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Candidatus Nitrosocaldus Cavascurensis, an Ammonia Candidatus Nitrosocaldus cavascurensis, an Ammonia Oxidizing, Extremely Thermophilic Archaeon with a Highly Mobile Genome Sophie Abby, Michael Melcher, Melina Kerou, Mart Krupovic, Michaela Stieglmeier, Claudia Rossel, Kevin Pfeifer, Christa Schleper To cite this version: Sophie Abby, Michael Melcher, Melina Kerou, Mart Krupovic, Michaela Stieglmeier, et al.. Can- didatus Nitrosocaldus cavascurensis, an Ammonia Oxidizing, Extremely Thermophilic Archaeon with a Highly Mobile Genome. Frontiers in Microbiology, Frontiers Media, 2018, 9, pp.28. 10.3389/fmicb.2018.00028. hal-01702026 HAL Id: hal-01702026 https://hal.archives-ouvertes.fr/hal-01702026 Submitted on 6 Feb 2018 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. fmicb-09-00028 January 29, 2018 Time: 12:16 # 1 ORIGINAL RESEARCH published: 26 January 2018 doi: 10.3389/fmicb.2018.00028 Candidatus Nitrosocaldus cavascurensis, an Ammonia Oxidizing, Extremely Thermophilic Archaeon with a Highly Mobile Genome Sophie S. Abby1,2†, Michael Melcher1†, Melina Kerou1, Mart Krupovic3, Michaela Stieglmeier1, Claudia Rossel1, Kevin Pfeifer1 and Christa Schleper1* 1 Division of Archaea Biology and Ecogenomics, Department of Ecogenomics and Systems Biology, University of Vienna, Vienna, Austria, 2 Laboratoire Techniques de l’Ingénierie Médicale et de la Complexité – Informatique, Mathématiques et Applications, Centre National de la Recherche Scientifique, Université Grenoble Alpes, Grenoble, France, 3 Unité Biologie Moléculaire du Gène chez les Extrêmophiles, Institut Pasteur, Paris, France Ammonia oxidizing archaea (AOA) of the phylum Thaumarchaeota are widespread in moderate environments but their occurrence and activity has also been demonstrated Edited by: in hot springs. Here we present the first enrichment of a thermophilic representative Martin G. Klotz, Washington State University Tri-Cities, with a sequenced genome, which facilitates the search for adaptive strategies and United States for traits that shape the evolution of Thaumarchaeota. Candidatus Nitrosocaldus Reviewed by: cavascurensis has been enriched from a hot spring in Ischia, Italy. It grows optimally Ivan A. Berg, at 68◦C under chemolithoautotrophic conditions on ammonia or urea converting Universität Münster, Germany Willm Martens-Habbena, ammonia stoichiometrically into nitrite with a generation time of approximately 23 h. University of Florida, United States Phylogenetic analyses based on ribosomal proteins place the organism as a sister Lisa Y. Stein, University of Alberta, Canada group to all known mesophilic AOA. The 1.58 Mb genome of Ca. N. cavascurensis *Correspondence: harbors an amoAXCB gene cluster encoding ammonia monooxygenase and genes Christa Schleper for a 3-hydroxypropionate/4-hydroxybutyrate pathway for autotrophic carbon fixation, [email protected] but also genes that indicate potential alternative energy metabolisms. Although a bona † These authors have contributed fide gene for nitrite reductase is missing, the organism is sensitive to NO-scavenging, equally to this work. underlining the potential importance of this compound for AOA metabolism. Ca. N. Specialty section: cavascurensis is distinct from all other AOA in its gene repertoire for replication, cell This article was submitted to division and repair. Its genome has an impressive array of mobile genetic elements Evolutionary and Genomic Microbiology, and other recently acquired gene sets, including conjugative systems, a provirus, a section of the journal transposons and cell appendages. Some of these elements indicate recent exchange Frontiers in Microbiology with the environment, whereas others seem to have been domesticated and might Received: 28 December 2017 Accepted: 08 January 2018 convey crucial metabolic traits. Published: 26 January 2018 Keywords: ammonia oxidation, archaea, Thaumarchaeota, nitrification, mobile genetic elements, thermophilic Citation: adaptations, amoA gene, DNA repair enzymes Abby SS, Melcher M, Kerou M, Krupovic M, Stieglmeier M, Rossel C, Pfeifer K and Schleper C INTRODUCTION (2018) Candidatus Nitrosocaldus cavascurensis, an Ammonia Ammonia oxidizing archaea (AOA) now collectively classified as Nitrososphaeria within the Oxidizing, Extremely Thermophilic Archaeon with a Highly Mobile phylum Thaumarchaeota (Brochier-Armanet et al., 2008; Spang et al., 2010; Stieglmeier et al., Genome. Front. Microbiol. 9:28. 2014; Kerou et al., 2016a) represent the sole archaeal group that is globally distributed in oxic doi: 10.3389/fmicb.2018.00028 environments efficiently competing with aerobic bacteria. Because of their large numbers in the Frontiers in Microbiology| www.frontiersin.org 1 January 2018| Volume 9| Article 28 fmicb-09-00028 January 29, 2018 Time: 12:16 # 2 Abby et al. Thermophilic Thaumarchaeon Cultivation and Genome ocean plankton, in marine sediments, in lakes and in soils, A remarkable diversity of archaea with different metabolisms AOA are considered one of the most abundant groups of has been described from terrestrial and marine hot springs prokaryotes on this planet (Schleper et al., 2005; Prosser and and hyperthermophilic organisms tend to be found at the base Nicol, 2008; Erguder et al., 2009; Schleper and Nicol, 2010; of almost all lineages of archaea. Therefore, it has often been Pester et al., 2011; Hatzenpichler, 2012; Stahl and de la Torre, proposed that the ancestor of all archaea and the ancestors 2012; Offre et al., 2013). All currently cultivated AOA strains of mesophilic lineages of archaea were hyperthermophilic or gain energy exclusively through the oxidation of ammonia to at least thermophiles (Barns et al., 1996; Lopez-Garcia et al., nitrite, i.e., they perform the first step in nitrification. They 2004; Gribaldo and Brochier-Armanet, 2006; Brochier-Armanet grow chemolithoautotrophically from inorganic carbon supply. et al., 2012; Eme et al., 2013). This has been supported by Some strains show growth only in the presence of small organic sequence analyses which suggested a parallel adaptation from acids (Tourna et al., 2011; Qin et al., 2014) which seem to hot to moderate temperatures in several lineages of archaea catalyze degradation of reactive oxygen species (ROS) from (Groussin and Gouy, 2011; Williams et al., 2017). Indeed, the the medium (Kim et al., 2016). Different from their bacterial thermophilic strain Ca. Nitrosocaldus yellowstonensis emerged ammonia oxidizing counterparts, AOA are often adapted to in 16S rRNA phylogeny as a sister group of all known mesophilic rather low levels of ammonia for growth, which seems to AOA (de la Torre et al., 2008) indicating that AOA also evolved favor their activities in oligotrophic environments, such as the in hot environments. marine pelagic ocean and marine sediments, but also in acidic However, until now, no genome of an obligate thermophilic environments, where the concentration of ammonia decreases AOA was available to analyze in depth the phylogenetic in favor of ammonium (Nicol et al., 2008). However, AOA placement of thermophilic AOA and to investigate adaptive occur also in large numbers in terrestrial environments, including features of these ammonia oxidizers that have a pivotal position fertilized soils and some waste water treatment plants, and several in understanding the evolution of Thaumarchaeota. studies indicate alternative energy metabolisms (Mussmann et al., In this work we present the physiology and first genome of 2011; Alves et al., 2013). Although ammonia oxidation in an extremely thermophilic AOA of the Nitrosocaldus lineage that archaea has not been biochemically resolved, the presence of we cultivated from a hot spring in Southern Italy. We analyze genes for an ammonia monooxygenase in all AOA with remote its phylogeny based on ribosomal proteins and reconstruct similarity to methane and ammonia monooxygenases of bacteria metabolic and genomic features and adaptations. implies involvement of this complex in the process (Konneke et al., 2005; Treusch et al., 2005; Nicol and Schleper, 2006). Hydroxylamine has been suggested to be the first product of MATERIALS AND METHODS ammonia oxidation (Vajrala et al., 2013), but further conversion to nitrite is performed in an unknown process, as no homolog Sampling and Enrichment of the bacterial hydroxylamine dehydrogenase has been found About 500 mL of mud were sampled from a terrestrial hot in the genomes of AOA. However, nitric oxide (NO) has been spring on the Italian island Ischia at “Terme di Cavascura” and ◦ suggested to be involved in the process, because NO production stored at 4 C until it arrived at the laboratory in Vienna (after ◦ and re-consumption have been observed (Martens-Habbena about one week, October 2013). A temperature of 77 C and et al., 2015; Kozlowski et al., 2016b) and the NO scavenger pH 7–8 were measured in situ using a portable thermometer PTIO was shown to inhibit AOA at very low concentrations (HANNA HI935005) and pH stripes. Initial enrichments (20 mL (Yan et al., 2012; Shen et al., 2013; Martens-Habbena et al., final volume) were set up in 120 mL serum
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