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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

Relationship between total dissolved Fe:Cu molar ratios and dissolved O2 concentrations in seawater samples from 0 to 1000 m water depth. Closed circles are Atlantic Ocean samples taken along the A16N transect from 62°N to 5°S along 20–30°W on CLIVAR cruise A16N (see Supplementary Figure 1 for station maps). Open circles are Pacific Ocean samples taken along the CLIVAR cruise P16N and P16S transect from 37°N to 46°S along 150°W (Supplementary Figure 1). Red, blue and green circles ETNP NH-1315, ETSP AT-15-61, and BATS samples, respectively, for which full depth profiles are shown in Figure 1F. A linear fit equation of the Atlantic Ocean data (R2 = 0.75) is provided. A linear fit equation is not provided for the Pacific Ocean data due to the low R2 value (0.12).
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Figure 2: Relationship between total dissolved Fe:Cu molar ratios and dissolved O2 concentrations in seawater samples from 0 to 1000 m water depth. Closed circles are Atlantic Ocean samples taken along the A16N transect from 62°N to 5°S along 20–30°W on CLIVAR cruise A16N (see Supplementary Figure 1 for station maps). Open circles are Pacific Ocean samples taken along the CLIVAR cruise P16N and P16S transect from 37°N to 46°S along 150°W (Supplementary Figure 1). Red, blue and green circles ETNP NH-1315, ETSP AT-15-61, and BATS samples, respectively, for which full depth profiles are shown in Figure 1F. A linear fit equation of the Atlantic Ocean data (R2 = 0.75) is provided. A linear fit equation is not provided for the Pacific Ocean data due to the low R2 value (0.12).

Mentions: Molar Fe:Cu ratios vs. O2 were compared on an ocean basin scale to identify global gradients over which metalloenzyme distributions were predicted to vary. Fe:Cu ratios for seawater samples from 0 to 1000 m water depth were compiled from Atlantic and Pacific CLIVAR ocean basin scale cruises (Figure 2). Fe:Cu molar ratios from the Atlantic A16N transect ranged from 0.08 to 1.6 (0.08–1.5 nM dFeT; 0.5–1.3 nM dCuT) over 67–284 μM O2 with a significant inverse relationship between Fe:Cu ratios and O2 concentrations that could be fit to the linear equation Fe:Cu molar ratio = −0.006[μM O2] + 1.8 (R2 = 0.75; Figure 2). Highest Fe:Cu and lowest O2 along the Atlantic transect were found at 200–600 m depth in the tropics (~4–14°N).


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)

Relationship between total dissolved Fe:Cu molar ratios and dissolved O2 concentrations in seawater samples from 0 to 1000 m water depth. Closed circles are Atlantic Ocean samples taken along the A16N transect from 62°N to 5°S along 20–30°W on CLIVAR cruise A16N (see Supplementary Figure 1 for station maps). Open circles are Pacific Ocean samples taken along the CLIVAR cruise P16N and P16S transect from 37°N to 46°S along 150°W (Supplementary Figure 1). Red, blue and green circles ETNP NH-1315, ETSP AT-15-61, and BATS samples, respectively, for which full depth profiles are shown in Figure 1F. A linear fit equation of the Atlantic Ocean data (R2 = 0.75) is provided. A linear fit equation is not provided for the Pacific Ocean data due to the low R2 value (0.12).
© Copyright Policy
Related In: Results  -  Collection

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

Figure 2: Relationship between total dissolved Fe:Cu molar ratios and dissolved O2 concentrations in seawater samples from 0 to 1000 m water depth. Closed circles are Atlantic Ocean samples taken along the A16N transect from 62°N to 5°S along 20–30°W on CLIVAR cruise A16N (see Supplementary Figure 1 for station maps). Open circles are Pacific Ocean samples taken along the CLIVAR cruise P16N and P16S transect from 37°N to 46°S along 150°W (Supplementary Figure 1). Red, blue and green circles ETNP NH-1315, ETSP AT-15-61, and BATS samples, respectively, for which full depth profiles are shown in Figure 1F. A linear fit equation of the Atlantic Ocean data (R2 = 0.75) is provided. A linear fit equation is not provided for the Pacific Ocean data due to the low R2 value (0.12).
Mentions: Molar Fe:Cu ratios vs. O2 were compared on an ocean basin scale to identify global gradients over which metalloenzyme distributions were predicted to vary. Fe:Cu ratios for seawater samples from 0 to 1000 m water depth were compiled from Atlantic and Pacific CLIVAR ocean basin scale cruises (Figure 2). Fe:Cu molar ratios from the Atlantic A16N transect ranged from 0.08 to 1.6 (0.08–1.5 nM dFeT; 0.5–1.3 nM dCuT) over 67–284 μM O2 with a significant inverse relationship between Fe:Cu ratios and O2 concentrations that could be fit to the linear equation Fe:Cu molar ratio = −0.006[μM O2] + 1.8 (R2 = 0.75; Figure 2). Highest Fe:Cu and lowest O2 along the Atlantic transect were found at 200–600 m depth in the tropics (~4–14°N).

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