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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

Taxonomy of metagenomic (A,C,E) and metatranscriptomic (B,D,F) sequences for bulk protein-coding genes (A,B), Cu-binding proteins (C,D), and Fe-binding proteins (E,F) through five zones in ETNP and ETSP OMZs and at BATS. The OP1 candidate phylum is not listed because it was not included in the MEGAN database, but comprises the majority of formate dehydrogenase transcripts classified as dissimilatory membrane-bound nitrate reductase in OMZ cores based on BLASTX analysis.
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Figure 3: Taxonomy of metagenomic (A,C,E) and metatranscriptomic (B,D,F) sequences for bulk protein-coding genes (A,B), Cu-binding proteins (C,D), and Fe-binding proteins (E,F) through five zones in ETNP and ETSP OMZs and at BATS. The OP1 candidate phylum is not listed because it was not included in the MEGAN database, but comprises the majority of formate dehydrogenase transcripts classified as dissimilatory membrane-bound nitrate reductase in OMZ cores based on BLASTX analysis.

Mentions: Bacteria comprised 75–96% of total protein-coding DNA and RNA sequences in OMZ and BATS datasets (Supplementary Table 4). At the phylum level, Proteobacteria were consistently dominant (42–63% of total DNA and RNA protein-coding sequences; Figures 3A,B). Of the known N-cycling phyla, Planctomycetes (including anammox-capable Brocadiales) reached 10% of total DNA and RNA sequences within OMZs and Nitrospinae comprised up to 20% of total RNA sequences in the upper OMZ in the ETSP. Archaea comprised 0–9% of total protein-coding DNA sequences at BATS vs. 2–22% of total DNA and RNA protein-coding sequences in OMZs (Supplementary Table 4), with notable peaks of Thaumarchaeota in the oxyclines and upper OMZ (Figures 3A,B). Eukaryotes, dominated by Opisthokonta, Stramenopiles and Viridiplantae, comprised 1–5% of total protein-coding DNA sequences in OMZs vs. 6–8% at BATS (Figure 3A; Supplementary Table 4). The slightly higher percentage of eukaryotes at BATS may be due to the inclusion of larger cells in BATS samples where a pre-filter was not used and thus all cells >0.2 μm were collected vs. OMZ metagenomes comprised solely of the 0.2–1.6 μm size fraction. Alternatively, microbial eukaryotes may be relatively more abundant in oxic waters.


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)

Taxonomy of metagenomic (A,C,E) and metatranscriptomic (B,D,F) sequences for bulk protein-coding genes (A,B), Cu-binding proteins (C,D), and Fe-binding proteins (E,F) through five zones in ETNP and ETSP OMZs and at BATS. The OP1 candidate phylum is not listed because it was not included in the MEGAN database, but comprises the majority of formate dehydrogenase transcripts classified as dissimilatory membrane-bound nitrate reductase in OMZ cores based on BLASTX analysis.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 3: Taxonomy of metagenomic (A,C,E) and metatranscriptomic (B,D,F) sequences for bulk protein-coding genes (A,B), Cu-binding proteins (C,D), and Fe-binding proteins (E,F) through five zones in ETNP and ETSP OMZs and at BATS. The OP1 candidate phylum is not listed because it was not included in the MEGAN database, but comprises the majority of formate dehydrogenase transcripts classified as dissimilatory membrane-bound nitrate reductase in OMZ cores based on BLASTX analysis.
Mentions: Bacteria comprised 75–96% of total protein-coding DNA and RNA sequences in OMZ and BATS datasets (Supplementary Table 4). At the phylum level, Proteobacteria were consistently dominant (42–63% of total DNA and RNA protein-coding sequences; Figures 3A,B). Of the known N-cycling phyla, Planctomycetes (including anammox-capable Brocadiales) reached 10% of total DNA and RNA sequences within OMZs and Nitrospinae comprised up to 20% of total RNA sequences in the upper OMZ in the ETSP. Archaea comprised 0–9% of total protein-coding DNA sequences at BATS vs. 2–22% of total DNA and RNA protein-coding sequences in OMZs (Supplementary Table 4), with notable peaks of Thaumarchaeota in the oxyclines and upper OMZ (Figures 3A,B). Eukaryotes, dominated by Opisthokonta, Stramenopiles and Viridiplantae, comprised 1–5% of total protein-coding DNA sequences in OMZs vs. 6–8% at BATS (Figure 3A; Supplementary Table 4). The slightly higher percentage of eukaryotes at BATS may be due to the inclusion of larger cells in BATS samples where a pre-filter was not used and thus all cells >0.2 μm were collected vs. OMZ metagenomes comprised solely of the 0.2–1.6 μm size fraction. Alternatively, microbial eukaryotes may be relatively more abundant in oxic waters.

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