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

Glass JB, Kretz CB, Ganesh S, Ranjan P, Seston SL, Buck KN, Landing WM, Morton PL, Moffett JW, Giovannoni SJ, Vergin KL, Stewart FJ - Front Microbiol (2015)

Bottom Line: Transcripts encoding cytochrome c oxidase, the Fe- and Cu-containing terminal reductase in aerobic respiration, were positively correlated with O2 content.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.

View Article: PubMed Central - PubMed

Affiliation: School of Earth and Atmospheric Sciences, Georgia Institute of Technology Atlanta, GA, USA ; School of Biology, Georgia Institute of Technology Atlanta, GA, USA.

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[Formula: see text], NO[Formula: see text], 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.

No MeSH data available.


Related in: MedlinePlus

Depth profiles of dissolved (A) O2, (B) NO, (C) NO, (D) Fe, (E) Cu and (F) Fe:Cu molar ratios for stations 2, 4, 6 and 10 in the ETNP, stations 1 (BIG RAPA) and 3 (MOOMZ), 10 and 11 in the ETSP, and BATS in the Sargasso Sea, North Atlantic Ocean (see Supplementary Figure 1 for station maps). Gray boxes depict oxygen and depth ranges for each zone and their labels are shown in (A).
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Figure 1: Depth profiles of dissolved (A) O2, (B) NO, (C) NO, (D) Fe, (E) Cu and (F) Fe:Cu molar ratios for stations 2, 4, 6 and 10 in the ETNP, stations 1 (BIG RAPA) and 3 (MOOMZ), 10 and 11 in the ETSP, and BATS in the Sargasso Sea, North Atlantic Ocean (see Supplementary Figure 1 for station maps). Gray boxes depict oxygen and depth ranges for each zone and their labels are shown in (A).

Mentions: Oxygen and depth profiles were used to identify five zones through ETNP and ETSP OMZs: the upper oxic zone (15–30 m; >200 μM O2), the upper oxycline (50–85 m; 10–200 μM O2), the upper OMZ (70–125 m; < 10 μM O2), the core OMZ (200–300 m; < 5 μM O2) and the lower oxycline (500–1000 m; 5–50 μM O2). The base of the upper oxycline deepened with increasing distance from shore, from 70 m at ETNP station 6, to 200 m at 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). The secondary NO maximum was most pronounced at nearshore stations (5–6 μM NO at ETNP stations 4, 6, and 10 at ETSP station 3) and was weaker and deeper at offshore stations (1–2 μM NO at ETNP station 2 and ETSP station 10; Figure 1B). Secondary NO maxima corresponded with NO minima in all OMZ stations (Figure 1C). At BATS, O2 did not drop below 150 μM and NO was undetectable at all depths, while NO increased from under detection at 0–120 m to 3 μM at 250 m (Figures 1A–C).


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

Glass JB, Kretz CB, Ganesh S, Ranjan P, Seston SL, Buck KN, Landing WM, Morton PL, Moffett JW, Giovannoni SJ, Vergin KL, Stewart FJ - Front Microbiol (2015)

Depth profiles of dissolved (A) O2, (B) NO, (C) NO, (D) Fe, (E) Cu and (F) Fe:Cu molar ratios for stations 2, 4, 6 and 10 in the ETNP, stations 1 (BIG RAPA) and 3 (MOOMZ), 10 and 11 in the ETSP, and BATS in the Sargasso Sea, North Atlantic Ocean (see Supplementary Figure 1 for station maps). Gray boxes depict oxygen and depth ranges for each zone and their labels are shown in (A).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4585252&req=5

Figure 1: Depth profiles of dissolved (A) O2, (B) NO, (C) NO, (D) Fe, (E) Cu and (F) Fe:Cu molar ratios for stations 2, 4, 6 and 10 in the ETNP, stations 1 (BIG RAPA) and 3 (MOOMZ), 10 and 11 in the ETSP, and BATS in the Sargasso Sea, North Atlantic Ocean (see Supplementary Figure 1 for station maps). Gray boxes depict oxygen and depth ranges for each zone and their labels are shown in (A).
Mentions: Oxygen and depth profiles were used to identify five zones through ETNP and ETSP OMZs: the upper oxic zone (15–30 m; >200 μM O2), the upper oxycline (50–85 m; 10–200 μM O2), the upper OMZ (70–125 m; < 10 μM O2), the core OMZ (200–300 m; < 5 μM O2) and the lower oxycline (500–1000 m; 5–50 μM O2). The base of the upper oxycline deepened with increasing distance from shore, from 70 m at ETNP station 6, to 200 m at 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). The secondary NO maximum was most pronounced at nearshore stations (5–6 μM NO at ETNP stations 4, 6, and 10 at ETSP station 3) and was weaker and deeper at offshore stations (1–2 μM NO at ETNP station 2 and ETSP station 10; Figure 1B). Secondary NO maxima corresponded with NO minima in all OMZ stations (Figure 1C). At BATS, O2 did not drop below 150 μM and NO was undetectable at all depths, while NO increased from under detection at 0–120 m to 3 μM at 250 m (Figures 1A–C).

Bottom Line: Transcripts encoding cytochrome c oxidase, the Fe- and Cu-containing terminal reductase in aerobic respiration, were positively correlated with O2 content.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.

View Article: PubMed Central - PubMed

Affiliation: School of Earth and Atmospheric Sciences, Georgia Institute of Technology Atlanta, GA, USA ; School of Biology, Georgia Institute of Technology Atlanta, GA, USA.

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[Formula: see text], NO[Formula: see text], 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.

No MeSH data available.


Related in: MedlinePlus