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Title: Metaproteomics reveals differential modes of metabolic coupling among ubiquitous oxygen minimum zone microbes

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America, 111(31):11395-11400

Oxygen minimum zones (OMZs) are intrinsic water column features arising from respiratory oxygen demand during organic matter degradation in stratified marine waters. Currently OMZs are expanding due to global climate change. This expansion alters marine ecosystem function and the productivity of fisheries due to habitat compression and changes in biogeochemical cycling leading to fixed nitrogen loss and greenhouse gas production. Here we use metaproteomics to chart spatial and temporal patterns of gene expression along defined redox gradients in a seasonally anoxic fjord, Saanich Inlet to better understand microbial community responses to OMZ expansion. The expression of metabolic pathway components for nitrification, anaerobic ammonium oxidation (anammox), denitrification and inorganic carbon fixation predominantly co-varied with abundance and distribution patterns of Thaumarchaeota, Nitrospira, Planctomycetes and SUP05/ARCTIC96BD-19 Gammaproteobacteria. Within these groups, pathways mediating inorganic carbon fixation and nitrogen and sulfur transformations were differentially expressed across the redoxcline. Nitrification and inorganic carbon fixation pathways affiliated with Thaumarchaeota dominated dysoxic waters and denitrification, sulfur-oxidation and inorganic carbon fixation pathways affiliated with SUP05 dominated suboxic and anoxic waters. Nitrite-oxidation and anammox pathways affiliated with Nitrospina and Planctomycetes respectively, also exhibited redox partitioning between dysoxic and suboxic waters. The differential expression of these pathways under changing water column redox conditions has quantitative implications for coupled biogeochemical cycling linking different modes of inorganic carbon fixation with distributed nitrogen and sulfur-based energy metabolism extensible to coastal and open ocean OMZs.

Research Organization:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)
Sponsoring Organization:
USDOE
Grant/Contract Number:
AC05-76RL01830
OSTI ID:
1170462
Report Number(s):
PNNL-SA-100391; 47981; KP1704020
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, 111(31):11395-11400, Journal Name: Proceedings of the National Academy of Sciences of the United States of America, 111(31):11395-11400
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 118 works
Citation information provided by
Web of Science

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Morphological Plasticity in a Sulfur-Oxidizing Marine Bacterium from the SUP05 Clade Enhances Dark Carbon Fixation journal May 2019
Oxygen minimum zone cryptic sulfur cycling sustained by offshore transport of key sulfur oxidizing bacteria journal April 2018
Cyanobacterial Diazotrophy and Earth’s Delayed Oxygenation journal September 2016
Putative archaeal viruses from the mesopelagic ocean journal January 2017
Systems-based approaches to unravel multi-species microbial community functioning journal January 2015
Utilization of urea and cyanate in waters overlying and within the eastern tropical north Pacific oxygen deficient zone journal July 2018
Microbial diversity of the Arabian Sea in the Oxygen minimum zones by metagenomics approach posted_content January 2019
A compendium of multi-omic sequence information from the Saanich Inlet water column journal October 2017
Crustacean zooplankton release copious amounts of dissolved organic matter as taurine in the ocean: Dissolved free taurine in oceanic waters journal June 2017
A decade of metaproteomics: Where we stand and what the future holds: PROTEOMICS journal September 2015
Critical decisions in metaproteomics: achieving high confidence protein annotations in a sea of unknowns journal November 2016
Monitoring microbial responses to ocean deoxygenation in a model oxygen minimum zone journal October 2017
Five decades of N2 fixation research in the North Atlantic Ocean journal June 2015
Confounding effects of oxygen and temperature on the TEX 86 signature of marine Thaumarchaeota journal August 2015
Nitrogen and Oxygen Isotope Effects of Ammonia Oxidation by Thermophilic Thaumarchaeota from a Geothermal Water Stream journal May 2016
Widespread methane seepage along the continental margin off Svalbard - from Bjørnøya to Kongsfjorden journal February 2017
Constraint-based stoichiometric modelling from single organisms to microbial communities journal November 2016
Function and functional redundancy in microbial systems journal April 2018
ANPELA: analysis and performance assessment of the label-free quantification workflow for metaproteomic studies journal January 2019
Simple approach for the preparation of 15−15N2-enriched water for nitrogen fixation assessments: evaluation, application and recommendations journal August 2015
Ubiquitous Gammaproteobacteria dominate dark carbon fixation in coastal sediments journal February 2016
Success of chemolithoautotrophic SUP05 and Sulfurimonas GD17 cells in pelagic Baltic Sea redox zones is facilitated by their lifestyles as K- and r -strategists: SUP05 and Sulfurimonas in sulfidic redox zones journal May 2017
Diversity and Composition of Pelagic Prokaryotic and Protist Communities in a Thin Arctic Sea-Ice Regime journal January 2019
Gene swapping in the dead zone journal October 2014
Taurine Is a Major Carbon and Energy Source for Marine Prokaryotes in the North Atlantic Ocean off the Iberian Peninsula journal January 2019
Unexpected genomic features in widespread intracellular bacteria: evidence for motility of marine chlamydiae journal June 2017
The life sulfuric: microbial ecology of sulfur cycling in marine sediments: Microbial sulfur cycling in marine sediments journal May 2017
Agulhas Current properties shape microbial community diversity and potential functionality journal July 2018
Impacts of chemical gradients on microbial community structure journal January 2017
Diverse Marinimicrobia bacteria may mediate coupled biogeochemical cycles along eco-thermodynamic gradients journal November 2017
Inorganic and Organic Carbon Uptake Processes and Their Connection to Microbial Diversity in Meso- and Bathypelagic Arctic Waters (Eastern Fram Strait) journal November 2019
Proteomic Stable Isotope Probing Reveals Biosynthesis Dynamics of Slow Growing Methane Based Microbial Communities journal April 2016
Global prevalence and distribution of genes and microorganisms involved in mercury methylation journal October 2015
Major role of nitrite-oxidizing bacteria in dark ocean carbon fixation journal November 2017
Microorganisms and ocean global change journal May 2017
MS analysis of a dilution series of bacteria:phytoplankton to improve detection of low abundance bacterial peptides journal June 2018
Microbial Community and Functional Structure Significantly Varied among Distinct Types of Paddy Soils But Responded Differently along Gradients of Soil Depth Layers journal May 2017
Nitrospina bacteria in a rocky intertidal habitat (Quintay Bay, central Chile) journal May 2018
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Microbial Surface Colonization and Biofilm Development in Marine Environments journal December 2015
Cultivation of a chemoautotroph from the SUP05 clade of marine bacteria that produces nitrite and consumes ammonium journal July 2016
Microbial niches in marine oxygen minimum zones journal September 2018
Growth phase proteomics of the heterotrophic marine bacterium Ruegeria pomeroyi journal December 2019
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