Atopobium Parvulum Type Stain IPP 1246
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Lawrence Berkeley National Laboratory Recent Work Title Complete genome sequence of Atopobium parvulum type strain (IPP 1246). Permalink https://escholarship.org/uc/item/1cs0z5p2 Journal Standards in genomic sciences, 1(2) ISSN 1944-3277 Authors Copeland, Alex Sikorski, Johannes Lapidus, Alla et al. Publication Date 2009 DOI 10.4056/sigs.29547 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Standards in Genomic Sciences (2009) 1: 166-173 DOI:10.4056/sigs.29547 Complete genome sequence of Atopobium parvulum type strain (IPP 1246T) Alex Copeland1, Johannes Sikorski2, Alla Lapidus1, Matt Nolan1, Tijana Glavina Del Rio1, Su- san Lucas1, Feng Chen1, Hope Tice1, Sam Pitluck1, Jan-Fang Cheng1, Rüdiger Pukall2, Olga Chertkov1,3, Thomas Brettin1,3, Cliff Han1,3, John C. Detter1,3, Cheryl Kuske1,3, David Bruce1,3, Lynne Goodwin1,3, Natalia Ivanova1, Konstantinos Mavromatis1, Natalia Mikhailova1, Amy Chen4, Krishna Palaniappan4, Patrick Chain1,5, Manfred Rohde6, Markus Göker2, Jim Bris- tow1, Jonathan A. Eisen1,7, Victor Markowitz4, Philip Hugenholtz1, Nikos C. Kyrpides1, Hans- Peter Klenk2*, and John C. Detter1,3 1 DOE Joint Genome Institute, Walnut Creek, California, USA 2 DSMZ - German Collection of Microorganisms and Cell Cultures GmbH, Braunschweig, Germany 3 Los Alamos National Laboratory, Bioscience Division, Los Alamos, New Mexico, USA 4 Biological Data Management and Technology Center, Lawrence Berkeley National Labora- tory, Berkeley, California, USA 5 Lawrence Livermore National Laboratory, Livermore, California, USA 6 HZI - Helmholtz Centre for Infection Research, Braunschweig, Germany 7 University of California Davis Genome Center, Davis, California, USA *Corresponding author: Hans-Peter Klenk Keywords: halitosis, obligately anaerobic, human respiratory tract, risk group 2, malodor, Co- riobacteriaceae Atopobium parvulum (Weinberg et al. 1937) Collins and Wallbanks 1993 comb. nov. is the type strain of the species and belongs to the genomically yet unstudied Atopobium/Olsenella branch of the family Coriobacteriaceae. The species A. parvulum is of interest because its members are frequently isolated from the human oral cavity and are found to be associated with halitosis (oral malodor) but not with periodontitis. Here we describe the features of this organism, together with the complete genome sequence, and annotation. This is the first complete genome sequence of the genus Atopobium, and the 1,543,805 bp long single repli- con genome with its 1369 protein-coding and 49 RNA genes is part of the Genomic Encyclo- pedia of Bacteria and Archaea project. Introduction Strain IPP 1246T (= DSM 20469 = ATCC 33793 = the sulfur containing amino acids cysteine and JCM 10300) is the type strain of the species Atopo- methionine [3,4]. However, for A. parvulum itself, bium parvulum and was first described by Wein- the production of these substances has not yet berg et al. 1937 as ‘Streptococcus parvulus’ (ba- been studied. A. parvulum has not been found to sonym) [1]. In 1992 it was reclassified as A. parvu- be significantly associated with chronic periodon- lum [2]. A. parvulum is of high interest because it titis, though a participation in periodontitis can has frequently been isolated from the human oral not be fully excluded [5]. Nevertheless, A. parvu- cavity, especially from the tongue dorsum, where lum has been associated with odontogenic infec- it has been associated with patients suffering from tions, e.g. dental implants, but also with the saliva halitosis (oral malodor) [3,4]. In general, the malo- of healthy subjects [6]. Here we present a sum- dorous compounds are volatile sulfur compounds, mary classification and a set of features for A. par- with the most frequent ones being hydrogen sul- vulum IPP 1246T together with the description of fide, methyl mercaptan, and dimethyl sulfide, the complete genomic sequencing and annotation. which are produced by bacterial metabolism of The Genomic Standards Consortium Copeland, et al. Classification and features Figure 1 shows the phylogenetic neighborhood of A. Phylotypes with significant 16S sequence similari- parvulum strain IPP P1246T in a 16S rRNA based ty to strain IPP 1246T were observed from intu- tree. The sequence of the sole copy of the 16S bated patients (EF510777) and from metagenom- rRNA gene in the genome is identical with the ic human skin surveys (GQ081350) [7]. No signifi- previously published sequence generated from cant similarities were found in human gut meta- ATCC 22793 (AF292372), but differs by four nuc- genomes (highest similarity is 92%, leotides from the sequence used for the last tax- BABE01011651) [8], or in marine metagenomes onomic emendation (X67150) [2]. (87%, AACY020304192) [9] (status June 2009). Figure 1. Phylogenetic tree of A. parvulum strain IPP 1246T, all other type strains of the genus Ato- pobium and the type strains of all other genera within the Coriobacteriaceae, inferred from 1345 aligned characters [10,11] of the 16S rRNA gene sequence under the maximum likelihood criterion [12]. The tree was rooted with the type strains of the genera within the subclass Rubrobacteridae. The branches are scaled in terms of the expected number of substitutions per site. Numbers above branches are support values from 1000 bootstrap replicates if larger than 60%. Lineages with type strain genome sequencing projects registered in GOLD [13] are shown in blue, published genomes in bold, including two of which are reported in this issue of SIGS [14,15] The cells are cocci (approximately 0.3 to 0.6 µm in sucrose, and trehalose; erythritol and xylose were diameter) that occur singly, in pairs, in clumps, weakly fermented; no acid was produced from and in short chains, occasionally with central amygdalin, arabinose, glycerol, glycogen, inositol, swelling [16,17] (Table 1 and Figure 2). The strains mannitol, melezitose, melibiose, pectin, raffinose, are non-motile and obligate anaerobic. Interes- rhamnose, ribose, sorbitol, or starch. Esculin was tingly, growth is substantially stimulated by hydrolyzed; neither starch nor hippurate was hy- 0.02% (vol/vol) Tween 80 and by 10% (vol/vol) drolyzed. Nitrate was not reduced. Indole was not rabbit serum added to culture media [16]. Strain formed. A solid acid curd formed in milk; neither IPP 1246T is susceptible to chloramphenicol (12 milk, gelatin, nor meat was digested. Neither cata- µg/ml), clindamycin (1.6 µg/ml), erythromycin (3 lase, urease, deoxyribonuclease, lecithinase, nor µg/ml), penicillin G (2 U/ml), and tetracycline (6 lipase was detected [17]. Other enzyme activities µg/ml) [17]. are positive for acid phosphatase, alanine aryla- Strain IPP 1126T produces acid (final pH < 4.7) -galactosidase, from cellobiose, esculin, fructose, galactose, glu- leucine arylamidase, pyroglutamic acid arylami- cose, inulin, lactose, maltose, mannose, salicin, dase,midase, glycine arginine arylamidase, arylamidase, tyrosine β arylamidase, http://standardsingenomics.org 167 Atopobium parvulum type stain IPP 1246 but negative for arginine dihydrolase, histidine (type A11.31 according to the DSMZ catalogue of arylamidase, proline arylamidase, serine arylami- strains) [25]. The major cellular fatty acids (FAME: dase, as determined using the API system [24]. fatty acid methyl ester; DMA: dimethylacetyl) are C18:1 cis-9 (38.2%, FAME), C18:1 cis-9 (24.1%, DMA), Chemotaxonomy C16:1 cis-9 (5.0%, FAME), C17:1 cis-8 (5.0%, FAME), The chemotaxonomy of A. parvulum IPP 1246T is C18:1 c11/t9/t6 (5.0%, FAME), C18:1 cis-11 (3.9%, unfortunately hardly studied. There are no data DMA), C14:0 (3.4%, FAME), C10:0 (3.0%, FAME) [16]. known on the polar lipids. The strain possesses cell- - -D-Asp T Tablewall 1. Classification peptidoglycan and ofgeneral type featuresA4α, L ofLys A. parvulum IPP 1146 according to the MIGS recommendations [18]. Evidence MIGS ID Property Term code Domain Bacteria TAS [19] Phylum Actinobacteria TAS [20] Class Actinobacteria TAS [20] Subclass Coriobacteridae TAS [21] Current classification Order Coriobacteriales TAS [21] Suborder “Coriobacterineae” TAS [21] Family Coriobacteriaceae TAS [21] Genus Atopobium TAS [2] Species Atopobium parvulum TAS [2] Type strain IPP 1246 Gram stain positive TAS [16] Cell shape small cocci that occasionally appear to be elliptical TAS [16] Motility nonmotile TAS [17] Sporulation nonsporulating TAS [16] Temperature range 25°C–45°C TAS [17] Optimum temperature 37°C–45°C TAS [17] Salinity less than 6.5% NaCl TAS [17] MIGS-22 Oxygen requirement obligate anaerobic TAS [17] acid production from cellobiose, esculin, fructose, Carbon source galactose, glucose, inulin, lactose, maltose, man- TAS [17] nose, salicin, sucrose, and trehalose Energy source carbohydrates TAS [17] MIGS-6 Habitat human respiratory tract. TAS [1,17] MIGS-15 Biotic relationship free living NAS MIGS-14 Pathogenicity associated with halitosis and human oral infections TAS [3,4,6] Biosafety level 2 TAS [22] unknown for this specific strain, but Weinberg et al Isolation reported that the principal habitat was the respirato- TAS [1,17] ry tract. MIGS-4 Geographic location unknown, probably France TAS [1,17] MIGS-5 Sample collection time before 1937 TAS [1,17] MIGS-4.1 Latitude – Longitude unknown MIGS-4.2 MIGS-4.3 Depth not reported MIGS-4.4 Altitude not reported Evidence codes - IDA: Inferred from Direct Assay (first time in publication); TAS: Traceable Author Statement (i.e., a direct report exists in the literature); NAS: Non-traceable Author Statement (i.e., not directly observed