfide in the summer hypoxia. The simultaneous presence and activity of organoheterotrophic denitrifying bacteria, sulfide-dependent denitrifiers, and anammox bacteria suggests a tight network of bacteria coupling carbon-, nitrogen-, and sulfur cycling in Lake Grevelingen sediments.

Highlights

  • Nitrogen availability is a major factor controlling primary production in temperate coastal marine environments with high anthropogenic nitrogen input (Herbert, 1999)

  • We focus on (1) denitrification, the stepwise conversion of nitrate/nitrite to dinitrogen gas which is mainly performed by facultative organoheterotrophic anaerobic bacteria and some archaea (Zumft, 1997); (2) anaerobic ammonium oxidation, the oxidation of ammonium with nitrite to dinitrogen gas carried out by anammox bacteria (Kuypers et al, 2003); and (3) sulfide-dependent denitrification, the oxidation of sulfide with nitrate performed by autotrophic members of α, β, γ, and ε-proteobacteria, which could contribute to denitrification and to the removal of sulfide in the oxygen transition zone of coastal marine sediments (Shao et al, 2010)

  • Our starting hypothesis is that the abundance and potential activity of organoheterotrophic denitrifiers and anammox bacteria would decrease upon increase of the sulfide concentration found in the sediments during the summer hypoxia

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Summary

Introduction

Nitrogen availability is a major factor controlling primary production in temperate coastal marine environments with high anthropogenic nitrogen input (Herbert, 1999). We focus on (1) denitrification, the stepwise conversion of nitrate/nitrite to dinitrogen gas which is mainly performed by facultative organoheterotrophic anaerobic bacteria and some archaea (Zumft, 1997); (2) anaerobic ammonium oxidation (anammox), the oxidation of ammonium with nitrite to dinitrogen gas carried out by anammox bacteria (Kuypers et al, 2003); and (3) sulfide-dependent denitrification, the oxidation of sulfide with nitrate performed by autotrophic members of α-, β-, γ-, and ε-proteobacteria, which could contribute to denitrification and to the removal of sulfide in the oxygen transition zone of coastal marine sediments (Shao et al, 2010) Numerous environmental factors, such as the availability of nitrogen speciation and concentration, temperature, oxygen concentrations, organic matter quality and quantity, bioturbation, and other sediment characteristics have been suggested to affect the distribution and abundance of denitrifying and anammox bacteria (Thamdrup and Dalsgaard, 2002; Meyer et al, 2005; Jensen et al, 2008; Dang et al, 2010; Laverock et al, 2013; Prokopenko et al, 2013; Babbin et al, 2014; Zhang et al, 2014). Jensen et al (2008) showed that sulfide had a direct inhibiting effect on the activity of anammox bacteria in the Black Sea

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