Meta-omic signatures of microbial metal and nitrogen cycling in marine oxygen minimum zones

Abstract

Iron (Fe) and copper (Cu) are essential cofactors for microbial metalloenzymes, but little is known about the metalloenyzme inventory of anaerobic marine microbial communities despite their importance to the nitrogen cycle. We compared dissolved O2, NO3−, NO2−, Fe and Cu concentrations with nucleic acid sequences encoding Fe and Cu-binding proteins in 21 metagenomes and 9 metatranscriptomes from Eastern Tropical North and South Pacific oxygen minimum zones and 7 metagenomes from the Bermuda Atlantic Time-series Station. Dissolved Fe concentrations increased sharply at upper oxic-anoxic transition zones, with the highest Fe:Cu molar ratio (1.8) occurring at the anoxic core of the Eastern Tropical North Pacific oxygen minimum zone and matching the predicted maximum ratio based on data from diverse ocean sites. The relative abundance of genes encoding Fe-binding proteins was negatively correlated with O2, driven by significant increases in genes encoding Fe-proteins involved in dissimilatory nitrogen metabolisms under anoxia. Transcripts encoding cytochrome c oxidase, the Fe- and Cu-containing terminal reductase in aerobic respiration, were positively correlated with O2 content. A comparison of the taxonomy of genes encoding Fe- and Cu-binding vs. bulk proteins in OMZs revealed that Planctomycetes represented a higher percentage of Fe genes while Thaumarchaeota represented a higher percentage of Cu genes, particularly at oxyclines. These results are broadly consistent with higher relative abundance of genes encoding Fe-proteins in the genome of a marine planctomycete vs. higher relative abundance of genes encoding Cu-proteins in the genome of a marine thaumarchaeote. These findings highlight the importance of metalloenzymes for microbial processes in oxygen minimum zones and suggest preferential Cu use in oxic habitats with Cu > Fe vs. preferential Fe use in anoxic niches with Fe > Cu.

Metabolic potential and in situ activity of marine Marinimicrobia bacteria in an anoxic water column

“…In addition, under anoxic conditions, iron is present in the more soluble ferrous state (Fe 2+ ) and can be used as an electron donor. To our knowledge, however, while anoxic OMZs are relatively enriched in dissolved Fe 2+ (Glass et al ., ), anaerobic water column Fe(II) oxidation has not been observed. Overall, the high transcriptional activity of fep and fec homologues in Marinimicrobia suggests a need for further investigation of Fe utilization in OMZs.…”

“…Fe is required for a multitude of biochemical redox reactions spanning diverse metabolisms, such as respiration and oxidation of sulfur and nitrogen compounds. Indeed, a high proportional representation of iron‐requiring redox enzymes, such as nitrate reductases, has been observed previously in OMZs (Glass et al ., ), and nitrate reductase‐encoding transcripts were also abundant in the Golfo Dulce at 90 meters. In addition, under anoxic conditions, iron is present in the more soluble ferrous state (Fe 2+ ) and can be used as an electron donor.…”

Elevated trace metal content of prokaryotic communities associated with marine oxygen deficient zones

“…This may reflect elevated Cu demand, a shift in Cu speciation/bioavailability, or Cu accumulation by heterotrophic organisms living in the ODZ core compared to the autotrophic–dominated upper ODZ. Interestingly, recent meta–omic results predict the opposite effect, with greater Cu demand expected for upper ODZ species and greater Fe demand in the ODZ core (Glass et al ).…”

Species‐Dependent Chromium Isotope Fractionation Across the Eastern Tropical North Pacific Oxygen Minimum Zone

“…Samples for δ 53 Cr analysis were taken from the 30–500‐m depth range (Figures and ) on R/V New Horizon cruise NH‐1315 in June 2013 offshore Manzanillo, Mexico at station 2 (18.9°N, 108.8°W), station 4 (18.9°N, 106.3°W), and station 10 (18.8°N, 104.7°W; Glass et al, ). The dissolved O 2 concentration drops sharply to <4 μM at ~70 m at stations 4 and 10 and at ~120 m depth at station 2, due to vertical thinning of the OMZ toward the west.…”