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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

Schematic of major metabolisms involved in O2 (photosynthesis and aerobic respiration) and nitrogen cycling (nitrification, canonical denitrification and anammox) in four zones in OMZs. Metalloenzymes are depicted as red (Fe) or green (Cu) circles. Shading indicates relative abundance of transcripts normalized to total Fe and Cu transcripts (see legend) from ETNP station 6 and ETSP station 3 metatranscriptomes (see Supplementary Table 5 for transcript abundances). Abbreviations: Cyt c, cytochrome c; OEC, oxygen evolving complex; red, reduced; ox, oxidized; Cox, cytochrome c oxidase; Nar, dissimilatory nitrate reductase; Nxr, nitrite oxidoreductase; NirK, copper-containing nitrite reductase; NirS, iron-containing nitrite reductase; Nor, nitric oxidase reductase. NirK is divided into two groups: one for nitrifier nirK transcripts most related to uncultured Thaumarchaeota thought to perform ammonia oxidation and nitrite-oxidizing bacteria, and the other in the denitrification pathway for all other nirK transcripts. Nar and Nxr are contained within the formate dehydrogenase protein fold family (SCOPe ID: c.81.1.1), NirK is contained within the multidomain cupredoxin protein fold family (SCOPe ID: b.6.1.3), Nor is contained within the ROO N-terminal domain-like protein fold family (SCOPe ID: d.157.1.3), and NirS is classified as SCOPe ID b.70.2.1 (C-terminus) and a.3.1.2 (N-terminus). Known nitrogen cycle metalloenzymes not yet in the SCOPe database (ammonia monooxygenase in nitrification and hydrazine synthase/reductase in anammox) are represented as colored arrows. Question mark indicates the unknown enzyme performing thaumarchaeotal hydroxylamine oxidation to nitrite.
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Figure 5: Schematic of major metabolisms involved in O2 (photosynthesis and aerobic respiration) and nitrogen cycling (nitrification, canonical denitrification and anammox) in four zones in OMZs. Metalloenzymes are depicted as red (Fe) or green (Cu) circles. Shading indicates relative abundance of transcripts normalized to total Fe and Cu transcripts (see legend) from ETNP station 6 and ETSP station 3 metatranscriptomes (see Supplementary Table 5 for transcript abundances). Abbreviations: Cyt c, cytochrome c; OEC, oxygen evolving complex; red, reduced; ox, oxidized; Cox, cytochrome c oxidase; Nar, dissimilatory nitrate reductase; Nxr, nitrite oxidoreductase; NirK, copper-containing nitrite reductase; NirS, iron-containing nitrite reductase; Nor, nitric oxidase reductase. NirK is divided into two groups: one for nitrifier nirK transcripts most related to uncultured Thaumarchaeota thought to perform ammonia oxidation and nitrite-oxidizing bacteria, and the other in the denitrification pathway for all other nirK transcripts. Nar and Nxr are contained within the formate dehydrogenase protein fold family (SCOPe ID: c.81.1.1), NirK is contained within the multidomain cupredoxin protein fold family (SCOPe ID: b.6.1.3), Nor is contained within the ROO N-terminal domain-like protein fold family (SCOPe ID: d.157.1.3), and NirS is classified as SCOPe ID b.70.2.1 (C-terminus) and a.3.1.2 (N-terminus). Known nitrogen cycle metalloenzymes not yet in the SCOPe database (ammonia monooxygenase in nitrification and hydrazine synthase/reductase in anammox) are represented as colored arrows. Question mark indicates the unknown enzyme performing thaumarchaeotal hydroxylamine oxidation to nitrite.

Mentions: Total Cu genes and transcripts ranged from 35 to 221 per 100,000 protein-coding genes and tended to decrease with depth and diminishing O2 (Figures 4A,B; Supplementary Table 5). With one exception, >60% of total Cu genes and transcripts at all depths and stations were associated with cytochrome c oxidase, the terminal reductase in aerobic respiration that catalyzes the transfer of electrons from reduced cytochrome to O2 (Figure 5). The proportional abundance of cytochrome c oxidase transcripts was positively correlated with O2 content (p > 0.001) and negatively correlated with depth (p = 0.02; Supplementary Table 6).


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)

Schematic of major metabolisms involved in O2 (photosynthesis and aerobic respiration) and nitrogen cycling (nitrification, canonical denitrification and anammox) in four zones in OMZs. Metalloenzymes are depicted as red (Fe) or green (Cu) circles. Shading indicates relative abundance of transcripts normalized to total Fe and Cu transcripts (see legend) from ETNP station 6 and ETSP station 3 metatranscriptomes (see Supplementary Table 5 for transcript abundances). Abbreviations: Cyt c, cytochrome c; OEC, oxygen evolving complex; red, reduced; ox, oxidized; Cox, cytochrome c oxidase; Nar, dissimilatory nitrate reductase; Nxr, nitrite oxidoreductase; NirK, copper-containing nitrite reductase; NirS, iron-containing nitrite reductase; Nor, nitric oxidase reductase. NirK is divided into two groups: one for nitrifier nirK transcripts most related to uncultured Thaumarchaeota thought to perform ammonia oxidation and nitrite-oxidizing bacteria, and the other in the denitrification pathway for all other nirK transcripts. Nar and Nxr are contained within the formate dehydrogenase protein fold family (SCOPe ID: c.81.1.1), NirK is contained within the multidomain cupredoxin protein fold family (SCOPe ID: b.6.1.3), Nor is contained within the ROO N-terminal domain-like protein fold family (SCOPe ID: d.157.1.3), and NirS is classified as SCOPe ID b.70.2.1 (C-terminus) and a.3.1.2 (N-terminus). Known nitrogen cycle metalloenzymes not yet in the SCOPe database (ammonia monooxygenase in nitrification and hydrazine synthase/reductase in anammox) are represented as colored arrows. Question mark indicates the unknown enzyme performing thaumarchaeotal hydroxylamine oxidation to nitrite.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 5: Schematic of major metabolisms involved in O2 (photosynthesis and aerobic respiration) and nitrogen cycling (nitrification, canonical denitrification and anammox) in four zones in OMZs. Metalloenzymes are depicted as red (Fe) or green (Cu) circles. Shading indicates relative abundance of transcripts normalized to total Fe and Cu transcripts (see legend) from ETNP station 6 and ETSP station 3 metatranscriptomes (see Supplementary Table 5 for transcript abundances). Abbreviations: Cyt c, cytochrome c; OEC, oxygen evolving complex; red, reduced; ox, oxidized; Cox, cytochrome c oxidase; Nar, dissimilatory nitrate reductase; Nxr, nitrite oxidoreductase; NirK, copper-containing nitrite reductase; NirS, iron-containing nitrite reductase; Nor, nitric oxidase reductase. NirK is divided into two groups: one for nitrifier nirK transcripts most related to uncultured Thaumarchaeota thought to perform ammonia oxidation and nitrite-oxidizing bacteria, and the other in the denitrification pathway for all other nirK transcripts. Nar and Nxr are contained within the formate dehydrogenase protein fold family (SCOPe ID: c.81.1.1), NirK is contained within the multidomain cupredoxin protein fold family (SCOPe ID: b.6.1.3), Nor is contained within the ROO N-terminal domain-like protein fold family (SCOPe ID: d.157.1.3), and NirS is classified as SCOPe ID b.70.2.1 (C-terminus) and a.3.1.2 (N-terminus). Known nitrogen cycle metalloenzymes not yet in the SCOPe database (ammonia monooxygenase in nitrification and hydrazine synthase/reductase in anammox) are represented as colored arrows. Question mark indicates the unknown enzyme performing thaumarchaeotal hydroxylamine oxidation to nitrite.
Mentions: Total Cu genes and transcripts ranged from 35 to 221 per 100,000 protein-coding genes and tended to decrease with depth and diminishing O2 (Figures 4A,B; Supplementary Table 5). With one exception, >60% of total Cu genes and transcripts at all depths and stations were associated with cytochrome c oxidase, the terminal reductase in aerobic respiration that catalyzes the transfer of electrons from reduced cytochrome to O2 (Figure 5). The proportional abundance of cytochrome c oxidase transcripts was positively correlated with O2 content (p > 0.001) and negatively correlated with depth (p = 0.02; Supplementary Table 6).

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