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Nitrososphaera viennensis gen. nov., sp. nov., an aerobic and mesophilic, ammonia-oxidizing archaeon from soil and a member of the archaeal phylum Thaumarchaeota.

Stieglmeier M, Klingl A, Alves RJ, Rittmann SK, Melcher M, Leisch N, Schleper C - Int. J. Syst. Evol. Microbiol. (2014)

Bottom Line: The organism gained energy by oxidizing ammonia to nitrite aerobically, thereby fixing CO2, but growth depended on the addition of small amounts of organic acids.The optimal growth temperature was 42 °C and the optimal pH was 7.5, with ammonium and pyruvate concentrations of 2.6 and 1 mM, respectively.Additionally, we propose the family Nitrososphaeraceae fam. nov., the order Nitrososphaerales ord. nov. and the class Nitrososphaeria classis nov.

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Affiliation: University of Vienna, Department of Ecogenomics and Systems Biology, Archaea Biology and Ecogenomics Division, Althanstr. 14, 1090 Vienna, Austria.

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Maximum-likelihood 16S rRNA gene phylogeny of the Thaumarchaeota and representative strains of the Crenarchaeota, Euryarchaeota and other proposed archaeal phyla. The tree depicts Nitrososphaera viennensis EN76T (bold), the marine pure culture ‘Candidatus Nitrosopumilus maritimus’ SCM1, organisms from laboratory or natural enrichment cultures (labelled Candidatus) and a selection of environmental sequences representing major uncultured lineages. Proposed phyla and uncharacterized archaeal lineages are placed in quotes. Phylogeny reconstruction was based on 1202-bp 16S rRNA gene fragments and calculated with RaxML VI-HPC using the GTR+I+G model. Bootstrap support values (1000 replicates) are indicated by circles: filled, ≥90 %; shaded, ≥80 % but <90 %; open, ≥70 % but <80 %. Some branching points are not well supported in the displayed tree, such as the lineages of ‘Candidatus Caldiarchaeum’ and ‘Candidatus Korarchaeum’. The former was affiliated rather with Thaumarchaeota in more comprehensive phylogenetic calculations (see e.g. Eme et al., 2013).
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f5: Maximum-likelihood 16S rRNA gene phylogeny of the Thaumarchaeota and representative strains of the Crenarchaeota, Euryarchaeota and other proposed archaeal phyla. The tree depicts Nitrososphaera viennensis EN76T (bold), the marine pure culture ‘Candidatus Nitrosopumilus maritimus’ SCM1, organisms from laboratory or natural enrichment cultures (labelled Candidatus) and a selection of environmental sequences representing major uncultured lineages. Proposed phyla and uncharacterized archaeal lineages are placed in quotes. Phylogeny reconstruction was based on 1202-bp 16S rRNA gene fragments and calculated with RaxML VI-HPC using the GTR+I+G model. Bootstrap support values (1000 replicates) are indicated by circles: filled, ≥90 %; shaded, ≥80 % but <90 %; open, ≥70 % but <80 %. Some branching points are not well supported in the displayed tree, such as the lineages of ‘Candidatus Caldiarchaeum’ and ‘Candidatus Korarchaeum’. The former was affiliated rather with Thaumarchaeota in more comprehensive phylogenetic calculations (see e.g. Eme et al., 2013).

Mentions: Initial phylogenetic analyses of 16S RNA gene sequences from environmental studies placed the ‘mesophilic archaea’ (i.e. Thaumarchaeota), closely related to strain EN76T, as a deep-branching group of the Crenarchaeota (DeLong, 1992; Fuhrman et al., 1992). However, later analyses based on full rRNA gene sequences, concatenated ribosomal protein sequences and full-genome sequence comparisons provided strong evidence that these mesophilic and aerobic AOA represent a distinct phylum, the Thaumarchaeota (Brochier-Armanet et al., 2008; Spang et al., 2010). Members of this phylum encode a specific set of information-processing genes that is distinct from those in the phyla Crenarchaeota and Euryarchaeota, as well as in the proposed phylum ‘Korarchaeota’ (Brochier-Armanet et al., 2008; Spang et al., 2010) and in other currently proposed phyla (Brochier-Armanet et al., 2011; Rinke et al., 2013; Spang et al., 2013). Strain EN76T is affiliated with group I.1b of the Thaumarchaeota (also known as the ‘soil group’) based on 16S rRNA gene phylogeny (Fig. 5), also showing a consistent phylogenetic clustering based on concatenated AmoAB protein sequences (Tourna et al., 2011). ‘Candidatus Nitrososphaera gargensis’ Ga9.2 shares 97 % 16S rRNA gene sequence identity with strain EN76T (Tourna et al., 2011). ‘Candidatus Nitrosopumilus maritimus’ SCM1 is currently the only described pure culture of the second major group within group I.1a of the Thaumarchaeota (Könneke et al., 2005; Walker et al., 2010), and shares 85 % 16S rRNA gene sequence identity with strain EN76T. However, the name ‘Nitrosopumilus maritimus’ has not been validly published and does not have standing in nomenclature. Based on 16S rRNA gene sequence identity, Thermofilum pendens Hrk 5 (81 % 16S rRNA gene sequence identity) and Methanothermus fervidus DSM 2088T (79 %) represent the closest related cultivated strains of species with validly published names from the phyla Crenarchaeota and Euryarchaeota, respectively (Fig. 5). Strain EN76T has a DNA base composition of 52.7 mol% G+C (Tourna et al., 2011), which is similar to that of ‘Candidatus Nitrososphaera gargensis’ Ga9.2 (48.4 mol%) and higher than that of group I.1a strains such as ‘Candidatus Nitrosopumilus maritimus’ SCM1 (34.2 mol%), ‘Candidatus Nitrosoarchaeum koreensis’ MY1 (32.7 mol%) and ‘Candidatus Nitrosoarchaeum limnia’ SFB1 (32.4 mol%) (Blainey et al., 2011; Kim et al., 2011; Spang et al., 2012; Walker et al., 2010). In conclusion, groups I.1a and I.1b differ greatly in their G+C content and form two highly supported distinct phylogenetic lineages based on both 16S rRNA and amoA gene sequences (Fig. 5).


Nitrososphaera viennensis gen. nov., sp. nov., an aerobic and mesophilic, ammonia-oxidizing archaeon from soil and a member of the archaeal phylum Thaumarchaeota.

Stieglmeier M, Klingl A, Alves RJ, Rittmann SK, Melcher M, Leisch N, Schleper C - Int. J. Syst. Evol. Microbiol. (2014)

Maximum-likelihood 16S rRNA gene phylogeny of the Thaumarchaeota and representative strains of the Crenarchaeota, Euryarchaeota and other proposed archaeal phyla. The tree depicts Nitrososphaera viennensis EN76T (bold), the marine pure culture ‘Candidatus Nitrosopumilus maritimus’ SCM1, organisms from laboratory or natural enrichment cultures (labelled Candidatus) and a selection of environmental sequences representing major uncultured lineages. Proposed phyla and uncharacterized archaeal lineages are placed in quotes. Phylogeny reconstruction was based on 1202-bp 16S rRNA gene fragments and calculated with RaxML VI-HPC using the GTR+I+G model. Bootstrap support values (1000 replicates) are indicated by circles: filled, ≥90 %; shaded, ≥80 % but <90 %; open, ≥70 % but <80 %. Some branching points are not well supported in the displayed tree, such as the lineages of ‘Candidatus Caldiarchaeum’ and ‘Candidatus Korarchaeum’. The former was affiliated rather with Thaumarchaeota in more comprehensive phylogenetic calculations (see e.g. Eme et al., 2013).
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f5: Maximum-likelihood 16S rRNA gene phylogeny of the Thaumarchaeota and representative strains of the Crenarchaeota, Euryarchaeota and other proposed archaeal phyla. The tree depicts Nitrososphaera viennensis EN76T (bold), the marine pure culture ‘Candidatus Nitrosopumilus maritimus’ SCM1, organisms from laboratory or natural enrichment cultures (labelled Candidatus) and a selection of environmental sequences representing major uncultured lineages. Proposed phyla and uncharacterized archaeal lineages are placed in quotes. Phylogeny reconstruction was based on 1202-bp 16S rRNA gene fragments and calculated with RaxML VI-HPC using the GTR+I+G model. Bootstrap support values (1000 replicates) are indicated by circles: filled, ≥90 %; shaded, ≥80 % but <90 %; open, ≥70 % but <80 %. Some branching points are not well supported in the displayed tree, such as the lineages of ‘Candidatus Caldiarchaeum’ and ‘Candidatus Korarchaeum’. The former was affiliated rather with Thaumarchaeota in more comprehensive phylogenetic calculations (see e.g. Eme et al., 2013).
Mentions: Initial phylogenetic analyses of 16S RNA gene sequences from environmental studies placed the ‘mesophilic archaea’ (i.e. Thaumarchaeota), closely related to strain EN76T, as a deep-branching group of the Crenarchaeota (DeLong, 1992; Fuhrman et al., 1992). However, later analyses based on full rRNA gene sequences, concatenated ribosomal protein sequences and full-genome sequence comparisons provided strong evidence that these mesophilic and aerobic AOA represent a distinct phylum, the Thaumarchaeota (Brochier-Armanet et al., 2008; Spang et al., 2010). Members of this phylum encode a specific set of information-processing genes that is distinct from those in the phyla Crenarchaeota and Euryarchaeota, as well as in the proposed phylum ‘Korarchaeota’ (Brochier-Armanet et al., 2008; Spang et al., 2010) and in other currently proposed phyla (Brochier-Armanet et al., 2011; Rinke et al., 2013; Spang et al., 2013). Strain EN76T is affiliated with group I.1b of the Thaumarchaeota (also known as the ‘soil group’) based on 16S rRNA gene phylogeny (Fig. 5), also showing a consistent phylogenetic clustering based on concatenated AmoAB protein sequences (Tourna et al., 2011). ‘Candidatus Nitrososphaera gargensis’ Ga9.2 shares 97 % 16S rRNA gene sequence identity with strain EN76T (Tourna et al., 2011). ‘Candidatus Nitrosopumilus maritimus’ SCM1 is currently the only described pure culture of the second major group within group I.1a of the Thaumarchaeota (Könneke et al., 2005; Walker et al., 2010), and shares 85 % 16S rRNA gene sequence identity with strain EN76T. However, the name ‘Nitrosopumilus maritimus’ has not been validly published and does not have standing in nomenclature. Based on 16S rRNA gene sequence identity, Thermofilum pendens Hrk 5 (81 % 16S rRNA gene sequence identity) and Methanothermus fervidus DSM 2088T (79 %) represent the closest related cultivated strains of species with validly published names from the phyla Crenarchaeota and Euryarchaeota, respectively (Fig. 5). Strain EN76T has a DNA base composition of 52.7 mol% G+C (Tourna et al., 2011), which is similar to that of ‘Candidatus Nitrososphaera gargensis’ Ga9.2 (48.4 mol%) and higher than that of group I.1a strains such as ‘Candidatus Nitrosopumilus maritimus’ SCM1 (34.2 mol%), ‘Candidatus Nitrosoarchaeum koreensis’ MY1 (32.7 mol%) and ‘Candidatus Nitrosoarchaeum limnia’ SFB1 (32.4 mol%) (Blainey et al., 2011; Kim et al., 2011; Spang et al., 2012; Walker et al., 2010). In conclusion, groups I.1a and I.1b differ greatly in their G+C content and form two highly supported distinct phylogenetic lineages based on both 16S rRNA and amoA gene sequences (Fig. 5).

Bottom Line: The organism gained energy by oxidizing ammonia to nitrite aerobically, thereby fixing CO2, but growth depended on the addition of small amounts of organic acids.The optimal growth temperature was 42 °C and the optimal pH was 7.5, with ammonium and pyruvate concentrations of 2.6 and 1 mM, respectively.Additionally, we propose the family Nitrososphaeraceae fam. nov., the order Nitrososphaerales ord. nov. and the class Nitrososphaeria classis nov.

View Article: PubMed Central - PubMed

Affiliation: University of Vienna, Department of Ecogenomics and Systems Biology, Archaea Biology and Ecogenomics Division, Althanstr. 14, 1090 Vienna, Austria.

Show MeSH
Related in: MedlinePlus