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The Genome of the Ammoniaoxidizing Candidatus Nitrososphaera Gargensis

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The Genome of the Ammoniaoxidizing Candidatus Nitrososphaera Gargensis bs_bs_banner Environmental Microbiology (2012) 14(12), 3122–3145 doi:10.1111/j.1462-2920.2012.02893.x The genome of the ammonia-oxidizing Candidatus Nitrososphaera gargensis: insights into metabolic versatility and environmental adaptations Anja Spang,1† Anja Poehlein,2† Pierre Offre,1 quently found in high numbers in many terrestrial Sabine Zumbrägel,3 Susanne Haider,4 environments. With its 2.83 Mb the genome is much Nicolas Rychlik,3 Boris Nowka,3 larger than that of other AOA. The presence of Christel Schmeisser,3 Elena V. Lebedeva,5 a high number of (active) IS elements/transposases, Thomas Rattei,6 Christoph Böhm,4 Markus Schmid,4 genomic islands, gene duplications and a complete Alexander Galushko,4 Roland Hatzenpichler,4‡ CRISPR/Cas defence system testifies to its dynamic Thomas Weinmaier,6 Rolf Daniel,2 Christa Schleper,1 evolution consistent with low degree of synteny Eva Spieck,3 Wolfgang Streit3** and with other thaumarchaeal genomes. As expected, Michael Wagner4* the repertoire of conserved enzymes proposed to be 1Department of Genetics in Ecology, University of required for archaeal ammonia oxidation is encoded Vienna, Althanstr. 14, 1090 Vienna, Austria. by N. gargensis, but it can also use urea and possibly 2Laboratorium für Genomanalyse, Universität Göttingen, cyanate as alternative ammonia sources. Further- 37077 Göttingen, Germany. more, its carbon metabolism is more flexible at the 3Biozentrum Klein Flottbek, Abteilung für Mikrobiologie central pyruvate switch point, encompasses the und Biotechnologie, Universität Hamburg, ability to take up small organic compounds and Ohnhorststrasse 18, 22609 Hamburg, Germany. might even include an oxidative pentose phosphate 4Department of Microbial Ecology, University of Vienna, pathway. Furthermore, we show that thaumarchaeota Althanstr. 14, 1090 Vienna, Austria. produce cofactor F420 as well as polyhydroxyal- 5Winogradsky Institute of Microbiology, Russian kanoates. Lateral gene transfer from bacteria and Academy of Sciences, Prospect 60-let Oktyabrya 7/2, euryarchaeota has contributed to the metabolic Moscow 117312, Russia. versatility of N. gargensis. This organisms is well 6Department of Computational Systems Biology, adapted to its niche in a heavy metal-containing University of Vienna, Althanstr., 14, 1090 Vienna, thermal spring by encoding a multitude of heavy Austria. metal resistance genes, chaperones and mannosylg- lycerate as compatible solute and has the genetic ability to respond to environmental changes by signal Summary transduction via a large number of two-component The cohort of the ammonia-oxidizing archaea systems, by chemotaxis and flagella-mediated (AOA) of the phylum Thaumarchaeota is a diverse, motility and possibly even by gas vacuole formation. widespread and functionally important group of These findings extend our understanding of thaumar- microorganisms in many ecosystems. However, our chaeal evolution and physiology and offer many test- understanding of their biology is still very rudimen- able hypotheses for future experimental research on tary in part because all available genome sequences these nitrifiers. of this phylum are from members of the Nitro- sopumilus cluster. Here we report on the complete Introduction genome sequence of Candidatus Nitrososphaera gargensis obtained from an enrichment culture, rep- The discovery of ammonia-oxidizing archaea (AOA) after resenting a different evolutionary lineage of AOA fre- more than 100 years of nitrification research (Könneke et al., 2005; Treusch et al., 2005) has dramatically Received 31 August, 2012; accepted 1 September, 2012. For changed our perception of the diversity (Francis et al., correspondence. *E-mail [email protected]; Tel. (+43) 2005), abundance (Leininger et al., 2006) and niche 1 4277 54390; Fax (+43) 1 4277 54389. **E-mail wolfgang.streit@ adaptations (Martens-Habbena et al., 2009; Gubry- uni-hamburg.de; Tel. (+49) 40 42816 463; Fax (+49) 40 42816 459. †Contributed equally. ‡Current address: Division of Geological and Rangin et al., 2011; Verhamme et al., 2011) of nitrifying Planetary Sciences, California Institute of Technology. microbes in the environment. 16S rRNA- and amoA- © 2012 Society for Applied Microbiology and Blackwell Publishing Ltd The genome of Candidatus Nitrososphaera gargensis 3123 based surveys of AOA revealed an astonishing diversity of members of this guild with hundreds of predicted species (Schleper et al., 2005; Gubry-Rangin et al., 2011; Pester BD31 et al., 2012) belonging to several major clades (Fig. S1A) c cluster, group I.1a variable salinity within the newly described phylum Thaumarchaeota culture Nitrosopumilus salaria Nitrosopumilus Sediment with Enrichment (Brochier-Armanet et al., 2008; Spang et al., 2010). n.d. Among them, the Nitrosopumilus (also called group I.1a or marine group I) and the Nitrososphaera clusters includ- ing its recently described sister cluster (Pester et al., BD20 2012) (collectively referred to as group I.1b or soil group) c cluster, group I.1a sediment seem to be most abundant in aquatic and terrestrial envi- culture Nitrosoarchaeum limnia Nitrosopumilus Low-salinity ronments respectively. Till today only a few enrichment cultures (Hatzenpichler et al., 2008; de la Torre et al., 2008; Jung et al., 2011; Lehtovirta-Morley et al., 2011; French et al., 2012; Kim et al., 2012; Mosier et al., MY1 2012a,b) and two pure cultures (Könneke et al., 2005; cluster, group I.1a Tourna et al., 2011) of AOA are available for physiological Caragana sinica Nitrosopumilus Nitrosoarchaeum koreensis Soil rhizosphere of and molecular experiments. So far, only closely related Enrichment culture Enrichment members from the Nitrosopumilus cluster (Hallam et al., ), which might explain the relatively low number of detected tRNAs. 2006a; Walker et al., 2010; Blainey et al., 2011; Kim et al., 2011; Urakawa et al., 2011; Mosier et al., 2012a,c) and a few short fosmid sequences from members of the SFB1 cluster, group I.1a sediment Nitrososphaera cluster (Treusch et al., 2005; Bartossek culture Nitrosopumilus Nitrosoarchaeum limnia Enrichment et al., 2010; 2012) have been investigated genomically (Fig. S1A; Table 1), revealing that AOA exploit a surpris- Supporting information ingly different enzymatic repertoire for energy and carbon A metabolism compared with their ammonia-oxidizing bac- terial counterparts. For example, members of the Nitro- cluster, group I.1a sopumilus cluster lack homologues for hydroxylamine (sponge host) Nitrosopumilus Cenarchaeum symbiosum oxidoreductase or cytochromes c552 and c554 typically Sponge symbiont Low-salinity found in ammonia-oxidizing bacteria (AOB), suggesting an alternative substrate conversion pathway and different components for electron transport, likely including copper cluster, binding proteins (Walker et al., 2010). Furthermore, thau- SCM1 marchaeota of the Nitrosopumilus cluster apparently use a modified version of the 3-hydroxypropionate/4- group I.1a 21–23°C Nitrosopumilus Tropical fish tank, Nitrosopumilus maritimus 44 45 45 42 39 40 hydroxybutyrate pathway for autotrophic carbon fixation Mesophilic Mesophilic Mesophilic Mesophilic Mesophilic Mesophilic (Berg et al., 2007; 2010a) instead of the Calvin–Benson– ) to other proteins excluding those predicted for organisms from same phylum. 4 Bassham cycle common to all known AOB. However, - a comprehensive understanding of the physiology and 10 < cluster, evolutionary history of Thaumarchaeota will require com- genome in comparison with those of other published thaumarchaeal genomes. parative genomic analyses with members of the other -value E evolutionary lines of descent within this phylum. (1) 1.65 (1) 2.05 (1) 1.77 (76) 1.61 (1) 1.86 (343) 1.57 (171) possesses some tRNAs with non-canonical introns (for details, see a Here we report on the first complete genome of an d group I.1b pond of Garga spring) (46°C optimum) 2.83 N. gargensis Nitrososphaera Nitrososphaera gargensis 32% 15% 30% 22% 23% n.d. AOA from the Nitrososphaera cluster. The 2.83 Mb Enrichment culture Pure culture Natural enrichment genome sequence of Candidatus Nitrososphaera gargen- sis (Fig. S1B and C; please note that the Candidatus N. gargensis designation was omitted in the following text to improve genome contains a large tandem duplication of a genomic fragment that is 16 966 bp in length. readability) was reconstructed from an enrichment culture obtained from a microbial mat growing in an outflow pond (45°C) of a terrestrial hot spring (Lebedeva et al., 2005; b General features of the Hatzenpichler et al., 2008). Thus, N. gargensis occupies a N. gargensis Predicted proteins without homology ( It should be noted that The fundamentally different niche to those AOA previously The genome sequence was not available when the ORPHAN analysis was performed. C content 48% 34% 58% 32% 33% 33% 34% of contigs in brackets sequences + Affiliation Habitat Microbial mat (outflow Table 1. Organism 16S–23S rRNA genesSeparate 5S rRNANumber of tRNAsa. 1 1 40 1 1 1 1 1 1 1 1 1 1 1 1 b. G ORPHANS Temperature range Moderate thermophilic c. d. Genome size in Mb, number investigated on the genomic level as also reflected by Origin of genome © 2012 Society for Applied Microbiology and Blackwell Publishing Ltd, Environmental Microbiology, 14, 3122–3145 3124 A. Spang et al. 1.6e+06 CO2 fixation similar to previously studied thaumarchaeota, 1.4e+06 but on the other hand revealed a very dynamically evolv- 1.2e+06 ing genome with frequent gene duplication and lateral 1e+06 gene transfer events contributing
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