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Eukaryotic nirK genes encoding copper-containing nitrite reductase: originating from the protomitochondrion?

ABSTRACT: Although denitrification or nitrate respiration has been found among a few eukaryotes, its phylogenetic relationship with the bacterial system remains unclear because orthologous genes involved in the bacterial denitrification system were not identified in these eukaryotes. In this study, we isolated a gene from the denitrifying fungus Fusarium oxysporum that is homologous to the bacterial nirK gene responsible for encoding copper-containing nitrite reductase (NirK). Characterization of the gene and its recombinant protein showed that the fungal nirK gene is the first eukaryotic ortholog of the bacterial counterpart involved in denitrification. Additionally, recent genome analyses have revealed the occurrence of nirK homologs in many fungi and protozoa, although the denitrifying activity of these eukaryotes has never been examined. These eukaryotic homolog genes, together with the fungal nirK gene of F. oxysporum, are grouped in the same branch of the phylogenetic tree as the nirK genes of bacteria, archaea, and eukaryotes, implying that eukaryotic nirK and its homologs evolved from a single ancestor (possibly the protomitochondrion). These results show that the fungal denitrifying system has the same origin as its bacterial counterpart.

SUBMITTER: Kim SW

PROVIDER: S-EPMC2681669 | biostudies-literature | 2009 May

REPOSITORIES: biostudies-literature

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Eukaryotic nirK genes encoding copper-containing nitrite reductase: originating from the protomitochondrion?

Kim Sang-Wan SW Fushinobu Shinya S Zhou Shengmin S Wakagi Takayoshi T Shoun Hirofumi H

Applied and environmental microbiology 20090306 9

Although denitrification or nitrate respiration has been found among a few eukaryotes, its phylogenetic relationship with the bacterial system remains unclear because orthologous genes involved in the bacterial denitrification system were not identified in these eukaryotes. In this study, we isolated a gene from the denitrifying fungus Fusarium oxysporum that is homologous to the bacterial nirK gene responsible for encoding copper-containing nitrite reductase (NirK). Characterization of the gene ...[more]

PMID: 19270125

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Project description:The versatile soil bacterium Anaeromyxobacter dehalogenans lacks the hallmark denitrification genes nirS and nirK (encoding NO2-→NO reductases) and couples growth to NO3- reduction to NH4+ (respiratory ammonification) and to N2O reduction to N2A. dehalogenans also grows by reducing Fe(III) to Fe(II), which chemically reacts with NO2- to form N2O (i.e., chemodenitrification). Following the addition of 100 μmol of NO3- or NO2- to Fe(III)-grown axenic cultures of A. dehalogenans, 54 (±7) μmol and 113 (±2) μmol N2O-N, respectively, were produced and subsequently consumed. The conversion of NO3- to N2 in the presence of Fe(II) through linked biotic-abiotic reactions represents an unrecognized ecophysiology of A. dehalogenans The new findings demonstrate that the assessment of gene content alone is insufficient to predict microbial denitrification potential and N loss (i.e., the formation of gaseous N products). A survey of complete bacterial genomes in the NCBI Reference Sequence database coupled with available physiological information revealed that organisms lacking nirS or nirK but with Fe(III) reduction potential and genes for NO3- and N2O reduction are not rare, indicating that NO3- reduction to N2 through linked biotic-abiotic reactions is not limited to A. dehalogenans Considering the ubiquity of iron in soils and sediments and the broad distribution of dissimilatory Fe(III) and NO3- reducers, denitrification independent of NO-forming NO2- reductases (through combined biotic-abiotic reactions) may have substantial contributions to N loss and N2O flux.IMPORTANCE Current attempts to gauge N loss from soils rely on the quantitative measurement of nirK and nirS genes and/or transcripts. In the presence of iron, the common soil bacterium Anaeromyxobacter dehalogenans is capable of denitrification and the production of N2 without the key denitrification genes nirK and nirS Such chemodenitrifiers denitrify through combined biotic and abiotic reactions and have potentially large contributions to N loss to the atmosphere and fill a heretofore unrecognized ecological niche in soil ecosystems. The findings emphasize that the comprehensive understanding of N flux and the accurate assessment of denitrification potential can be achieved only when integrated studies of interlinked biogeochemical cycles are performed.

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Eukaryotic nirK genes encoding copper-containing nitrite reductase: originating from the protomitochondrion?

Publications

Eukaryotic nirK genes encoding copper-containing nitrite reductase: originating from the protomitochondrion?

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