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Kyrpidia Tusciae Comb. Nov. and Emendation of the Family Alicyclobacillaceae Da Costa And Lawrence Berkeley National Laboratory Recent Work Title Complete genome sequence of the thermophilic, hydrogen-oxidizing Bacillus tusciae type strain (T2) and reclassification in the new genus, Kyrpidia gen. nov. as Kyrpidia tusciae comb. nov. and emendation of the family Alicyclobacillaceae da Costa and... Permalink https://escholarship.org/uc/item/3m89z7ps Journal Standards in genomic sciences, 5(1) ISSN 1944-3277 Authors Klenk, Hans-Peter Lapidus, Alla Chertkov, Olga et al. Publication Date 2011-10-01 DOI 10.4056/sigs.2144922 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Standards in Genomic Sciences (2011) 5:121-134 DOI:10.4056/sigs.2144922 Complete genome sequence of the thermophilic, hydrogen-oxidizing Bacillus tusciae type strain (T2T) and reclassification in the new genus, Kyrpidia gen. nov. as Kyrpidia tusciae comb. nov. and emendation of the family Alicyclobacillaceae da Costa and Rainey, 2010 Hans-Peter Klenk1*, Alla Lapidus2, Olga Chertkov2,3, Alex Copeland2, Tijana Glavina Del Rio2, Matt Nolan2, Susan Lucas2, Feng Chen2, Hope Tice2, Jan-Fang Cheng2, Cliff Han2,3, David Bruce2,3, Lynne Goodwin2,3, Sam Pitluck2, Amrita Pati2, Natalia Ivanova2, Konstantinos Mavromatis2, Chris Daum2, Amy Chen4, Krishna Palaniappan4, Yun-juan Chang2,5, Miriam Land2,5, Loren Hauser2,5, Cynthia D. Jeffries2,5, John C. Detter2,3, Manfred Rohde6, Birte Abt1, Rüdiger Pukall1, Markus Göker1, James Bristow2, Victor Markowitz4, Philip Hugenholtz2,7, and Jonathan A. Eisen2,8 1 DSMZ – German Collection of Microorganisms and Cell Cultures GmbH, Braunschweig, Germany 2 DOE Joint Genome Institute, Walnut Creek, California, USA 3 Los Alamos National Laboratory, Bioscience Division, Los Alamos, New Mexico, USA 4 Biological Data Management and Technology Center, Lawrence Berkeley National Laboratory, Berkeley, California, USA 5 Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA 6 HZI – Helmholtz Centre for Infection Research, Braunschweig, Germany 7 Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, Australia 8 University of California Davis Genome Center, Davis, California, USA *Corresponding author: Hans-Peter Klenk Keywords: hydrogen-oxidizing, aerobe, facultative chemolithoautotroph, thermoacidophile, free-living, solfatara, spore-forming, Bacillaceae, GEBA Bacillus tusciae Bonjour & Aragno 1994 is a hydrogen-oxidizing, thermoacidophilic spore former that lives as a facultative chemolithoautotroph in solfataras. Although 16S rRNA gene sequencing was well established at the time of the initial description of the organism, 16S se- quence data were not available and the strain was placed into the genus Bacillus based on limited chemotaxonomic information. Despite the now obvious misplacement of strain T2T as a member of the genus Bacillus in 16S rRNA-based phylogenetic trees, the misclassification remained uncorrected for many years, which was likely due to the extremely difficult, analy- sis-hampering cultivation conditions and poor growth rate of the strain. Here we provide a taxonomic re-evaluation of strain T2T (= DSM 2912 = NBRC 15312) and propose its reclassi- fication as the type strain of a new species, Kyrpidia tusciae, and the type species of the new genus Kyrpidia, which is a sister-group of Alicyclobacillus. The family Alicyclobacillaceae da Costa and Rainey, 2010 is emended. The 3,384,766 bp genome with its 3,323 protein-coding and 78 RNA genes is part of the Genomic Encyclopedia of Bacteria and Archaea project. Introduction Strain T2T (= DSM 2912 = NBRC 15312) is the type [1]. In the original study of Bonjour and Aragno strain of the Bacillus tusciae [1]. Both strain T2T [1], DNA:DNA reassociation studies of strains T2T, and strain T201 were isolated from ponds in the Bacillus schlegelii (also autotrophic) and the ther- solfatara of San Federigo, a geothermal area near moacidophilic Bacillus acidocaldarius (later on Lago, Tuscany, Italy [1,Table 1], as indicated in the reclassified as Alicyclobacillus acidocaldarius) Latin species epithet tusciae, meaning from Tuscia from another hot spring were carried out. Because The Genomic Standards Consortium Kyrpidia tusciae comb. nov. of the low levels of hybridization observed, the The most frequently occurring keywords within authors proposed that strains T2T and T201 the labels of all environmental samples that were formed a distinct taxonomic unit [1]. However, hits were 'microbi' (13.3%), 'thermophil' (12.5%), only limited chemotaxonomic data was available 'cell, fuel' (12.4%), 'ecolog, firmicut, identifi, role' at the time and 16S rRNA sequence data was not (6.2%) and 'experi' (6.1%) (151 hits in total). The available, which led the authors to place the spe- most frequently occurring keywords within the cies into the genus Bacillus [1]. Rather difficult cul- labels of those environmental samples which tivation conditions and the poor growth rate of yielded hits of a higher score than the highest strain T2T likely delayed an earlier re- scoring species were 'microbi' (13.9%), 'cell, fuel, classification although Rainey et al. previously thermophil' (13.1%), 'ecolog, firmicut, identifi, noted the link to the genus Alicyclobacillus [19]. role' (6.5%), 'experi' (6.4%) and 'acetate-f' (4.7%) This was recently corroborated by the observation (124 hits in total). These keywords corroborate that strain T2T as well as A. acidocaldarius lack the the features of the environment from which strain sspE gene for acid-soluble spore proteins fre- T2T was isolated. quently found in members of the Bacillales [20]. Figure 1 shows the phylogenetic neighborhood of Here we present a summary classification and a B. tusciae in a 16S rRNA tree. The sequences of the set of features for B. tusciae strain T2T, a descrip- five 16S rRNA gene copies in the genome differ tion of the complete genome sequencing and an- from each other by up to eight nucleotides, and notation and a proposal to reclassify B. tusciae as a differ by up to six nucleotides from the previously member of the new genus Kyrpidia as Kyrpidia published 16S rRNA sequence AB042062. tuscae comb. nov. B. tusciae cells are straight rods measuring 0.8 x 4- Figure 2) with single laterally in- Classification and features serted flagella [1]. In young cultures, cells stain A representative genomic 16S rRNA sequence of Gram5 μm- positivelength ( and exhibit oval, subterminal B. tusciae T2T was compared using NCBI BLAST spores that swell the sporangium [1]. Cultures [21] under default settings (e.g., considering only grow at 55°C at a pH ranging from 4.2 to 4.8 [1]. the high-scoring segment pairs (HSPs) from the Although cells grow best under autotrophic condi- best 250 hits) with the most recent release of the tions via hydrogen oxidation, they can also grow Greengenes database [22] and the relative fre- heterotrophic on alcohols, amino acids and short quencies of taxa and keywords (reduced to their chain fatty acids, but not with sugars [1]. Sub- stems [23]) were determined, weighted by BLAST strate usage was described in detail by Bonjour scores. The most frequently occurring genera and Aragno [1]. Cells contain a soluble malate- were Alicyclobacillus (67.8%), Bacillus (18.2%), dehydrogenase activity, which cannot reduce py- Thermoactinomyces (6.0%), Paenibacillus (5.6%) ridine (NAD+/NAD(P)+) [1], nor NADH oxidation and Exiguobacterium (1.6%) (99 hits in total). Re- was observed [1]. Hydrogenase activity was re- garding the seven hits to sequences from mem- ported as being inducible [1]. An operational Cal- bers of the species, the average identity within vin cycle was reported based on the presence of HSPs was 99.6%, whereas the average coverage ribulose-1,5-bisphosphate carboxylase activity in by HSPs was 99.5%. Among all other species, the autotrophically-grown cells [1]. Autotrophically one yielding the highest score was A. acidiphilus grown cells show inclusions of poly- - NR_028637, which corresponds to an identity of hydroxybutyric acid [1]. 92.4% and an HSP coverage of 57.7%. (Note that β the Greengenes database uses the INSDC (= Chemotaxonomy EMBL/NCBI/DDBJ) annotation, which is not an The structure of the cell wall of strain T2T was re- authoritative source for nomenclature or classifi- ported as typically Gram-positive, without a pro- cation.) The highest-scoring environmental se- tein coat [1 -alicyclic fatty acids are lacking and quence was EU638396 ('Ecological Role Firmi- menaquinone MK-7 was identified as the main cutes Identified Thermophilic Microbial Fuel Cells quinone (personal]. ω communication Brian J. Tin- thermophilic microbial fuel cell acetate-fed expe- dall). riment clone SHBZ1905')), which showed an iden- tity of 99.4% and an HSP coverage of 90.0%. 122 Standards in Genomic Sciences Klenk et al. Table 1. Classification and general features of Kyrpidia tusciae strain T2T according to the MIGS recommenda- tions [2] and the NamesforLife database [3]. MIGS ID Property Term Evidence code Domain Bacteria TAS [4] Phylum Firmicutes TAS [5-7] Class Bacilli TAS [8,9] Current classification Order Bacillales TAS [10,11] Family Bacillaceae TAS [10,12] Genus Bacillus TAS [10,13,14] Species Bacillus tusciae TAS[1,15] Type strain T2 TAS [1] Family Alicyclobacillaceae TAS [9,16] Revised classification Genus Kyrpidia NAS Species Kyrpidia tusciae NAS Gram stain positive TAS [1] Cell shape straight rods TAS [1] Motility not reported, but lateral flagella visible TAS [1] Sporulation sporulating TAS [1] Temperature range
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