Physiological and Genomic Characterization of a Hyperthermophilic Archaeon Archaeoglobus neptunius sp. nov. Isolated From a Deep-Sea Hydrothermal Vent Warrants the Reclassification of the Genus Archaeoglobus Galina Slobodkina, Maxime Allioux, Alexander Merkel, Marie-Anne Cambon-Bonavita, Karine Alain, Mohamed Jebbar, Alexander Slobodkin To cite this version: Galina Slobodkina, Maxime Allioux, Alexander Merkel, Marie-Anne Cambon-Bonavita, Karine Alain, et al.. Physiological and Genomic Characterization of a Hyperthermophilic Archaeon Ar- chaeoglobus neptunius sp. nov. Isolated From a Deep-Sea Hydrothermal Vent Warrants the Re- classification of the Genus Archaeoglobus. Frontiers in Microbiology, Frontiers Media, 2021,12, 10.3389/fmicb.2021.679245. hal-03322688 HAL Id: hal-03322688 https://hal.archives-ouvertes.fr/hal-03322688 Submitted on 19 Aug 2021 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. ORIGINAL RESEARCH published: 16 July 2021 doi: 10.3389/fmicb.2021.679245 Physiological and Genomic Characterization of a Hyperthermophilic Archaeon Archaeoglobus neptunius sp. nov. Isolated From a Deep-Sea Hydrothermal Vent Warrants the Edited by: Reclassification of the Genus Rafael R. de la Haba, University of Sevilla, Spain Archaeoglobus Reviewed by: Chaomin Sun, Galina Slobodkina 1*, Maxime Allioux 2, Alexander Merkel 1, Marie-Anne Cambon-Bonavita 2, Institute of Oceanology, Karine Alain 2, Mohamed Jebbar 2 and Alexander Slobodkin 1 Chinese Academy of Sciences (CAS), China 1 Winogradsky Institute of Microbiology, Federal Research Center of Biotechnology of the Russian Academy of Sciences, Tamara N. Nazina, Moscow, Russia, 2 Laboratoire de Microbiologie des Environnements Extrêmes LM2E, Univ Brest, CNRS, IFREMER, Winogradsky Institute of IRP 1211 MicrobSea, UMR 6197, Plouzané, France Microbiology, Russian Academy of Sciences (RAS), Russia Ida Helene Steen, Hyperthermophilic archaea of the genus Archaeoglobus are the subject of many University of Bergen, Norway fundamental and biotechnological researches. Despite their significance, the class *Correspondence: Archaeoglobi is currently represented by only eight species obtained as axenic cultures Galina Slobodkina [email protected] and taxonomically characterized. Here, we report the isolation and characterization of a new species of Archaeoglobus from a deep-sea hydrothermal vent (Mid-Atlantic Ridge, Specialty section: TAG) for which the name Archaeoglobus neptunius sp. nov. is proposed. The type strain This article was submitted to T T T Extreme Microbiology, is SE56 (=DSM 110954 = VKM B-3474 ). The cells of the novel isolate are motile irregular a section of the journal cocci growing at 50–85°C, pH 5.5–7.5, and NaCl concentrations of 1.5–4.5% (w/v). Strain Frontiers in Microbiology T SE56 grows lithoautotrophically with H2 as an electron donor, sulfite or thiosulfate as an Received: 11 March 2021 electron acceptor, and CO /HCO − as a carbon source. It is also capable of Accepted: 30 June 2021 2 3 Published: 16 July 2021 chemoorganotrophic growth by reduction of sulfate, sulfite, or thiosulfate. The genome Citation: of the new isolate consists of a 2,115,826 bp chromosome with an overall G + C content Slobodkina G, Allioux M, Merkel A, of 46.0 mol%. The whole-genome annotation confirms the key metabolic features of the Cambon-Bonavita M-A, Alain K, Jebbar M and Slobodkin A (2021) novel isolate demonstrated experimentally. Genome contains a complete set of genes Physiological and Genomic involved in CO2 fixation via reductive acetyl-CoA pathway, gluconeogenesis, hydrogen Characterization of a and fatty acids oxidation, sulfate reduction, and flagellar motility. The phylogenomic Hyperthermophilic Archaeon Archaeoglobus neptunius sp. nov. reconstruction based on 122 conserved single-copy archaeal proteins supported by Isolated From a Deep-Sea average nucleotide identity (ANI), average amino acid identity (AAI), and alignment fraction Hydrothermal Vent Warrants the Reclassification of the Genus (AF) values, indicates a polyphyletic origin of the species currently included into the genus Archaeoglobus. Archaeoglobus, warranting its reclassification. Front. Microbiol. 12:679245. doi: 10.3389/fmicb.2021.679245 Keywords: sulfate reduction, chemolithoautotroph, anaerobe, hyperthermophile, Archaea Frontiers in Microbiology | www.frontiersin.org 1 July 2021 | Volume 12 | Article 679245 Slobodkina et al. Archaeoglobus neptunius sp. nov. INTRODUCTION high salts concentrations, and its ability to degrade alkanes (Park and Park, 2018). Over several decades since their discovery, thermophilic archaea At the time of writing, the genus Archaeoglobus includes have been the subject of an increasing number of studies related five species with validly published names:A. fulgidus (Stetter, to microbial ecology, biogeochemistry, origin of life, and evolution 1988), A. profundus (Burggraf et al., 1990), A. veneficus (Huber of the biosphere (Offre et al., 2013). It was long thought that et al., 1997), A. infectus (Mori et al., 2008). and A. sulfaticallidus hyperthermophilic archaea represented the deepest and shortest (Steinsbu et al., 2010). Together with related genera, Geoglobus phylogenetic branches of the tree of life and could be considered and Ferroglobus, they compose the family Archaeoglobaceae the first living organisms on Earth since most of them have belonging to the order Archaeoglobales, class Archaeoglobi (Parte a chemolithoautotrophic mode of nutrition (Stetter, 2006; Martin et al., 2020; http://www.bacterio.net/index.html). It is notable and Sousa, 2016; Weiss et al., 2016), but this hypothesis is that class Archaeoglobi is represented by only eight species now being questioned. Indeed, numerous archaeal lineages, with obtained as axenic cultures and taxonomically characterized new complete genomes or high-quality metagenomes-assembled in detail. All known representatives of Archaeoglobi are strict genomes (MAGs) and single-amplified genomes (SAGs), have anaerobes and hyperthermophiles isolated from marine been discovered thanks to remarkable advances in sequencing hydrothermal systems and off-shore oil reservoirs. With the techniques and in data processing capabilities, allowing the exception of A. infectus and A. profundus, all species of the construction of robust phylogenetic trees based on several genetic order Archaeoglobales are capable of chemolithoautotrophic markers, which demonstrate that the root is far from being growth. Members of this order differ significantly in terms of resolved (Baker et al., 2020). Dissimilatory sulfate reduction is the electron acceptors they use. All known species of the genus a microbial process with significant ecological and biogeochemical Archaeoglobus are able to grow by reduction of sulfite and implication (Rabus et al., 2015). It is mainly related to the thiosulfate. Archaeoglobus fulgidus, A. profundus, and marine environments because of the high sulfate concentrations. A. sulfaticallidus can also reduce sulfate with organic carbon In the marine ecosystems with temperatures above 80°C, the source, but only A. sulfaticallidus is capable of lithoautotrophic only conclusively proven actors of this process are the growth with sulfate as a terminal electron acceptor. Species representatives of the genus Archaeoglobus that was established of the genus Geoglobus are obligate iron-reducers (Kashefi et al., by Stetter et al. (1987) and Stetter (1988). The type strain, A. 2002; Slobodkina et al., 2009). The only representative of the fulgidus VC-16T, is one of the best studied Archaea, as it was genus Ferroglobus, F. placidus, can use nitrate, thiosulfate, and the first described hyperthermophilic sulfate-reducing archaea, Fe3+ as electron acceptors (Hafenbradl et al., 1996; Tor et al., 2001). and one of the first archaea whose genome has been sequenced Over the last decade, genomic data have increased (Stetter, 1988; Klenk et al., 1997). In addition to physiological exponentially and revealed many phylogenetic inconsistencies properties given in the original description, new metabolic that require revision and reclassification of existing prokaryotic features were found based on genome sequencing data analysis, taxonomy and nomenclature. These taxonomic issues were e.g., growth coupled with carbon monoxide oxidation and sulfate recently addressed by proposing a standardized taxonomy for reduction or acetogenesis (Henstra et al., 2007); the ability for Bacteria and Archaea referred to as the Genome Taxonomy anaerobic oxidation of fatty acids, n-alkenes, and n-alkanes DataBase (GTDB; Parks et al., 2018; https://gtdb.ecogenomic. (Khelifi et al., 2010, 2014); and growth with (per)chlorate org/), based on average nucleotide criteria to delineate species reduction combining biotic and abiotic reactions (Liebensteiner and on sets of protein markers to infer a taxonomic position et al., 2013). Along with the type strain, A. fulgidus 7324 has and define genomic clusters. Archaea were recognized as a been isolated from North Sea oilfield waters and its genome separate