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

Alyse K. Hawley; Heather M. Brewer; Angela D. Norbeck; Ljiljana Paša-Tolić; Steven J. Hallam

doi:10.1073/pnas.1322132111

New Research In

Edited by Edward F. DeLong, Massachusetts Institute of Technology, Cambridge, MA, and approved June 10, 2014 (received for review November 26, 2013)

Significance

Oxygen is an important organizing principle in marine ecosystems. As oxygen levels decline, energy is increasingly diverted away from higher trophic levels into microbial community metabolism causing changes in carbon and nutrient cycling. Here we use metagenomic and metaproteomic methods to chart in situ metabolic networks linking key microbial players driving carbon and nutrient cycling in a seasonally stratified fjord, Saanich Inlet, a model ecosystem for studying microbial responses to changing levels of water column oxygen deficiency. Based on this evidence, we develop a conceptual model that describes coupling of chemotrophic energy production with dark carbon fixation along defined redox gradients with implications for primary production and possibly carbon sedimentation in expanding marine oxygen minimum zones.

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.

Footnotes

↵¹To whom correspondence should be addressed. Email: shallam{at}mail.ubc.ca.

Author contributions: A.K.H., L.P.-T., and S.J.H. designed research; A.K.H. and H.M.B. performed research; A.K.H. and A.D.N. analyzed data; A.K.H. and S.J.H. wrote the paper; and S.J.H. supervised the project.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The sequence reported in this paper has been deposited in the NCBI BioProject database, www.ncbi.nlm.nih.gov/bioproject (BioProject no. 247822; accession nos. SAMN02781345–SAMN02781359).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1322132111/-/DCSupplemental.

View Full Text