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      Selective Pressure of Temperature on Competition and Cross-Feeding within Denitrifying and Fermentative Microbial Communities

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          Abstract

          In coastal marine sediments, denitrification and fermentation are important processes in the anaerobic decomposition of organic matter. Microbial communities performing these two processes were enriched from tidal marine sediments in replicated, long term chemostat incubations at 10 and 25°C. Whereas denitrification rates at 25°C were more or less stable over time, at 10°C denitrification activity was unstable and could only be sustained either by repeatedly increasing the amount of carbon substrates provided or by repeatedly decreasing the dilution rate. Metagenomic and transcriptomic sequencing was performed at different time points and provisional whole genome sequences (WGS) and gene activities of abundant populations were compared across incubations. These analyses suggested that a temperature of 10°C selected for populations related to Vibrionales/Photobacterium that contributed to both fermentation (via pyruvate/formate lyase) and nitrous oxide reduction. At 25°C, denitrifying populations affiliated with Rhodobacteraceae were more abundant. The latter performed complete denitrification, and may have used carbon substrates produced by fermentative populations (cross-feeding). Overall, our results suggest that a mixture of competition—for substrates between fermentative and denitrifying populations, and for electrons between both pathways active within a single population –, and cross feeding—between fermentative and denitrifying populations—controlled the overall rate of denitrification. Temperature was shown to have a strong selective effect, not only on the populations performing either process, but also on the nature of their ecological interactions. Future research will show whether these results can be extrapolated to the natural environment.

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          The global nitrogen cycle in the twenty-first century.

          Global nitrogen fixation contributes 413 Tg of reactive nitrogen (Nr) to terrestrial and marine ecosystems annually of which anthropogenic activities are responsible for half, 210 Tg N. The majority of the transformations of anthropogenic Nr are on land (240 Tg N yr(-1)) within soils and vegetation where reduced Nr contributes most of the input through the use of fertilizer nitrogen in agriculture. Leakages from the use of fertilizer Nr contribute to nitrate (NO3(-)) in drainage waters from agricultural land and emissions of trace Nr compounds to the atmosphere. Emissions, mainly of ammonia (NH3) from land together with combustion related emissions of nitrogen oxides (NOx), contribute 100 Tg N yr(-1) to the atmosphere, which are transported between countries and processed within the atmosphere, generating secondary pollutants, including ozone and other photochemical oxidants and aerosols, especially ammonium nitrate (NH4NO3) and ammonium sulfate (NH4)2SO4. Leaching and riverine transport of NO3 contribute 40-70 Tg N yr(-1) to coastal waters and the open ocean, which together with the 30 Tg input to oceans from atmospheric deposition combine with marine biological nitrogen fixation (140 Tg N yr(-1)) to double the ocean processing of Nr. Some of the marine Nr is buried in sediments, the remainder being denitrified back to the atmosphere as N2 or N2O. The marine processing is of a similar magnitude to that in terrestrial soils and vegetation, but has a larger fraction of natural origin. The lifetime of Nr in the atmosphere, with the exception of N2O, is only a few weeks, while in terrestrial ecosystems, with the exception of peatlands (where it can be 10(2)-10(3) years), the lifetime is a few decades. In the ocean, the lifetime of Nr is less well known but seems to be longer than in terrestrial ecosystems and may represent an important long-term source of N2O that will respond very slowly to control measures on the sources of Nr from which it is produced.
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            EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data

            Recovery of ribosomal small subunit genes by assembly of short read community DNA sequence data generally fails, making taxonomic characterization difficult. Here, we solve this problem with a novel iterative method, based on the expectation maximization algorithm, that reconstructs full-length small subunit gene sequences and provides estimates of relative taxon abundances. We apply the method to natural and simulated microbial communities, and correctly recover community structure from known and previously unreported rRNA gene sequences. An implementation of the method is freely available at https://github.com/csmiller/EMIRGE.
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              The unaccounted yet abundant nitrous oxide-reducing microbial community: a potential nitrous oxide sink.

              Nitrous oxide (N(2)O) is a major radiative forcing and stratospheric ozone-depleting gas emitted from terrestrial and aquatic ecosystems. It can be transformed to nitrogen gas (N(2)) by bacteria and archaea harboring the N(2)O reductase (N(2)OR), which is the only known N(2)O sink in the biosphere. Despite its crucial role in mitigating N(2)O emissions, knowledge of the N(2)OR in the environment remains limited. Here, we report a comprehensive phylogenetic analysis of the nosZ gene coding the N(2)OR in genomes retrieved from public databases. The resulting phylogeny revealed two distinct clades of nosZ, with one unaccounted for in studies investigating N(2)O-reducing communities. Examination of N(2)OR structural elements not considered in the phylogeny revealed that the two clades differ in their signal peptides, indicating differences in the translocation pathway of the N(2)OR across the membrane. Sequencing of environmental clones of the previously undetected nosZ lineage in various environments showed that it is widespread and diverse. Using quantitative PCR, we demonstrate that this clade was most often at least as abundant as the other, thereby more than doubling the known extent of the overall N(2)O-reducing community in the environment. Furthermore, we observed that the relative abundance of nosZ from either clade varied among habitat types and environmental conditions. Our results indicate a physiological dichotomy in the diversity of N(2)O-reducing microorganisms, which might be of importance for understanding the relationship between the diversity of N(2)O-reducing microorganisms and N(2)O reduction in different ecosystems.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                07 January 2016
                2015
                : 6
                : 1461
                Affiliations
                [1] 1Microbial Fitness Group, Max Planck Institute for Marine Microbiology Bremen, Germany
                [2] 2Center for Biotechnology, Institute for Genome Research and Systems Biology, University of Bielefeld Bielefeld, Germany
                [3] 3Energy Bioengineering Group, Department of Geoscience, University of Calgary Calgary, AB, Canada
                Author notes

                Edited by: Ivan Mijakovic, Chalmers University of Technology, Sweden

                Reviewed by: Dimitry Y. Sorokin, Delft University of Technology, Netherlands; Jan Martinussen, Technical University of Denmark, Denmark

                *Correspondence: Marc Strous mstrous@ 123456ucalgary.ca

                This article was submitted to Microbial Physiology and Metabolism, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2015.01461
                4703780
                26779132
                d8021472-615e-4bee-b025-2dc096337ae5
                Copyright © 2016 Hanke, Berg, Hargesheimer, Tegetmeyer, Sharp and Strous.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 18 October 2015
                : 07 December 2015
                Page count
                Figures: 5, Tables: 2, Equations: 0, References: 34, Pages: 14, Words: 8819
                Funding
                Funded by: European Research Council 10.13039/501100000781
                Award ID: 242635
                Funded by: Max-Planck-Gesellschaft 10.13039/501100004189
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                metagenomics,chemostat,marine sediment,rhodobacteraceae,vibrio,arcobacter,microbial ecology,nitric oxide dismutase

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