Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

Predominance and high diversity of genes associated to denitrification in metagenomes of subantarctic coastal sediments exposed to urban pollution

Journal Article · · PLoS ONE
 [1];  [1];  [1];  [2];  [3];  [1]
  1. Centro para el Estudio de Sistemas Marinos, Puerto Madryn (Argentina)
  2. Centro para el Estudio de Sistemas Marinos, Puerto Madryn (Argentina); CCT CONICET CENPAT, Puerto Madryn (Argentina)
  3. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)

The aim of this work was to characterize the microbial nitrogen cycling potential in sediments from Ushuaia Bay, a subantarctic environment that has suffered a recent explosive demographic growth. Subtidal sediment samples were retrieved in triplicate from two urban points in the Bay, and analyzed through metagenomic shotgun sequencing. Sequences assigned to genes related to nitrification, nitrate reduction and denitrification were predominant in this environment with respect to metagenomes from other environments, including other marine sediments. The nosZ gene, responsible for nitrous oxide transformation into di-nitrogen, presented a high diversity. The majority of NosZ sequences were classified as Clade II (atypical) variants affiliated to different bacterial lineages such as Bacteroidetes, Chloroflexi, Firmicutes, Proteobacteria, Verrucomicrobia, as well as to Archaea. The analysis of a fosmid metagenomic library from the same site showed that the genomic context of atypical variants was variable, and was accompanied by distinct regulatory elements, suggesting the evolution of differential ecophysiological roles. This work increases our understanding of the microbial ecology of nitrogen transformations in cold coastal environments and provides evidence of an enhanced denitrification potential in impacted sediment microbial communities. In addition, it highlights the role of yet overlooked populations in the mitigation of environmentally harmful forms of nitrogen.

Research Organization:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Organization:
USDOE
Grant/Contract Number:
AC05-76RL01830
OSTI ID:
1489274
Report Number(s):
PNNL-SA--125133
Journal Information:
PLoS ONE, Journal Name: PLoS ONE Journal Issue: 11 Vol. 13; ISSN 1932-6203
Publisher:
Public Library of ScienceCopyright Statement
Country of Publication:
United States
Language:
English

References (94)

Alkane Biodegradation Genes from Chronically Polluted Subantarctic Coastal Sediments and Their Shifts in Response to Oil Exposure journal May 2012
Diverse Bacterial Groups Contribute to the Alkane Degradation Potential of Chronically Polluted Subantarctic Coastal Sediments journal November 2015
The Curious Case of Achromobacter eurydice, a Gram-Variable Pleomorphic Bacterium Associated with European Foulbrood Disease in Honeybees journal June 2017
Nitrogen Metabolism Genes from Temperate Marine Sediments journal March 2017
Assessment of recent sediment influence in an urban polluted subantarctic coastal ecosystem. Beagle Channel (Southern Argentina) journal January 2011
Mitigating release of the potent greenhouse gas N2O from the nitrogen cycle – could enzymic regulation hold the key? journal July 2009
Genomics and Ecology of Novel N2O-Reducing Microorganisms journal January 2018
Structure of cytochrome c nitrite reductase journal July 1999
Metagenomics reveals sediment microbial community response to Deepwater Horizon oil spill journal January 2014
Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw journal November 2011
Unlocking the potential of metagenomics through replicated experimental design journal June 2012
Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system journal October 2016
QIIME allows analysis of high-throughput community sequencing data journal April 2010
Bioturbation: impact on the marine nitrogen cycle journal January 2011
Transcription regulation of the nir gene cluster encoding nitrite reductase of Paracoccus denitrificans involves NNR and NirI, a novel type of membrane protein journal October 1999
Copper control of bacterial nitrous oxide emission and its impact on vitamin B12-dependent metabolism journal November 2013
NsrR from Streptomyces coelicolor Is a Nitric Oxide-sensing [4Fe-4S] Cluster Protein with a Specialized Regulatory Function journal March 2015
Clustal W and Clustal X version 2.0 journal September 2007
Transcriptional and environmental control of bacterial denitrification and N2O emissions journal December 2017
IMG/M 4 version of the integrated metagenome comparative analysis system journal October 2013
Performance, Accuracy, and Web Server for Evolutionary Placement of Short Sequence Reads under Maximum Likelihood journal March 2011
Profiling gene expression to distinguish the likely active diazotrophs from a sea of genetic potential in marine sediments: Active nitrogen fixers in coastal marine sediments journal March 2014
Molecular genetic analysis of an FNR-dependent anaerobically inducible Escherichia coli promoter journal October 1990
Nitrogen cycling in coastal marine ecosystems journal October 1999
Regulators of bacterial responses to nitric oxide journal March 2007
Metagenomics reveals the high polycyclic aromatic hydrocarbon-degradation potential of abundant uncultured bacteria from chronically polluted subantarctic and temperate coastal marine environments journal June 2015
Genome-Derived Criteria for Assigning Environmental narG and nosZ Sequences to Operational Taxonomic Units of Nitrate Reducers journal June 2009
Nitrous Oxide Reduction Kinetics Distinguish Bacteria Harboring Clade I NosZ from Those Harboring Clade II NosZ journal April 2016
Nitrous Oxide Reduction by an Obligate Aerobic Bacterium, Gemmatimonas aurantiaca Strain T-27 journal April 2017
Actinobacterial Nitrate Reducers and Proteobacterial Denitrifiers Are Abundant in N 2 O-Metabolizing Palsa Peat journal June 2012
Changes in Benthic Denitrification, Nitrate Ammonification, and Anammox Process Rates and Nitrate and Nitrite Reductase Gene Abundances along an Estuarine Nutrient Gradient (the Colne Estuary, United Kingdom) journal March 2009
Abundance, Dynamics, and Biogeographic Distribution of Seven Polycyclic Aromatic Hydrocarbon Dioxygenase Gene Variants in Coastal Sediments of Patagonia journal January 2012
Nitrite Reductase Genes (nirK and nirS) as Functional Markers To Investigate Diversity of Denitrifying Bacteria in Pacific Northwest Marine Sediment Communities journal May 2000
NosR, a membrane-bound regulatory component necessary for expression of nitrous oxide reductase in denitrifying Pseudomonas stutzeri. journal August 1992
Transcription Factor FnrP from Paracoccus denitrificans Contains an Iron-Sulfur Cluster and Is Activated by Anoxia: Identification of Essential Cysteine Residues journal January 2002
Functional Domains of NosR, a Novel Transmembrane Iron-Sulfur Flavoprotein Necessary for Nitrous Oxide Respiration journal March 2005
Detecting Nitrous Oxide Reductase (nosZ) Genes in Soil Metagenomes: Method Development and Implications for the Nitrogen Cycle journal June 2014
Cell biology and molecular basis of denitrification journal December 1997
Microbial Nitrogen Cycling Processes in Oxygen Minimum Zones journal January 2011
Nitrogen Cycle of the Open Ocean: From Genes to Ecosystems journal January 2011
Metagenomics: Genomic Analysis of Microbial Communities journal December 2004
Highly diverse nirK genes comprise two major clades that harbour ammonium-producing denitrifiers journal February 2016
Fundamentals of Microbial Community Resistance and Resilience journal January 2012
Molecular characterization of vulnibactin biosynthesis in Vibrio vulnificus indicates the existence of an alternative siderophore journal January 2014
The diversity of the N2O reducers matters for the N2O:N2 denitrification end-product ratio across an annual and a perennial cropping system journal September 2015
Dissimilatory nitrogen reduction in intertidal sediments of a temperate estuary: small scale heterogeneity and novel nitrate-to-ammonium reducers journal October 2015
Anammox, denitrification and fixed-nitrogen removal in sediments from the Lower St. Lawrence Estuary journal January 2012
Environmental Characterization of a Eutrophicated Semi-Enclosed System: Nutrient Budget (Encerrada Bay, Tierra del Fuego Island, Patagonia, Argentina) journal April 2009
Respiration and denitrification in permeable continental shelf deposits on the South Atlantic Bight: Rates of carbon and nitrogen cycling from sediment column experiments journal July 2007
Rates of N2 production and diversity and abundance of functional genes associated with denitrification and anaerobic ammonium oxidation in the sediment of the Amundsen Sea Polynya, Antarctica journal January 2016
Bacterial nitrate reductases: Molecular and biological aspects of nitrate reduction journal May 2006
The unaccounted yet abundant nitrous oxide-reducing microbial community: a potential nitrous oxide sink journal November 2012
Fast gapped-read alignment with Bowtie 2 journal March 2012
Metabolic flexibility allows bacterial habitat generalists to become dominant in a frequently disturbed ecosystem journal May 2021
Competition between Escherichia coli strains expressing either a periplasmic or a membrane-bound nitrate reductase: does Nap confer a selective advantage during nitrate-limited growth? journal November 1999
Bioturbation: impact on the marine nitrogen cycle journal January 2011
Competition between Escherichia coli strains expressing either a periplasmic or a membrane-bound nitrate reductase: does Nap confer a selective advantage during nitrate-limited growth? journal November 1999
Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils journal November 2012
NsrR from Streptomyces coelicolor Is a Nitric Oxide-sensing [4Fe-4S] Cluster Protein with a Specialized Regulatory Function journal March 2015
CD-HIT Suite: a web server for clustering and comparing biological sequences journal January 2010
KEGG for linking genomes to life and the environment journal December 2007
Ab initio gene identification in metagenomic sequences journal April 2010
Biological sources and sinks of nitrous oxide and strategies to mitigate emissions
  • Thomson, Andrew J.; Giannopoulos, Georgios; Pretty, Jules
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 367, Issue 1593 https://doi.org/10.1098/rstb.2011.0415
journal May 2012
Metagenomics unveils the attributes of the alginolytic guilds of sediments from four distant cold coastal environments: Alginolytic guilds from cold sediments journal July 2016
Transcriptional control, translation and function of the products of the five open reading frames of the Escherichia coli nir operon journal October 1992
Functional analysis of NsrR, a nitric oxide-sensing Rrf2 repressor in Neisseria gonorrhoeae journal January 2009
Non-parametric multivariate analyses of changes in community structure journal March 1993
Nitrous Oxide (N2O): The Dominant Ozone-Depleting Substance Emitted in the 21st Century journal August 2009
Genome-Derived Criteria for Assigning Environmental narG and nosZ Sequences to Operational Taxonomic Units of Nitrate Reducers journal June 2009
Nitrous Oxide Reduction Kinetics Distinguish Bacteria Harboring Clade I NosZ from Those Harboring Clade II NosZ journal April 2016
Nitrous Oxide Reduction by an Obligate Aerobic Bacterium, Gemmatimonas aurantiaca Strain T-27 journal April 2017
Actinobacterial Nitrate Reducers and Proteobacterial Denitrifiers Are Abundant in N 2 O-Metabolizing Palsa Peat journal June 2012
Changes in Benthic Denitrification, Nitrate Ammonification, and Anammox Process Rates and Nitrate and Nitrite Reductase Gene Abundances along an Estuarine Nutrient Gradient (the Colne Estuary, United Kingdom) journal March 2009
Abundance, Dynamics, and Biogeographic Distribution of Seven Polycyclic Aromatic Hydrocarbon Dioxygenase Gene Variants in Coastal Sediments of Patagonia journal January 2012
Nitrite Reductase Genes (nirK and nirS) as Functional Markers To Investigate Diversity of Denitrifying Bacteria in Pacific Northwest Marine Sediment Communities journal May 2000
Nitrogen Cycling in the Ocean: New Perspectives on Processes and Paradigms journal March 2002
Transcription Factor FnrP from Paracoccus denitrificans Contains an Iron-Sulfur Cluster and Is Activated by Anoxia: Identification of Essential Cysteine Residues journal January 2002
Functional Domains of NosR, a Novel Transmembrane Iron-Sulfur Flavoprotein Necessary for Nitrous Oxide Respiration journal March 2005
Detecting Nitrous Oxide Reductase (nosZ) Genes in Soil Metagenomes: Method Development and Implications for the Nitrogen Cycle journal June 2014
Complete Genome Sequence of Clostridium botulinum CJ0611A1, a Type A(B) Isolate Associated with an International Outbreak of Botulism from Commercial Carrot Juice journal January 2021
Ray Meta: scalable de novo metagenome assembly and profiling journal January 2012
Genomic resolution of linkages in carbon, nitrogen, and sulfur cycling among widespread estuary sediment bacteria journal April 2015
Dissimilatory Metabolism of Nitrogen Oxides in Bacteria: Comparative Reconstruction of Transcriptional Networks journal January 2005
Dissimilatory Metabolism of Nitrogen Oxides in Bacteria: Comparative Reconstruction of Transcriptional Networks journal January 2005
A Format for Phylogenetic Placements journal February 2012
The PhyloPythiaS Web Server for Taxonomic Assignment of Metagenome Sequences journal June 2012
Intergenomic Comparisons Highlight Modularity of the Denitrification Pathway and Underpin the Importance of Community Structure for N2O Emissions journal December 2014
Accelerating shrinkage of Patagonian glaciers from the Little Ice Age (~AD 1870) to 2011 journal January 2012
Predicting microbial nitrate reduction pathways in coastal sediments journal January 2014
The microbial nitrogen cycling potential is impacted by polyaromatic hydrocarbon pollution of marine sediments journal March 2014
Anaerobic ammonium oxidation in deep-sea sediments off the Washington margin journal July 2009
Intensive and extensive nitrogen loss from intertidal permeable sediments of the Wadden Sea journal January 2012
A format for phylogenetic placements text January 2012
The Importance of Dissimilatory Nitrate Reduction to Ammonium (DNRA) in the Nitrogen Cycle of Coastal Ecosystems journal September 2013

Figures / Tables (6)


Similar Records

High wax ester and triacylglycerol biosynthesis potential in coastal sediments of Antarctic and Subantarctic environments
Journal Article · Mon Jul 17 00:00:00 EDT 2023 · PLoS ONE · OSTI ID:2422817

Related Subjects