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

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.M arine oxygen (O 2 ) minimum zones (OMZs) are widespread and naturally occurring water column features that arise when respiratory O 2 demand during decomposition of organic matter exceeds O 2 availability in stratified waters. Operationally defined by dissolved O 2 concentrations <20 μM, OMZs promote the use of alternative terminal electron acceptors (TEAs) in microbial energy metabolism that results in climate active gas production including carbon dioxide (CO 2 ), nitrous oxide (N 2 O), and methane (CH 4 ) (1). Currently, OMZs constitute ∼7% of the ocean volume (1, 2). However, global warming promotes conditions for OMZ expansion and intensification, e.g., reduced O 2 solubility and increased stratification, with resulting feedback on the climate system (3, 4).Within OMZs, the use of nitrate (NO 3 − ) and nitrite (NO 2 − ) as TEAs in dissimilatory nitrate reduction (denitrification) and anaerobic ammonium oxidation (anammox) results in fixed nitrogen loss in the form of N 2 O and dinitrogen gas (N 2 ), respectively (5, 6). Because OMZs account for up to 50% of oceanic N 2 production, they have the potential to limit primary production in overlying surface waters (7,8). A recent model suggests that nitrogen fixation in proximity to OMZ waters can balance nitrogen loss processes (9), and several studies along redoxclines in the Eastern Tropical South Pacific and Baltic Sea have measured nitrogen fixation rates that support a close spatial coupling between nitro...

Confounding effects of oxygen and temperature on the TEX 86 signature of marine Thaumarchaeota

“…In addition, TEX 86 values of sediment recovered from the summit of the Murray Ridge seamount that extends into the OMZ of the Arabian Sea were higher than those of sediment recovered from adjacent deeper locations well below the OMZ, and the reconstructed TEX 86 temperatures from sediment cores within the OMZ were more than 5°C higher than the mean annual SST (51). Although surface waters are not O 2 -deficient in these areas, the AOA are of higher abundance in the oxycline and upper OMZ where waters can be oxygen-deficient (9,10). The AOA living under O 2 limitation would likely be the major contributor to the sedimentary GDGTs collected within the Arabian Sea OMZ (51).…”

“…They are generally recognized as the main drivers of oceanic nitrification (5)(6)(7), are closely coupled with anammox organisms in oxygen minimum zones (OMZs) (8)(9)(10), and have been implicated as a source of the greater part of oceanic emissions of the ozone-depleting greenhouse gas nitrous oxide (11). Their wide habitat range suggests both high ecotypic diversity and adaptive capacity (12,13).…”

Integrating biogeochemistry with multiomic sequence information in a model oxygen minimum zone

“…Each gene is a proxy for a particular redox pathway that couples the oxidation of an external electron donor to the reduction of an external electron acceptor. The model builds on a large reservoir of previous work that provides conceptual insight into the microbial metabolic network in Saanich Inlet (12)(13)(14)(16)(17)(18) and includes aerobic remineralization of organic matter (ROM), nitrification, anaerobic ammonium oxidation (anammox), and denitrification coupled to sulfide oxidation (Fig. 1A).…”

“…1A). Certain pathways found in other OMZs, such as aerobic sulfide oxidation (19), dissimilatory nitrate reduction to ammonium (DNRA), (20) and sulfate reduction (5), were excluded from our model based on information from previous studies (12)(13)(14)(16)(17)(18) as well as preliminary tests with model variants (as explained below). Reaction rates (per gene) depend on the concentrations of utilized metabolites according to first-or second-order (Michaelis-Menten) kinetics (21).…”

“…Our model explicitly describes DNA, mRNA, and protein dynamics as well as biogeochemical reaction rates at ecosystem scales. To calibrate and validate our model, we use geochemical depth profiles; rate measurements for N cycling processes; and metagenomic, metatranscriptomic, and metaproteomic sequence data as well as qPCR-based abundance estimates for SUP05 Gammaproteobacteria-the dominant denitrifiers in Saanich Inlet (14), all obtained from a single location in Saanich Inlet in early or mid-2010.…”