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

Jennifer B Glass,William M Landing,Piyush Ranjan,Frank J Stewart,Cecilia B Kretz,Kevin L Vergin,Kristen N Buck,James W Moffett,Sangita Ganesh,Stephen J Giovannoni,Peter L Morton,Sherry L Seston

doi:10.3389/fmicb.2015.00998

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, NO, NO, 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.

Highlights

Marine oxygen minimum zones (OMZs) play important roles in global biogeochemical cycles and are expanding throughout the world’s oceans (Stramma et al, 2008; Keeling et al, 2010)
The base of the upper oxycline deepened with increasing distance from shore, from 70 m at Eastern Tropical North Pacific (ETNP) station 6, to 200 m at Eastern Tropical South Pacific (ETSP) stations 10 and 11 (Figure 1A, Supplementary Figure 1)
The lower oxycline was deeper in the ETNP (800–900 m) than in the ETSP (400–700 m; Figure 1A)

Summary

Introduction

Marine oxygen minimum zones (OMZs) play important roles in global biogeochemical cycles and are expanding throughout the world’s oceans (Stramma et al, 2008; Keeling et al, 2010). Diverse organisms mediate OMZ N cycling, but members of the Planctomycetes, Thaumarchaeota and Nitrospinae phyla appear to perform the majority of anammox, ammonia oxidation and nitrite oxidation, respectively, based on rate measurements coupled to primer-based 16S rRNA and functional gene sequencing, as well as metagenomic and metatranscriptomic approaches (Lam et al, 2009; Füssel et al, 2011; Newell et al, 2011; Stewart et al, 2012; Ulloa et al, 2012; Wright et al, 2012; Ganesh et al, 2014, 2015; Hawley et al, 2014). Fe has been shown to be an important micronutrient, electron acceptor (as Fe3+) and electron donor (as Fe2+) for anammox bacteria (Van De Vossenberg et al, 2008; Oshiki et al, 2013; Van de Vossenberg et al, 2013; Ali et al, 2014), suggesting that it may play a role in marine OMZs where anammox occurs

Methods

Results

Conclusion