Enhanced metabolic versatility of planktonic sulfur-oxidizing γ-proteobacteria in an oxygen-deficient coastal ecosystem

Abstract

Sulfur-oxidizing γ-proteobacteria are abundant in marine oxygen-deficient waters, and appear to play a key role in a previously unrecognized cryptic sulfur cycle. Metagenomic analyses of members of the uncultured SUP05 lineage in the Canadian seasonally anoxic fjord Saanich Inlet (SI), hydrothermal plumes in the Guaymas Basin (GB) and single cell genomics analysis of two ARCTIC96BD-19 representatives from the South Atlantic Sub-Tropical Gyre (SASG) have shown them to be metabolically versatile. However, SI and GB SUP05 bacteria seem to be obligate chemolithoautotrophs, whereas ARCTIC96BD-19 has the genetic potential for aerobic respiration. Here, we present results of a metagenomic analysis of sulfur-oxidizing γ-proteobacteria (GSO), closely related to the SUP05/ARCTIC96BD-19 clade, from a coastal ecosystem in the eastern South Pacific (ESP). This ecosystem experiences seasonal anoxia and accumulation of nitrite and ammonium at depth, with a corresponding increase in the abundance of GSO representatives. The ESP-GSOs appear to have a significantly different gene complement than those from SI, GB, and SASG. Genomic analyses of de novo assembled contigs indicate the presence of a complete aerobic respiratory complex based on the cytochrome bc1 oxidase. Furthermore, they appear to encode a complete TCA cycle and several transporters for dissolved organic carbon species, suggesting a mixotrophic lifestyle. Thus, the success of sulfur-oxidizing γ-proteobacteria in oxygen-deficient marine ecosystems appears due not only to their previously recognized anaerobic metabolic versatility, but also to their capacity to function under aerobic conditions using different carbon sources. Finally, members of ESP-GSO cluster also have the genetic potential for reducing nitrate to ammonium based on the nirBD genes, and may therefore facilitate a tighter coupling of the nitrogen and sulfur cycles in oxygen-deficient waters.

Vertical segregation among pathways mediating nitrogen loss (N<sub>2</sub> and N<sub>2</sub>O production) across the oxygen gradient in a coastal upwelling ecosystem

“…Nevison et al, 2004;Naqvi et al, 2010), which is clearly evident in this system . N 2 O is a potent greenhouse gas, with a ∼ 300 times greater radiative effect than CO 2 , and also contributes to the destruction of the stratospheric ozone (Ravishankara et al, 2009;Portmann et al, 2012).…”

“…During this period the exhaustion of O 2 also intensified at the bottom (< 5 µmol L −1 ). Thus, three layers are established in the water column as a consequence of the influx of ESSW (Farías et al, 2009): a well oxygenated mixed layer, the oxycline characterized by a marked reduction of the dissolved O 2 content over a compressed vertical scale, and the bottom layer, where the oxygen deficiencies led to potentially anoxic conditions (Murillo et al, 2014). Furthermore, an increased availability of NO , and H 2 S as donors, are also characterized by the intensification of upwelling through the two deeper layers .…”

“…The increase in respiration rates creates extreme O 2 depletion at depth during the summer (∼ 4 µmol L −1 ; Fig. 2e) and occasionally anoxic conditions occur in the bottom waters of this system (Murillo et al, 2014 Fig. 2g, h), which in turn may support chemolitho-and chemoorganotrophic metabolisms including nitrification, anammox, and denitrification, contributing in this way to the loss of fixed N.…”

“…Fixed-N removal occurs predominantly in the form of N 2 , generated by canonical denitrification and anammox processes (Gruber and Sarmiento, 1997;Codispoti et al, 2001;Devol, 2003). The steep oxygen (O 2 ) gradients observed at the OMZ's boundaries further trigger a substantial production and accumulation of nitrous oxide -N 2 O (Naqvi et al, 2010;Dalsgaard et al, 2012), which may eventually be emitted to the atmosphere, thus contributing to the overall N loss. OMZs are notable features of eastern boundary ecosystems (i.e.…”

Ammonium and nitrite oxidation at nanomolar oxygen concentrations in oxygen minimum zone waters

“…Oxygen concentrations in the OMZ core generally fall below the detection limit (<1-10 nmol·L −1 ) of the highly sensitive switchable trace amount oxygen (STOX) sensors (21)(22)(23)(24)(25). The nondetectable levels of oxygen in conjunction with the dominance of gene transcripts associated with anaerobic processes (26) and the long residence time of OMZ waters (upward of several months) imply that the OMZ cores are, to a wide extent, functionally anoxic (22,27).…”