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Non-contiguous finished genome sequence of Ornithobacterium rhinotracheale strain H06-030791

Abstract

The Gram-negative, pleomorphic, rod-shaped bacterium Ornithobacterium rhinotracheale is a cause of pneumonia and airsacculitis in poultry. It is a member of the family Flavobacteriaceae of the phylum “Bacteroidetes”. O. rhinotracheale strain H06-030791 was isolated from the lung of a turkey in North Carolina in 2006. Its genome consists of a circular chromosome of 2,319,034 bp in length with a total of 2243 protein-coding genes and nine RNA genes. Genome sequences are available for two additional strains of O. rhinotracheale, isolated in 1988 and 1995, the latter described in a companion genome report in this issue of SIGS. The genome sequence of O. rhinotracheale strain H06-030791, a more contemporary isolate, will be of value in establishing core and pan-genomes for O. rhinotracheale and elucidating its evolutionary history.

Introduction

Ornithobacterium rhinotracheale has been implicated as a cause of respiratory disease in domesticated fowl since at least 1981 [1]. Initially characterized as a phenotypically unusual bacterium of uncertain identity [2], Vandamme et al. [3] further characterized and named O. rhinotracheale in 1994. O. rhinotracheale is a global pathogen in farmed turkeys and chickens as well as a variety of other domesticated and wild birds, including chukar partridges, geese, ducks, guinea fowl, ostriches, gulls, pheasants, partridges, pigeons, quail, rooks, and falcons [4, 5]. Based on the reactivity of heat-extracted antigens with monospecific antisera, 18 serotypes of O. rhinotracheale have been defined, designated as A through R [1, 4], although not all isolates are typeable. The most common clinical signs of disease related to O. rhinotracheale are tracheitis, pneumonia, airsacculitis, sinusitis, and pericarditis [1, 4]. The bacterium is responsible for substantial economic losses to the poultry industry worldwide, resulting from decreased egg production, reduced eggshell quality and hatchability, reduced weight gain, increased mortality, and increased condemnation rates [69]. Whole-cell bacterin and live, attenuated vaccines have met with variable success, likely due to the lack of cross-protection against heterologous serotypes. Recent studies have identified antigens that appear to provide cross-protective immunity when formulated as a recombinant, multi-component subunit vaccine [10].

O. rhinotracheale strain H06-030791 was isolated in 2006 from the lung of a turkey in North Carolina and subsequently determined to be serotype A in the laboratory of Dr. K. V. Nagaraja at the University of Minnesota, St. Paul, MN. Further study revealed that growth of O. rhinotracheale strain H06-030791 in vitro is unaffected by the presence of an iron chelator [11] a phenotype not shared by most of the other field isolates tested. Whether or how this attribute plays a role in disease is not yet clear. Although O. rhinotracheale has generally been considered nonhemolytic on blood agar, Tabatabai et al. [12] documented strong β-hemolytic activity of O. rhinotracheale strain H06-030791 and suggested that a hemolysin-like protein may function as a virulence factor. Here we present a description of the non-contiguous finished genome of O. rhinotracheale strain H06-030791 and its annotation. This isolate (alias P5932) was provided to the National Animal Disease Center by the University of Minnesota and is available from the National Animal Disease Center Biological Agent Archive.

Organism information

Classification and features

The genus Ornithobacterium belongs to the class Flavobacteriia and is in the family Flavobacteriaceae [13] (Table 1). O. rhinotracheale is the sole species within the genus. Phylogenetic analysis based on 16S ribosomal RNA of O. rhinotracheale and other genera within the Flavobacteriaceae family is shown in Figure 1. The 16S rRNA sequences of O. rhinotracheale strain H06-030791 and the type strain, LMG 9086, share 99.9% nucleotide sequence identity. Three rRNA loci were found in the genome of O. rhinotracheale strain H06-030791. All O. rhinotracheale strains in Figure 1 were isolated from turkeys, with the exception of strain LMG 11554, which was cultured from a rook.

O. rhinotracheale strain H06-030791 is a Gram-negative, pleomorphic rod, when grown in broth medium, ranging from 1.57-2.19 μm (mean, 1.93 μm) in length and 0.42-0.64 μm (mean, 0..48 μm) in width (Figure 2). The bacterium is nonmotile and microaerophilic, and prefers a 7.5% CO2 humidified atmosphere from 30°C to 42°C for growth. Colonies are approximately 1 mm in diameter and yellowish in color after 48 h incubation at 37°C on blood agar. Although O. rhinotracheale type strain LMG 9086 is nonhemolytic [3], O. rhinotracheale strain H06-030791 is β-hemolytic on 5% sheep blood agar [12].

Biochemical tests for O. rhinotracheale strains can yield variable results [1]. After seven days of incubation at 37°C, O. rhinotracheale strain H06-030791 is weakly acidic on a triple sugar iron agar slant and does not produce hydrogen sulfide or gas. Dextrose is weakly fermented with or without the addition of 2% chicken serum, while galactose and lactose are weakly fermented only with the addition of 2% chicken serum. Sucrose, sorbitol, xylose, and mannitol are not fermented with or without the addition of 2% chicken serum. The isolate is lysine decarboxylase positive, ornithine decarboxylase negative, and urease negative.

Table 1 Classification and general features of O. rhinotracheale strain H06-030791 in accordance with the MIGS recommendations [14]
Figure 1
figure1

Phylogenetic tree based on 16S rRNA showing the position of O. rhinotracheale strain H06-030791 (highlighted in bold) in relation to other O. rhinotracheale isolates for which sequence is available and to the type strains (T) of closely related species and genera within the family Flavobacteriaceae . Escherichia coli (a member of the Enterobacteriaceae family) was included as an outgroup. An internal region of the 16S RNA gene (1251 bp with no gap-containing sites) was aligned using CLUSTALW and phylogenetic inferences were obtained using the maximum likelihood method and the Jukes-Cantor model within MEGA version 5.10 software [37]. Numbers at the nodes are percentages of bootstrap values obtained by repeating the analysis 1000 times to generate a majority consensus tree. GenBank accession numbers for the DNA sequences used are shown in parentheses. The scale bar represents 5% substitution per nucleotide position.

Figure 2
figure2

Transmission electron micrograph of O. rhinotracheale strain H06-030791 cells cultured in broth, using a Tecnai G2 (FEI, Hillsboro, OR) at an operating voltage of 80 kV. The average length of representative cells was 1.93 μm and the average width was 0.48 μm. The scale bar represents 500 nm.

Genome sequencing and annotation

Genome project history

Genome sequences are currently available for only two additional strains of O. rhinotracheale, the type strain LMG 9086 (isolated in 1988) and strain ORT-UMN 88 (isolated in 1995; see companion report in this issue of SIGS). O. rhinotracheale strain H06-030791 was selected for sequencing to provide a basis for comparative analysis of contemporary versus historical isolates. Additionally, O. rhinotracheale strain H06-030791 possesses phenotypic traits unique from those of O. rhinotracheale strain LMG 9086 and O. rhinotracheale strain ORT-UMN 88 [11, 12] that may permit a more accurate representation of the core and pan-genomes of O. rhinotracheale. The Whole Genome Shotgun project and non-contiguous finished genome sequence of O. rhinotracheale strain H06-030791 has been deposited in DDBJ/EMBL/GenBank under accession no. AXDE00000000. Sequencing, finishing, and final annotation were performed at the DNA Facility of Iowa State University and the National Animal Disease Center, Ames IA. A summary of the project information is given in Table 2.

Table 2 Project information of O. rhinotracheale strain H06-030791

Growth conditions and DNA isolation

A clonal population of O. rhinotracheale strain H06-030791 was derived from a single colony serially passaged three times and archived at −80°C for future analysis. The bacterium was grown on 5% sheep blood agar plates (Becton, Dickinson and Company, Sparks, MD) incubated for 48 h at 37°C with 7.5% CO2 and 15% humidity. Colonies were used to inoculate 5 ml of brain heart infusion broth in a snap-cap tube which was incubated at 37°C for 24 h with rotation at 100 rpm. Twenty ml of these BHI cultures were inoculated into 100 ml of fresh BHI in a 250-ml flask and incubated at 37°C for 48 h with rotation at 75 rpm (final OD600 = 0.278). An aliquot was plated on 5% sheep blood agar to confirm purity and 20 ml was removed for DNA preparation. Cells were pelleted successively into one 2-ml centrifuge tube at 16,000 × g. Genomic DNA was isolated using the Wizard Genomic DNA Purification Kit (Promega Corporation, Madison, WI) with the following modifications: the cell pellet was resuspended in 480 μl of 200 mM EDTA, 60 μl of 10 mg/ml lysozyme, and 60 μl of double distilled water prior to lysis, then 10 μl of 10 mg/ml RNase solution was added to the cell lysate. The precipitated genomic DNA was rehydrated at 65°C for 1 h in 10 mM Tris–HCl, pH 8.5, evaluated on a 6% agarose gel to verify the lack of low molecular weight fragments, and quantified using the Quant-iT PicoGreen ds DNA Assay Kit (Invitrogen, Carlsbad, CA).

Genome sequencing and assembly

A scaffolded genome was assembled using MIRA v. 3.4 [30] and the Roche gsAssembler v. 2.6 to achieve 49 × total genome coverage through the assembly of Roche GS FLX shotgun, GS FLX large insert (8.3 kb) mate pair, Illumina 75-bp single direction, and Illumina 2 × 75 bp paired-end sequencing reads. Some of remaining sequencing gaps in the scaffolded assembly were PCR amplified and sequenced by the Sanger method. GAP5 [31], from the Staden Package, was used as the editor for incorporating the gap-closing sequences, ultimately resulting in a high quality assembly consisting of eight contigs and seven gaps. (The genome start and end points are in a complete contig that was intentionally split to facilitate comparisons to a completed genome of the same genus and species.) Base calling errors in the genome assembly were corrected by using SEQuel [32] to map Illumina reads back to the contigs at approximately 100 × total coverage.

Genome annotation

The assembled genome was submitted to the National Center for Biotechnology Information (Bethesda, MD) through the Whole Genome Shotgun genome sequencing portal [33] and annotated with the NCBI Prokaryotic Genome Annotation Pipeline. Signal peptides were distinguished from transmembrane regions by using SignalP 4.0 software [34], transmembrane helices were predicted with the method of Krogh et al. [35], and the CRISPR motif was discovered with a web tool described by Griss et al. [36].

Genome properties

The genome properties and statistics of O. rhinotracheale strain H06-030791 (Accession AXDE00000000) are presented in Tables 3 and 4 and Figure 3. The non-contiguous finished genome consists of a circular 2,319,034 bp chromosome with a 34.53% G + C content and no plasmids. Of the 2,300 genes predicted, 2,243 are protein-coding genes, six are pseudogenes, and nine are RNA genes. The percentage of the protein-coding genes that were assigned a putative function is 47.17%. The distribution of genes into COGs functional categories is presented in Table 4. One CRISPR motif was also detected.

Table 3 Genome statistics of O. rhinotracheale strain H06-030791
Table 4 Number of genes associated with the 25 general COG functional categories of O. rhinotracheale strain H06-030791
Figure 3
figure3

Graphical map of the O. rhinotracheale strain H06-030791 chromosome. From outside to the center: genes on forward strand (color by COG categories), CDS on forward strand, tRNA, rRNA, other; CDS on reverse strand, tRNA, rRNA, other, genes on reverse strand (color by COG categories); GC content; GC skew, where green indicates positive values and magenta indicates negative values.

Conclusions

Prior to this report only a single genome sequence was available for O. rhinotracheale, from the type strain LMG 9086, and no corresponding analysis of an O. rhinotracheale genome has been published. Examination of the aligned genomes of these isolates revealed that rearrangements and inversions are the major distinguishing features. Relative to LMG 9086, the genome of H06-030791 contains a single rearrangement of ~31 Kb, a single inversion of ~17 Kb and three regions that are both inverted and rearranged, varying from ~59-354 Kb each, many with a transposase or transposon present at one terminus. Thus, mobile elements may play a role in shaping genome structure and evolution of O. rhinotracheale. Within one of the inverted and rearranged segments of H06-030791 is an apparent deletion of ~37 Kb found in LMG 9086, comprised primarily of CDSs annotated as hypothetical proteins but also including a holin family protein, an ATP-dependent serine protease, a helix-turn-helix protein and several phage-related proteins. Owing to gaps in the H06-030791 genome, the putative deletion requires confirmation but it does lie well within the boundaries of the contig in which it is found and adjacent sequences are syntenous with the LMG 9086 genome. Also within the same rearranged/inverted region is an insertion in H06-030791 with five predicted CDSs, four annotated as hypothetical proteins and one as a multidrug ABC transporter.

Notable phenotypes associated with H06-030791 but not the type strain include β-hemolytic activity [12] and the ability to grow in the presence of an iron chelator [11]. Only three CDSs whose annotations suggest a function in hemolytic activity were apparent in H06-030791. Identical or nearly identical homologs were found in the LMG 9086 genome. One additional CDS annotated in LMG 9086 as a hemolysin was also found in H06-030791, identical in sequence but annotated there as a glycerol acyltransferase. Among 15 CDSs collectively found in H06-030791 and LMG 9086 whose annotations suggest a role in iron acquisition or transport, only one was found to have considerable sequence divergence. The integral membrane protein and ferrous iron transporter FeoB is predicted to be identical in both isolates over the N-terminal 395 amino acids but only 94.7% identical over the C-terminal 301 amino acids. Motifs found within the divergent region of the protein include a ferrous iron transport protein B C terminus (PF07664.7) flanked by two gate nucleoside recognition domains (PF07670.9). As these are believed to comprise the membrane pore region, sequence heterogeneity may perhaps affect the specificity of transport. Other homologs in H06-030791 and LMG 9086 with obvious sequence divergence include several annotated as hypothetical proteins, a transcriptional regulator/sugar kinase with a highly divergent stretch of ~50 bp, a Crp/Fnr family transcriptional regulator with nearly all amino acid substitutions in the cyclic nucleotide binding domain (PF00027.24) of the predicted protein and a PAO141 family polyphosphate kinase 2, with substitutions concentrated in the polyphosphate kinase 2 domain (PF03976.9).

The genome sequence of H06-030791, together with those of the type strain and an additional, recently sequenced isolate [38] will provide a framework for future investigations designed to elucidate the genetic basis of virulence in O. rhinotracheale and for understanding genome structure and evolution.

References

  1. 1.

    Chin RP, Van Empel PCM, Hafez HM: Ornithobacterium rhinotracheale infection. In Diseases of Poultry. 12th edition. Edited by: Saif YM. Ames, IA: Blackwell Publishing; 2008:765–74.

    Google Scholar 

  2. 2.

    Charlton BR, Channing-Santiago SE, Bickford AA, Cardona CJ, Chin RP, Cooper GL, Droual R, Jeffrey JS, Meteyer CU, Shivaprasad HL, Walker RL: Preliminary characterization of a pleomorphic gram-negative rod associated with avian respiratory disease. J Vet Diagn Invest 1993, 5: 47–51. PMID: 8466980 10.1177/104063879300500111

    CAS  Article  PubMed  Google Scholar 

  3. 3.

    Vandamme P, Segers P, Vancanneyt M, Van Hove K, Mutters R, Hommez J, Dewhirst F, Paster B, Kersters K, Falsen E, Devriese LA, Bisgaard M, Hinz K-H, Mannheim W: Ornithobacterium rhinotracheale gen. nov. sp. nov., isolated from the avian respiratory tract. Int J System Bacteriol 1994,44(1):24–37. PMID: 8123560 10.1099/00207713-44-1-24

    CAS  Article  Google Scholar 

  4. 4.

    Hafez HM, Vandamme P: Genus XXXIX. Ornithobacterium Vandamme, Segers, Vancanneyt, Van Hove, Mutters, Hommez, Dewhirst, Paster, Kersters, Falsen, Devriese, Bisgaard, Hinz and Mannheim 1994b, 35VP . In Bergey’s Manual of Systematic Bacteriology, Volume 4. 2nd edition. Edited by: Krieg NR, Staley JT, Brown DR, Hedlund BP, Paster BJ, Ward NL, Ludwig W, Whitman WB. New York: Springer; 2011:250–4.

    Google Scholar 

  5. 5.

    Hafez HM, Lierz M: Ornithobacterium rhinotracheale in nestling falcons. Avian Dis 2010,54(1):161–3. PMID: 20408418 10.1637/9008-080309-Case.1

    Article  PubMed  Google Scholar 

  6. 6.

    van Veen L, Gruys E, Frik K, van Empel P: Increased condemnation of broilers associated with Ornithobacterium rhinotracheale . Vet Rec 2000,147(15):422–3. doi:10.1136/vr.147.15.422 10.1136/vr.147.15.422

    CAS  Article  PubMed  Google Scholar 

  7. 7.

    Sprenger SJ, Halvorson DA, Nagaraja KV, Spasojevic R, Dutton RS, Shaw DP: Ornithobacterium rhinotracheale infection in commercial laying-type chickens. Avian Dis 2000,44(3):725–9. PMID: 11007028 10.2307/1593120

    CAS  Article  PubMed  Google Scholar 

  8. 8.

    De Rosa M, Droual R, Chin RP, Shivaprasad HL, Walker RL: Ornithobacterium rhinotracheale infection in turkey breeders. Avian Dis 1996,40(4):865–74. doi:10.2307/1592311 10.2307/1592311

    CAS  Article  PubMed  Google Scholar 

  9. 9.

    van Empel PCM, Hafez HM: Ornithobacterium rhinotracheale : a review. Avian Pathol 1999,28(3):217–27. doi:10.1080/03079459994704 10.1080/03079459994704

    Article  Google Scholar 

  10. 10.

    Schuijffel DF, van Empel PCM, Segers RPAM, Van Putten JPM, Nuijten PJM: Vaccine potential of recombinant Ornithobacterium rhinotracheale antigens. Vaccine 2006, 24: 1858–67. doi:10.1016/j.vaccine.2005.10.031 10.1016/j.vaccine.2005.10.031

    CAS  Article  PubMed  Google Scholar 

  11. 11.

    Tabatabai LB, Zehr ES, Zimmerli MK, Nagaraja KV: Iron acquisition by Ornithobacterium rhinotracheale. Avian Dis 2008,52(3):419–25. PMID: 18939629 10.1637/8185-113007-Reg

    Article  PubMed  Google Scholar 

  12. 12.

    Tabatabai LB, Zimmerli MK, Zehr ES, Briggs RE, Tatum FM: Ornithobacterium rhinotracheale North American field isolates express a hemolysin-like protein. Avian Dis 2010,54(3):994–1001. PMID: 20945779 10.1637/9070-091409-Reg.1

    Article  PubMed  Google Scholar 

  13. 13.

    Ludwig W, Euzéby J, Whitman WB: Taxonomic outlines of the phyla Bacteroidetes, Spirochaetes, Tenericutes (Mollicutes), Acidobacteria, Fibrobacteres, Fusobacteria, Dictyoglomi, Gemmatimonadetes, Lentisphaerae, Verrucomicrobia, Chlamydiae, and Planctomycetes . In Bergey’s Manual of Systematic Bacteriology, Volume 4.. 2nd edition. Edited by: Krieg NR, Staley JT, Brown DR, Hedlund BP, Paster BJ, Ward NL, Ludwig W, Whitman WB. New York: Springer; 2011:21–2.

    Google Scholar 

  14. 14.

    Field D, Garrity G, Gray T, Morrison N, Selengut J, Sterk P, Tatusova T, Thomson N, Allen MJ, Angiuoli SV, Ashburner M, Axelrod N, Baldauf S, Ballard S, Boore J, Cochrane G, Cole J, Dawyndt P, De Vos P, dePamphilis C, Edwards R, Faruque N, Feldman R, Gilbert J, Gilna P, Glöckner FO, Goldstein P, Guralnick R, Haft D, Hancock D, et al.: The minimum information about a genome sequence (MIGS) specification. Nat Biotechnol 2008,26(5):541–7. doi:10.1038/nbt1360 10.1038/nbt1360

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  15. 15.

    Garrity GM, Parker CT (Eds): Nomenclature Abstract for "Bacteria". The NamesforLife Abstracts LLC: NamesforLife; 2013. http://doi.org/10.1601/nm.419.

  16. 16.

    Woese CR, Kandler O, Wheelis ML: Towards a natural system of organisms: proposal for the domains Archaea , Bacteria , and Eucarya . Proc Natl Acad Sci U S A 1990, 87: 4576–9. 10.1073/pnas.87.12.4576

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  17. 17.

    Garrity GM, Parker CT (Eds): Nomenclature Abstract for "Bacteroidetes". The NamesforLife Abstracts LLC: NamesforLife; 2013. http://doi.org/10.1601/nm.7927.

  18. 18.

    Garrity GM, Lilburn TG, Cole JR, Harrison SH, Euzéby J, Tindall BJ: Taxonomic outline of the Bacteria and Archaea, Release 7.7 March 6, 2007; Part 1 - The “Archea”, Phyla “Crenarchaeota” and “Euryarchaeota”. Taxonomic Outline 2007, 551–73. doi:10.1601/TOBA7.7

    Chapter  Google Scholar 

  19. 19.

    Garrity GM, Parker CT (Eds): Nomenclature Abstract for “Flavobacteriia”. The NamesforLife Abstracts LLC: NamesforLife; 2014. http://doi.namesforlife.com/10.1601/nm.22978.

  20. 20.

    Bernardet J-F: Class II. Flavobacteriia class. nov. In Bergey’s Manual of Systematic Bacteriology. 2nd ed. Volume 4. Edited by: Krieg NR, Staley JT, Brown DR, Hedlund BP, Paster BJ, Ward NL, Ludwig W, Whitman WB. New York: Springer; 2011:105.

    Google Scholar 

  21. 21.

    Garrity GM, Parker CT (Eds): Nomenclature Abstract for Flavobacteriales. The NamesforLife Abstracts LLC: NamesforLife; 2012. http://doi.org/10.1601/nm.8069.

  22. 22.

    Bernardet J-F: Order I. Flavobacteriales ord. nov. In Bergey’s Manual of Systematic Bacteriology. 2nd edition. Edited by: Krieg NR, Staley JT, Brown DR, Hedlund BP, Paster BJ, Ward NL, Ludwig W, Whitman WB. New York: Springer; 2011:105.

    Google Scholar 

  23. 23.

    Garrity GM, Parker CT (Eds): Nomenclature Abstract for Flavobacteriaceae. The NamesforLife Abstracts LLC: NamesforLife; 2014. http://doi.org/10.1601/nm.8070

  24. 24.

    Reichenbach H: Order 1. Cytophagales Leadbetter 1974, 99A. In Bergey’s Manual of Systematic Bacteriology. 1st ed. Volume 3. Edited by: Holt JG. Baltimore, MD: The Williams and Wilkins Co; 1989:2011–3.

    Google Scholar 

  25. 25.

    Bernardet JF, Nakagawa Y, Holmes B: Proposed minimal standards for describing new taxa of the family Flavobacteriaceae, and emended description of the family. Int J Syst Evol Microbiol 2002, 52: 1049–70. doi:10.1099/ijs. 0.02136–0 10.1099/ijs.0.02136-0

    CAS  PubMed  Google Scholar 

  26. 26.

    Garrity GM, Parker CT (Eds): Nomenclature Abstract for Ornithobacterium. The NamesforLife Abstracts LLC: NamesforLife; 2009. http://doi.org/10.1601/nm.8175.

  27. 27.

    Vandamme P, Segers P, Vancanneyt M, van Hove K, Mutters R, Hommez J, Dewhirst F, Paster B, Kersters K, Falsen E, Devriese LA, Bisgaard M, Hinz K-H, Mannheim W: Ornithobacterium rhinotracheale gen. nov., sp. nov., isolated from the avian respiratory tract. Int J Syst Bacteriol 1994, 44: 24–37. doi:10.1099/00207713–44–1-24 10.1099/00207713-44-1-24

    CAS  Article  PubMed  Google Scholar 

  28. 28.

    BAuA) GFIfOSaH. 2010 Classification of prokaryotes (bacteria and archaea) into risk groups, technical rules for biological agents (TRBA) 466:159. Bundesanstalt für Arbeitsshutz und Arbeitsmedizin (BAuA http://www.baua.de/de/Startseite.html

  29. 29.

    Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G: Gene ontology: tool for the unification of biology. Nat Biotechnol 2000,25(1):25–9. doi:10.1038/75556

    CAS  Google Scholar 

  30. 30.

    Chevreux B, Wetter T, Suhai S: Genome sequence assembly using trace signals and additional sequence information. Comp. Sci. Biol.: Proc. German Conference on Bioinformatics GCB ’99 (GCB) 1999, 99: 45–56. http://www.bioinfo.de/isb/gcb99/talks/chevreux/

    Google Scholar 

  31. 31.

    Bonfield JK, Whitwham A: Gap5--editing the billion fragment sequence assemby. Bioinformatics 2010,26(14):1699–703. doi:10.1093/bioinformatics/btq268 10.1093/bioinformatics/btq268

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  32. 32.

    Ronen R, Boucher C, Chitsaz H, Pevzner P: SEQuel: improving the accuracy of genome assemblies. Bioinformatics 2012,28(12):i188–96. doi:10.1093/bioinformatics/bts219 10.1093/bioinformatics/bts219

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  33. 33.

    portal NWGSWgsp https://submit.ncbi.nlm.nih.gov/subs/wgs/

  34. 34.

    Petersen TN, Brunak S, von Heijne G, Nielsen H: SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 2011,8(10):785–6. doi:10.1038/nmeth.1701 10.1038/nmeth.1701

    CAS  Article  PubMed  Google Scholar 

  35. 35.

    Krogh A, Larson B, von Heijne G, Sonnhammer ELL: Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J Mol Biol 2001,305(3):567–80. doi:10.1006/jmbi.2000.4315 10.1006/jmbi.2000.4315

    CAS  Article  PubMed  Google Scholar 

  36. 36.

    Grissa I, Vergnaud G, Pourcel C: CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 2007, 35: W52–7. doi:10.1093/nar/gkm360 10.1093/nar/gkm360

    PubMed Central  Article  PubMed  Google Scholar 

  37. 37.

    Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011,28(10):2731–9. doi:10.1093/molbev/msr121 10.1093/molbev/msr121

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  38. 38.

    Zehr ES, Bayles DO, Boatwright WD, Tabatabai LB, Register KB: Complete genome sequence of Ornithobacterium rhinotracheale strain ORT-UMN 88. Stand . Genomic Sci 2014, 9: 16. doi:10.1186/1944–3277–9-16

    Article  Google Scholar 

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Acknowledgements

We thank Michael Baker of the Iowa State University DNA Facility, Ames, IA and David Alt of the Infectious Bacterial Diseases Research Unit at the National Animal Disease Center, Ames, IA for their DNA sequencing expertise. We thank Linda Cox of the National Veterinary Services Laboratories in Ames, IA for performing the biochemical testing and Judith Stasko and James Fosse of the National Centers for Animal Health, Ames, IA for electron microscopy and image preparation for publication, respectively.

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Correspondence to Emilie S Zehr.

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The authors declare that they have no competing interests.

Authors’ contributions

EZ participated in genome sequencing and drafted the original manuscript. DB directed genome sequence assembly and bioinformatics analyses. WB participated in genome sequencing and post-sequencing analyses. LT conceived of the study and participated in genome sequencing. KR participated in post-sequencing analysis and revised the manuscript. All authors read and approved the final manuscript.

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Zehr, E.S., Bayles, D.O., Boatwright, W.D. et al. Non-contiguous finished genome sequence of Ornithobacterium rhinotracheale strain H06-030791. Stand in Genomic Sci 9, 14 (2014). https://doi.org/10.1186/1944-3277-9-14

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Keywords

  • Ornithobacterium rhinotracheale
  • Respiratory disease
  • Poultry
  • Genome sequence