Streptobacillus Moniliformis Type Strain (9901T)
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Standards in Genomic Sciences (2009) 1: 300-307 DOI:10.4056/sigs.48727 Complete genome sequence of Streptobacillus T moniliformis type strain (9901 ) Matt Nolan1, Sabine Gronow2, Alla Lapidus1, Natalia Ivanova1, Alex Copeland1, Susan Lu- cas1, Tijana Glavina Del Rio1, Feng Chen1, Hope Tice1, Sam Pitluck1, Jan-Fang Cheng1, David Sims1,3, Linda Meincke1,3, David Bruce1,3, Lynne Goodwin1,3, Thomas Brettin1,3, Cliff Han1,3, John C. Detter1,3, Galina Ovchinikova1, Amrita Pati1, Konstantinos Mavromatis1, Natalia Mikhailova1, Amy Chen4, Krishna Palaniappan4, Miriam Land1,5, Loren Hauser1,5, Yun-Juan Chang1,5, Cynthia D. Jeffries1,5, Manfred Rohde6, Cathrin Spröer2, Markus Göker2, Jim Bris- tow1, Jonathan A. Eisen1,7, Victor Markowitz4, Philip Hugenholtz1, Nikos C. Kyrpides1, Hans- Peter Klenk2*, and Patrick Chain1,3 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 Oak Ridge National Laboratory, Oak Ridge, Tennessee, 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: Fusobacteria, 'Leptotrichiaceae', Gram-negative, rods in chains, L-form, zoonotic disease, non-motile, non-sporulating, facultative anaerobic, Tree of Life Streptobacillus moniliformis Levaditi et al. 1925 is the type and sole species of the genus Streptobacillus, and is of phylogenetic interest because of its isolated location in the sparsely populated and neither taxonomically nor genomically much accessed family 'Leptotrichiaceae' within the phylum Fusobacteria. The 'Leptotrichiaceae' have not been well characterized, genomically or taxonomically. S. moniliformis, is a Gram-negative, non- motile, pleomorphic bacterium and is the etiologic agent of rat bite fever and Haverhill fever. Strain 9901T, the type strain of the species, was isolated from a patient with rat bite fever. Here we describe the features of this organism, together with the complete genome sequence and annotation. This is only the second completed genome sequence of the order Fusobacte- riales and no more than the third sequence from the phylum Fusobacteria. The 1,662,578 bp long chromosome and the 10,702 bp plasmid with a total of 1511 protein-coding and 55 RNA genes are part of the Genomic Encyclopedia of Bacteria and Archaea project. Introduction Strain 9901T (= DSM 12112 = ATCC 14647 = NCTC members based on the low G+C content of 24- 10651) is the type strain of Streptobacillus monili- 26%, the fastidious requirements for growth and formis, which also represents the type species of the production of L-form organisms [3]. S. monili- the genus first described in 1925 by Levaditi et al. formis is commonly found in the nasopharynx of [1,2] The taxonomic history of S. moniliformis; affi- feral rats as well as in laboratory or pet rats. Be- liated several genera such as 'Haverhillia [1]' and tween 50 and 100% of wild rats carry the com- was only placed recently in the family “Leptotri- mensal and secrete it with their urine [4]. The or- chiaceae” (unpublished). It has also been sug- ganism has been associated with rat bite fever and gested that S. moniliformis be placed within the Haverhill fever in humans, following a bite or con- Mycoplasmatales due to its similarity to some tamination of food by rat urine, respectively. Be- The Genomic Standards Consortium Streptobacillus moniliformis type strain (9901T) fore it could be demonstrated that both diseases 9901T described in this report; other recently de- are caused by the same organism, the etiologic scribed strains (TSD4, IKB1, IKC1, and IKC5) iso- agent for Haverhill fever was called 'Haverhillia lated from feral rats in Japan differ in just 1-4 nuc- multiformis' [5]. Both are systemic illnesses cha- leotides [14]. No phylotypes from environmental racterized by fever, rigors and migratory po- screening or genomic surveys could be linked with lyarthralgias and nearly 75% of patients develop a more than 90% 16S rRNA sequence similarity to S. rash. Untreated, rat bite fever has a mortality rate moniliformis (status May 2009), indicating that the of approximately 10%, with most deaths occur- strain is rarely found in the environment outside ring due to endocarditis [6]. of its natural hosts. S. moniliformis is only the second species from the Figure 1 shows the phylogenetic neighborhood of S. phylum Fusobacteria for which a complete ge- moniliformis strain 9901T in a 16S rRNA based nome sequence is described. Here we present a tree. The sequences of the five 16S rRNA gene cop- summary classification and a set of features for S. ies in the genome of S. moniliformis 9901T do not moniliformis strain 9901T (Table 1), together with differ from each other, and differ by six nucleo- the description of the complete genomic sequenc- tides from the previously published 16S rRNA se- ing and annotation. quence generated from ATCC 14647 (Z35305). The difference between the genome data and the Classification and features reported 16S rRNA gene sequence is most likely Isolate H2730, from a clinical case of fatal rat bite due to sequencing errors in the previously re- fever in the US [13] perfectly matches the 16S ported sequence data. rRNA gene sequence of the genome of strain Figure 1. Phylogenetic tree highlighting the position of S. moniliformis 9901T relative to the other type strains of the family ‘Leptotrichiaceae’. The tree was inferred from 1399 aligned characters [15,16] of the 16S rRNA sequence under the maximum likelihood criterion [17] and rooted with the type strain of the family 'Fusobacteriaceae' The branches are scaled in terms of the expected num- ber of substitutions per site. Numbers above branches are support values from 1,000 bootstrap rep- licates if larger than 60%. Lineages with type strain genome sequencing projects registered in GOLD [18] are shown in blue, published genomes in bold, e.g. the GEBA type strain Leptotrichia buccalis [19]. S. moniliformis is a Gram-negative, non-motile, fas- dogs, cats, ferrets and pigs can also become hosts tidious, slow-growing and facultatively anaerobic and thus transfer the pathogen to humans. How- organism that grows as elongated rods (0.3-0.7 ever, the organism is not directly transmitted µm by 1-5 µm in length) which tend to form chains from person to person and thus presents a typical or filaments with occasional bulbar swellings zoonotic agent. A large number of case reports of leading to a necklace-like appearance ("monili- S. moniliformis infections have been published formis" means necklace-shaped) (Figure 2). The (references in [4]). For cultivation, complex media organism exists in two variants: the bacillary form containing blood, serum or ascitis fluid are neces- and a cell wall-deficient L-form, which is consi- sary and increased CO2 concentration enhances dered nonpathogenic [20]. The primary habitat of growth. The organism is extremely sensitive to S. moniliformis is small rodents, including rats sodium polyanethol sulfonate ("Liquoid"), an anti- (dominant reservoir) and more rarely gerbils, coagulant used in commercial blood culture bot- squirrels and mice. Rat-eating carnivores such as tles, which can lead to problems during primary 301 Standards in Genomic Sciences Nolan et al. isolation [21]. S. moniliformis is catalase and oxi- starch; H2S is produced. Arginine dihydrolase is dase negative and is biochemically rather inert. synthesized [22,23]. S. moniliformis is susceptible The metabolism is fermentative. Acid but no gas is - -lactamase activity produced from glucose, fructose, maltose and could be demonstrated thus far [10]. to all β lactam antibiotics, no β Figure 2. Scanning electron micrograph of S. moniliformis 9901T Chemotaxonomy tion and comprises a mixture of saturated and un- No data are available about the murein composi- saturated straight-chain acids: C16:0, C18:0, C18:1 and tion of strain 9901T. The fatty acid pattern of S. C18:2. The type of menaquinones and polar lipids moniliformis can be used for its rapid identifica- used by S. moniliformis has not been described yet. Table 1. Classification and general features of S. moniliformis 9901T according to the MIGS recommendations [7] MIGS ID Property Term Evidence code Domain Bacteria TAS [8] Phylum Fusobacteria TAS [9] Class Fusobacteria TAS [9] Current classification Order Fusobacteriales TAS [9] Family 'Leptotrichiaceae' NAS Genus Streptobacillus TAS [1] Species Streptobacillus moniliformis TAS [1] Type strain 9901 TAS [1] Gram stain negative TAS [1] Cell shape long rods TAS [1] Motility nonmotile TAS [1] Sporulation non-sporulating TAS [1] Temperature range mesophile TAS [1] Optimum temperature 37°C TAS [1] Salinity normal TAS [1] MIGS-22 Oxygen requirement facultative anaerobic TAS [1] http://standardsingenomics.org 302 Streptobacillus moniliformis type strain (9901T) Table 1. Classification and general features of S. moniliformis 9901T according to the MIGS recommendations [7] MIGS ID Property Term Evidence code Carbon source monosaccharides, starch TAS [10] Energy source carbohydrates TAS [10] MIGS-6 Habitat nasopharynx of rats TAS [1] MIGS-15 Biotic relationship free living NAS MIGS-14 Pathogenicity pathogenic for humans TAS [1] Biosafety level 2 TAS [11] Isolation patient with rat-bite fever NAS MIGS-4 Geographic location France NAS MIGS-5 Sample collection time unknown 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 for the living, isolated sample, but based on a generally accepted property for the species, or anecdotal evi- dence). These evidence codes are from the Gene Ontology project [12].