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PMID: 25053816 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

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

Proceedings of the National Academy of Sciences of the United States of America ·Vol. 111 ·No. 31 ·2014-08-05 ·Pages 11395-400

Hawley AK, Brewer HM, Norbeck AD, Paša-Tolić L, Hallam SJ

Abstract

Marine oxygen minimum zones (OMZs) are intrinsic water column features arising from respiratory oxygen demand during organic matter degradation in stratified waters. Currently OMZs are expanding due to global climate change with resulting feedback on marine ecosystem function. Here we use metaproteomics to chart spatial and temporal patterns of gene expression along defined redox gradients in a seasonally stratified fjord 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 were differentially expressed across the redoxcline and covaried with distribution patterns of ubiquitous OMZ microbes including Thaumarchaeota, Nitrospina, Nitrospira, Planctomycetes, and SUP05/ARCTIC96BD-19 Gammaproteobacteria. Nitrification and inorganic carbon fixation pathways affiliated with Thaumarchaeota dominated dysoxic waters, and denitrification, sulfur oxidation, and inorganic carbon fixation pathways affiliated with the SUP05 group of nitrate-reducing sulfur oxidizers dominated suboxic and anoxic waters. Nitrifier nitrite oxidation and anammox pathways affiliated with Nirospina, Nitrospira, and Planctomycetes, respectively, also exhibited redox partitioning between dysoxic and suboxic waters. The numerical abundance of SUP05 proteins mediating inorganic carbon fixation under anoxic conditions suggests that SUP05 will become increasingly important in global ocean carbon and nutrient cycling as OMZs expand.

MeSH Terms
Archaea/genetics,metabolism Bacteria/genetics,metabolism Cluster Analysis Ecosystem Energy Metabolism Gene Expression Profiling Gene Expression Regulation, Archaeal Gene Expression Regulation, Bacterial Genes, Archaeal Genes, Bacterial Models, Biological Nitrogen/metabolism Oxidation-Reduction Oxygen/metabolism Proteome/metabolism Proteomics/methods Sulfur/metabolism Water/chemistry
Chemicals
Proteome Water Sulfur Nitrogen Oxygen
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Hawley Alyse K
Department of Microbiology and Immunology.
Brewer Heather M
Biological and Computational Sciences Division, Pacific Northwest National Laboratory, Richland, WA 99352.
Norbeck Angela D
Biological and Computational Sciences Division, Pacific Northwest National Laboratory, Richland, WA 99352.
Paša-Tolić Ljiljana
Biological and Computational Sciences Division, Pacific Northwest National Laboratory, Richland, WA 99352.
Hallam Steven J
Department of Microbiology and Immunology,Graduate Program in Bioinformatics, andGenome Sciences and Technology Training Program, University of British Columbia, Vancouver, BC, Canada V6T 1Z3; and [email protected].
References (41)
41 references, click to expand
  1. The Genome of Nitrospina gracilis Illuminates the Metabolism and Evolution of the Major Marine Nitrite Oxidizer.
    Front Microbiol. 2013 Feb 21;4:27 PMID: 23439773
  2. Active nitrogen-fixing heterotrophic bacteria at and below the chemocline of the central Baltic Sea.
    ISME J. 2013 Jul;7(7):1413-23 PMID: 23446833
  3. Diversity and population structure of Marine Group A bacteria in the Northeast subarctic Pacific Ocean.
    ISME J. 2013 Feb;7(2):256-68 PMID: 23151638
  4. Detoxification of sulphidic African shelf waters by blooming chemolithotrophs.
    Nature. 2009 Jan 29;457(7229):581-4 PMID: 19078958
  5. Microbial ecology of expanding oxygen minimum zones.
    Nat Rev Microbiol. 2012 May 14;10(6):381-94 PMID: 22580367
  6. Revising the nitrogen cycle in the Peruvian oxygen minimum zone.
    Proc Natl Acad Sci U S A. 2009 Mar 24;106(12):4752-7 PMID: 19255441
  7. Denitrification as the dominant nitrogen loss process in the Arabian Sea.
    Nature. 2009 Sep 3;461(7260):78-81 PMID: 19727197
  8. Ocean deoxygenation in a warming world.
    Ann Rev Mar Sci. 2010;2:199-229 PMID: 21141663
  9. Isotopic signature of N(2)O produced by marine ammonia-oxidizing archaea.
    Science. 2011 Sep 2;333(6047):1282-5 PMID: 21798895
  10. Microbial metatranscriptomics in a permanent marine oxygen minimum zone.
    Environ Microbiol. 2012 Jan;14(1):23-40 PMID: 21210935
  11. 13C-isotope analyses reveal that chemolithoautotrophic Gamma- and Epsilonproteobacteria feed a microbial food web in a pelagic redoxcline of the central Baltic Sea.
    Environ Microbiol. 2009 Feb;11(2):326-37 PMID: 18793316
  12. Evolution of an octahaem cytochrome c protein family that is key to aerobic and anaerobic ammonia oxidation by bacteria.
    Environ Microbiol. 2008 Nov;10(11):3150-63 PMID: 18761666
  13. Phylogeny of the bacterial superfamily of Crp-Fnr transcription regulators: exploiting the metabolic spectrum by controlling alternative gene programs.
    FEMS Microbiol Rev. 2003 Dec;27(5):559-92 PMID: 14638413
  14. Molecular tools for investigating microbial community structure and function in oxygen-deficient marine waters.
    Methods Enzymol. 2013;531:305-29 PMID: 24060128
  15. Metagenome of a versatile chemolithoautotroph from expanding oceanic dead zones.
    Science. 2009 Oct 23;326(5952):578-82 PMID: 19900896
  16. A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria.
    Proc Natl Acad Sci U S A. 2010 Jul 27;107(30):13479-84 PMID: 20624973
  17. Giant hydrogen sulfide plume in the oxygen minimum zone off Peru supports chemolithoautotrophy.
    PLoS One. 2013 Aug 21;8(8):e68661 PMID: 23990875
  18. Microbial community structure across fluid gradients in the Juan de Fuca Ridge hydrothermal system.
    FEMS Microbiol Ecol. 2013 Feb;83(2):324-39 PMID: 22928928
  19. Evidence for hydrogen oxidation and metabolic plasticity in widespread deep-sea sulfur-oxidizing bacteria.
    Proc Natl Acad Sci U S A. 2013 Jan 2;110(1):330-5 PMID: 23263870
  20. Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea.
    Proc Natl Acad Sci U S A. 2010 May 11;107(19):8818-23 PMID: 20421470
  21. Microbial nitrogen cycling processes in oxygen minimum zones.
    Ann Rev Mar Sci. 2011;3:317-45 PMID: 21329208
  22. Insights into the phylogeny and coding potential of microbial dark matter.
    Nature. 2013 Jul 25;499(7459):431-7 PMID: 23851394
  23. Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota.
    PLoS Biol. 2006 Apr;4(4):e95 PMID: 16533068
  24. Nitrogen fixation in denitrified marine waters.
    PLoS One. 2011;6(6):e20539 PMID: 21687726
  25. Microbial oceanography of anoxic oxygen minimum zones.
    Proc Natl Acad Sci U S A. 2012 Oct 2;109(40):15996-6003 PMID: 22967509
  26. Spatial coupling of nitrogen inputs and losses in the ocean.
    Nature. 2007 Jan 11;445(7124):163-7 PMID: 17215838
  27. Primary production of the biosphere: integrating terrestrial and oceanic components
    Science. 1998 Jul 10;281(5374):237-40 PMID: 9657713
  28. Isolation of an autotrophic ammonia-oxidizing marine archaeon.
    Nature. 2005 Sep 22;437(7058):543-6 PMID: 16177789
  29. Deciphering the evolution and metabolism of an anammox bacterium from a community genome.
    Nature. 2006 Apr 6;440(7085):790-4 PMID: 16598256
  30. Nitrite oxidation in the upper water column and oxygen minimum zone of the eastern tropical North Pacific Ocean.
    ISME J. 2013 Nov;7(11):2192-205 PMID: 23804152
  31. Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea.
    Proc Natl Acad Sci U S A. 2007 Apr 24;104(17):7104-9 PMID: 17420469
  32. Microbial community dynamics in a seasonally anoxic fjord: Saanich Inlet, British Columbia.
    Environ Microbiol. 2010 Jan;12(1):172-91 PMID: 19788414
  33. Nitrite oxidation in the Namibian oxygen minimum zone.
    ISME J. 2012 Jun;6(6):1200-9 PMID: 22170426
  34. One carbon metabolism in SAR11 pelagic marine bacteria.
    PLoS One. 2011;6(8):e23973 PMID: 21886845
  35. Facets of diazotrophy in the oxygen minimum zone waters off Peru.
    ISME J. 2014 Nov;8(11):2180-92 PMID: 24813564
  36. Beyond the Calvin cycle: autotrophic carbon fixation in the ocean.
    Ann Rev Mar Sci. 2011;3:261-89 PMID: 21329206
  37. Metagenomic analysis of size-fractionated picoplankton in a marine oxygen minimum zone.
    ISME J. 2014 Jan;8(1):187-211 PMID: 24030599
  38. A cryptic sulfur cycle in oxygen-minimum-zone waters off the Chilean coast.
    Science. 2010 Dec 3;330(6009):1375-8 PMID: 21071631
  39. Sulfur oxidizers dominate carbon fixation at a biogeochemical hot spot in the dark ocean.
    ISME J. 2013 Dec;7(12):2349-60 PMID: 23842654
  40. Potential for chemolithoautotrophy among ubiquitous bacteria lineages in the dark ocean.
    Science. 2011 Sep 2;333(6047):1296-300 PMID: 21885783
  41. Gene-centric approach to integrating environmental genomics and biogeochemical models.
    Proc Natl Acad Sci U S A. 2014 Feb 4;111(5):1879-84 PMID: 24449851
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
DOI
10.1073/pnas.1322132111
Email
[email protected]
Published
2014-08-05
Epub
2014-00-22
Pages
11395-400
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC4128106
Subset
IM
External Links
PubMed source DOI: 10.1073/pnas.1322132111 PMC Full Text View journal details
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