Oxygen minimum zone cryptic sulfur cycling sustained by offshore transport of key sulfur oxidizing bacteria

Abstract

Members of the gammaproteobacterial clade SUP05 couple water column sulfide oxidation to nitrate reduction in sulfidic oxygen minimum zones (OMZs). Their abundance in offshore OMZ waters devoid of detectable sulfide has led to the suggestion that local sulfate reduction fuels SUP05-mediated sulfide oxidation in a so-called "cryptic sulfur cycle". We examined the distribution and metabolic capacity of SUP05 in Peru Upwelling waters, using a combination of oceanographic, molecular, biogeochemical and single-cell techniques. A single SUP05 species, ^U Thioglobus perditus, was found to be abundant and active in both sulfidic shelf and sulfide-free offshore OMZ waters. Our combined data indicated that mesoscale eddy-driven transport led to the dispersal of ^U T. perditus and elemental sulfur from the sulfidic shelf waters into the offshore OMZ region. This offshore transport of shelf waters provides an alternative explanation for the abundance and activity of sulfide-oxidizing denitrifying bacteria in sulfide-poor offshore OMZ waters.

Fig. 1

Station and mesoscale eddy location relative to near-surface chlorophyll a and maximum dissolved sulfide concentrations. a Monthly composite MODIS image (see Methods for source) showing near-surface chlorophyll concentrations for March 2013, where the arrows indicate cross-shelf advected filaments. b MODIS image of near-surface chlorophyll concentrations for 24 February 2013. The main water column sampling stations (U1, L1, and L2) are marked with black stars; additional stations with white circles. Times of station sampling are provided in Supplementary Table 1. Formation and propagation of the eddy westward occurring over time is indicated: E1 represents the initial eddy formation from 28 January to 3 February; E2 shows the expansion of the eddy (7–12 February 2013); and E3 is the location of the eddy when the image was taken (24 February 2013). c Maximum sulfide concentration reported for water masses with densities between 26.1 and 26.2 kg m⁻³

Fig. 2

Distribution of concentrations, abundances, and bulk and single-cell activities in the Peru Upwelling OMZ as a function of distance from the coast. The composite plots show depth and cross-shelf distribution a nitrate, b dissolved sulfide, c elemental sulfur, d % total bacteria (DAPI) identified as SUP05, e bulk rates of denitrification, and f single-cell determined rates of CO₂ fixed by SUP05 at the time of eddy-induced offshore transport of shelf waters. Note that station L2 (not included in composite) was located near station L1, but occupied 11 days later. Black dots indicate sample depths at each station included in the composite plots

Fig. 3

Phylogenetic diversity of GSO 16S rRNA genes recovered from sulfidic and non-sulfidic stations from the Peruvian upwelling region. The phylogenetic tree was calculated using the neighbor joining and RAxML methods, including various filters, an unrooted consensus tree is shown. The typeface in blue, black, and green represent sequences recovered from other studies. Typeface in red represents sequences recovered from sulfidic stations U1 and U1a, and from offshore stations L1, L2, and 378 (Supplementary Table 1). The coverage and specificity of the newly designed FISH GSO131 probe is indicated by the red brackets; for overall probe coverage details see Supplementary Table 3. The broad coverage GSO477 probe is indicated by the gray bracket

Fig. 4

SUP05 single-cell activity and sulfur content of ETSP-SUP05 bacteria. a CO₂ fixation rates based on ¹³C-bicarbonate uptake into SUP05 cells. b Normalized single-cell sulfur content. The mean (red line) and median (black line) are indicated. The boxes represent the distribution of data with 95th and 5th percentiles and outliers are indicated by the black circles. Standard deviations bars are shown. The number of SUP05 cells analyzed at station–depths were as follows: U1–30 m (48 cells); U1–60 m (59 cells); L1–50 m (35 cells); L1–200 m (32 cells); and L2–200 m (23 cells)

Fig. 5

Key metabolic pathways encoded in a SUP05 ^UThioglobus perditus population genome bin: Nar, nitrate reductase; Nir, nitrite reductase; Nor, nitric oxide reductase; Nos, nitrous oxide reductase; Dsr, dissmilatory sulfite reductase; Apr, adenylylsulfate reductase; Sat, sulfate adenylyltransferase; Fcc, sulfide-binding flavoprotein; Sqr, sulfide-quinone reductase. The metabolic prediction is based on a 95% complete SUP05 draft genome recovered from station U1. For a complete list of genes please refer to Supplementary Table 4