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Controls of Sediment Nitrogen Dynamics in Tropical Coastal Lagoons

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      Abstract

      Sediment denitrification rates seem to be lower in tropical environments than in temperate environments. Using the isotope pairing technique, we measured actual denitrification rates in the sediment of tropical coastal lagoons. To explain the low denitrification rates observed at all study sites (<5 μmol N 2 m -2 h -1), we also evaluated potential oxygen (O 2) consumption, potential nitrification, potential denitrification, potential anammox, and estimated dissimilatory nitrate (NO 3 -) reduction to ammonium (NH 4 +; DNRA) in the sediment. 15NO 3 - and 15NH 4 + conversion was measured in oxic and anoxic slurries from the sediment surface. Sediment potential O 2 consumption was used as a proxy for overall mineralization activity. Actual denitrification rates and different potential nitrogen (N) oxidation and reduction processes were significantly correlated with potential O 2 consumption. The contribution of potential nitrification to total O 2 consumption decreased from contributing 9% at sites with the lowest sediment mineralization rates to less than 0.1% at sites with the highest rates. NO 3 - reduction switched completely from potential denitrification to estimated DNRA. Ammonium oxidation and nitrite (NO 2 -) reduction by potential anammox contributed up to 3% in sediments with the lowest sediment mineralization rates. The majority of these patterns could be explained by variations in the microbial environments from stable and largely oxic conditions at low sediment mineralization sites to more variable conditions and the prevalences of anaerobic microorganisms at high sediment mineralization sites. Furthermore, the presence of algal and microbial mats on the sediment had a significant effect on all studied processes. We propose a theoretical model based on low and high sediment mineralization rates to explain the growth, activity, and distribution of microorganisms carrying out denitrification and DNRA in sediments that can explain the dominance or coexistence of DNRA and denitrification processes. The results presented here show that the potential activity of anaerobic nitrate-reducing organisms is not dependent on the availability of environmental NO 3 -.

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      Most cited references 13

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      Production of N(2) through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments.

      In the global nitrogen cycle, bacterial denitrification is recognized as the only quantitatively important process that converts fixed nitrogen to atmospheric nitrogen gas, N(2), thereby influencing many aspects of ecosystem function and global biogeochemistry. However, we have found that a process novel to the marine nitrogen cycle, anaerobic oxidation of ammonium coupled to nitrate reduction, contributes substantially to N(2) production in marine sediments. Incubations with (15)N-labeled nitrate or ammonium demonstrated that during this process, N(2) is formed through one-to-one pairing of nitrogen from nitrate and ammonium, which clearly separates the process from denitrification. Nitrite, which accumulated transiently, was likely the oxidant for ammonium, and the process is thus similar to the anammox process known from wastewater bioreactors. Anaerobic ammonium oxidation accounted for 24 and 67% of the total N(2) production at two typical continental shelf sites, whereas it was detectable but insignificant relative to denitrification in a eutrophic coastal bay. However, rates of anaerobic ammonium oxidation were higher in the coastal sediment than at the deepest site and the variability in the relative contribution to N(2) production between sites was related to large differences in rates of denitrification. Thus, the relative importance of anaerobic ammonium oxidation and denitrification in N(2) production appears to be regulated by the availability of their reduced substrates. By shunting nitrogen directly from ammonium to N(2), anaerobic ammonium oxidation promotes the removal of fixed nitrogen in the oceans. The process can explain ammonium deficiencies in anoxic waters and sediments, and it may contribute significantly to oceanic nitrogen budgets.
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        Nitrogen cycling in coastal marine ecosystems.

         R Herbert (1999)
        It is generally considered that nitrogen availability is one of the major factors regulating primary production in temperate coastal marine environments. Coastal regions often receive large anthropogenic inputs of nitrogen that cause eutrophication. The impact of these nitrogen additions has a profound effect in estuaries and coastal lagoons where water exchange is limited. Such increased nutrient loading promotes the growth of phytoplankton and fast growing pelagic macroalgae while rooted plants (sea-grasses) and benthic are suppressed due to reduced light availability. This shift from benthic to pelagic primary production introduces large diurnal variations in oxygen concentrations in the water column. In addition oxygen consumption in the surface sediments increases due to the deposition of readily degradable biomass. In this review the physico-chemical and biological factors regulating nitrogen cycling in coastal marine ecosystems are considered in relation to developing effective management programmes to rehabilitate seagrass communities in lagoons currently dominated by pelagic macroalgae and/or cyanobacteria.
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          Anaerobic ammonium oxidation in a tropical freshwater system (Lake Tanganyika).

          Here we provide the first direct evidence for the anammox process (anaerobic ammonium oxidation) in a lacustrine system, Lake Tanganyika, the second largest lake in the world. Incubations with (15)N labelled nitrate showed that anammox occurred in the suboxic water layer at 100-110 m water depth. Anammox rates up to 10 nM N(2) h(-1) are comparable to those reported for the marine water column. Up to approximately 13% of produced N(2) could be attributed to the anammox process whereas the remainder was related to denitrification. Typical lipid biomarkers characteristic of anammox bacteria were found in filtered water from the depths where anammox occurred, thus supporting the presence of anammox bacteria. Further evidence is provided by fluorescence in situ hybridization (FISH), revealing up to 13 000 anammox bacteria cells per ml or 1.4% of all DAPI (4'-6-Diamidino-2-phenylindole)-stained cells. Phylogenetic analyses of partial 16S rRNA genes indicated the presence of sequences most closely related to the known anammox bacterium Candidatus "Scalindua brodae" (95.7% similarity). Using the incubation results, a total loss of 0.2 Tg N(2) per year linked to anammox was estimated for the Northern basin of Lake Tanganyika.
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            Author and article information

            Affiliations
            [1 ]Laboratório de Biogeoquímica, Departamento de Ecologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Rio de Janeiro, Brazil
            [2 ]Department of Environmental Change, Linköping University, Linköping, Sweden
            [3 ]Departamento de Geoquímica, Universidade Federal Fluminense, Niterói, Rio de Janeiro, Brazil
            [4 ]Laboratório de Limnologia, Departamento de Ecologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Rio de Janeiro, Brazil
            [5 ]Núcleo de Pesquisas em Ecologia e Desenvolvimento Sócio-ambiental de Macaé, Universidade Federal do Rio de Janeiro, Macaé, Rio de Janeiro, Brazil
            [6 ]Department of Biology, University of Aarhus, Aarhus, Denmark
            CAS, CHINA
            Author notes

            Competing Interests: The authors have declared that no competing interests exist.

            Conceived and designed the experiments: AEP FAE LPN. Performed the experiments: AEP LPN. Analyzed the data: AEP VF. Contributed reagents/materials/analysis tools: FAE LPN. Wrote the paper: AEP LPN VF.

            ‡ This author is the first author on this work.

            Contributors
            Role: Editor
            Journal
            PLoS One
            PLoS ONE
            plos
            plosone
            PLoS ONE
            Public Library of Science (San Francisco, CA USA )
            1932-6203
            13 May 2016
            2016
            : 11
            : 5
            27175907
            4866711
            10.1371/journal.pone.0155586
            PONE-D-15-49694
            (Editor)
            © 2016 Enrich-Prast et al

            This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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            Figures: 5, Tables: 1, Pages: 17
            Product
            Funding
            Funded by: funder-id http://dx.doi.org/10.13039/501100004586, Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro;
            Award Recipient :
            Funded by: funder-id http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;
            Award Recipient :
            Funded by: funder-id http://dx.doi.org/10.13039/501100002322, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior;
            Award Recipient :
            Funded by: funder-id http://dx.doi.org/10.13039/501100004225, Petrobras;
            Award Recipient :
            Funded by: Coordinate Research Network - CRN3 - Nnet Project Interamerican Institute for Global Change Research
            Award Recipient :
            This work was supported in part by: Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro, http://www.faperj.br/ to AEP; Conselho Nacional de Desenvolvimento Científico e Tecnológico, http://www.cnpq.br/ to FAE; Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, http://www.capes.gov.br/ to AEP; and Coordinate Research Network - CRN3 - Nnet Project Interamerican Institute for Global Change Research, http://www.iai.int/ to AEP.
            Categories
            Research Article
            Earth Sciences
            Geology
            Petrology
            Sediment
            Earth Sciences
            Geology
            Sedimentary Geology
            Sediment
            Earth Sciences
            Marine and Aquatic Sciences
            Bodies of Water
            Lagoons
            Physical Sciences
            Chemistry
            Chemical Reactions
            Nitrification
            Physical Sciences
            Materials Science
            Materials by Structure
            Mixtures
            Slurries
            Earth Sciences
            Marine and Aquatic Sciences
            Oceanography
            Water Columns
            Physical Sciences
            Chemistry
            Chemical Properties
            Salinity
            Physical Sciences
            Chemistry
            Physical Chemistry
            Chemical Properties
            Salinity
            Physical Sciences
            Chemistry
            Chemical Reactions
            Oxidation
            Physical Sciences
            Chemistry
            Chemical Compounds
            Nitrates
            Custom metadata
            Data are available on Figshare at https://figshare.com/s/8c7f2179c0b718635ec0.

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