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      Response of the Ubiquitous Pelagic Diatom Thalassiosira weissflogii to Darkness and Anoxia

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          Abstract

          Thalassiosira weissflogii, an abundant, nitrate-storing, bloom-forming diatom in the world’s oceans, can use its intracellular nitrate pool for dissimilatory nitrate reduction to ammonium (DNRA) after sudden shifts to darkness and anoxia, most likely as a survival mechanism. T. weissflogii cells that stored 4 mM 15N-nitrate consumed 1.15 (±0.25) fmol NO 3 - cell -1 h -1 and simultaneously produced 1.57 (±0.21) fmol 15NH 4 + cell -1 h -1 during the first 2 hours of dark/anoxic conditions. Ammonium produced from intracellular nitrate was excreted by the cells, indicating a dissimilatory rather than assimilatory pathway. Nitrite and the greenhouse gas nitrous oxide were produced at rates 2-3 orders of magnitude lower than the ammonium production rate. While DNRA activity was restricted to the first few hours of darkness and anoxia, the subsequent degradation of photopigments took weeks to months, supporting the earlier finding that diatoms resume photosynthesis even after extended exposure to darkness and anoxia. Considering the high global abundance of T. weissflogii, its production of ammonium and nitrous oxide might be of ecological importance for oceanic oxygen minimum zones and the atmosphere, respectively.

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          Marine microorganisms and global nutrient cycles.

          The way that nutrients cycle through atmospheric, terrestrial, oceanic and associated biotic reservoirs can constrain rates of biological production and help structure ecosystems on land and in the sea. On a global scale, cycling of nutrients also affects the concentration of atmospheric carbon dioxide. Because of their capacity for rapid growth, marine microorganisms are a major component of global nutrient cycles. Understanding what controls their distributions and their diverse suite of nutrient transformations is a major challenge facing contemporary biological oceanographers. What is emerging is an appreciation of the previously unknown degree of complexity within the marine microbial community.
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            Microbial ecology of expanding oxygen minimum zones.

            Dissolved oxygen concentration is a crucial organizing principle in marine ecosystems. As oxygen levels decline, energy is increasingly diverted away from higher trophic levels into microbial metabolism, leading to loss of fixed nitrogen and to production of greenhouse gases, including nitrous oxide and methane. In this Review, we describe current efforts to explore the fundamental factors that control the ecological and microbial biodiversity in oxygen-starved regions of the ocean, termed oxygen minimum zones. We also discuss how recent advances in microbial ecology have provided information about the potential interactions in distributed co-occurrence and metabolic networks in oxygen minimum zones, and we provide new insights into coupled biogeochemical processes in the ocean.
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              Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils.

              Agricultural and industrial practices more than doubled the intrinsic rate of terrestrial N fixation over the past century with drastic consequences, including increased atmospheric nitrous oxide (N(2)O) concentrations. N(2)O is a potent greenhouse gas and contributor to ozone layer destruction, and its release from fixed N is almost entirely controlled by microbial activities. Mitigation of N(2)O emissions to the atmosphere has been attributed exclusively to denitrifiers possessing NosZ, the enzyme system catalyzing N(2)O to N(2) reduction. We demonstrate that diverse microbial taxa possess divergent nos clusters with genes that are related yet evolutionarily distinct from the typical nos genes of denitirifers. nos clusters with atypical nosZ occur in Bacteria and Archaea that denitrify (44% of genomes), do not possess other denitrification genes (56%), or perform dissimilatory nitrate reduction to ammonium (DNRA; (31%). Experiments with the DNRA soil bacterium Anaeromyxobacter dehalogenans demonstrated that the atypical NosZ is an effective N(2)O reductase, and PCR-based surveys suggested that atypical nosZ are abundant in terrestrial environments. Bioinformatic analyses revealed that atypical nos clusters possess distinctive regulatory and functional components (e.g., Sec vs. Tat secretion pathway in typical nos), and that previous nosZ-targeted PCR primers do not capture the atypical nosZ diversity. Collectively, our results suggest that nondenitrifying populations with a broad range of metabolisms and habitats are potentially significant contributors to N(2)O consumption. Apparently, a large, previously unrecognized group of environmental nosZ has not been accounted for, and characterizing their contributions to N(2)O consumption will advance understanding of the ecological controls on N(2)O emissions and lead to refined greenhouse gas flux models.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                2 December 2013
                : 8
                : 12
                : e82605
                Affiliations
                [1 ]Max Planck Institute for Marine Microbiology, Microsensor Group, Bremen, Germany
                [2 ]Jacobs University Bremen, Molecular Life Science Research Center, Bremen, Germany
                [3 ]University of Southern Denmark, Department of Biology, NordCEE, Odense, Denmark
                Stazione Zoologica, Italy
                Author notes

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

                Conceived and designed the experiments: AK PS DdB. Performed the experiments: AK PS JK. Analyzed the data: AK PS JK. Wrote the manuscript: AK PS DdB.

                Article
                PONE-D-13-40871
                10.1371/journal.pone.0082605
                3846789
                24312664
                dab21a49-cae1-4b77-a24d-0f9e95d766f2
                Copyright @ 2013

                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.

                History
                : 7 October 2013
                : 4 November 2013
                Funding
                Financial support was provided by the Max Planck Society (Germany), and by a grant from the German Research Foundation awarded to A.K. (KA 3187/2-1). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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