Open Access

Complete genome sequence of Arcanobacterium haemolyticum type strain (11018T)

  • Montri Yasawong
  • , Hazuki Teshima,
  • , Alla Lapidus
  • , Matt Nolan
  • , Susan Lucas
  • , Tijana Glavina Del Rio
  • , Hope Tice
  • , Jan-Fang Cheng
  • , David Bruce,
  • , Chris Detter,
  • , Roxanne Tapia,
  • , Cliff Han,
  • , Lynne Goodwin,
  • , Sam Pitluck
  • , Konstantinos Liolios
  • , Natalia Ivanova
  • , Konstantinos Mavromatis
  • , Natalia Mikhailova
  • , Amrita Pati
  • , Amy Chen
  • , Krishna Palaniappan
  • , Miriam Land,
  • , Loren Hauser,
  • , Yun-Juan Chang,
  • , Cynthia D. Jeffries,
  • , Manfred Rohde
  • , Johannes Sikorski
  • , Rüdiger Pukall
  • , Markus Göker
  • , Tanja Woyke
  • , James Bristow
  • , Jonathan A. Eisen,
  • , Victor Markowitz
  • , Philip Hugenholtz
  • , Nikos C. Kyrpides
  • and Hans-Peter Klenk
Corresponding author

DOI: 10.4056/sigs.1123072

Received: 28 September 2010

Published: 31 October 2010

Abstract

Arcanobacterium haemolyticum (ex MacLean et al. 1946) Collins et al. 1983 is the type species of the genus Arcanobacterium, which belongs to the family Actinomycetaceae. The strain is of interest because it is an obligate parasite of the pharynx of humans and farm animal; occasionally, it causes pharyngeal or skin lesions. It is a Gram-positive, nonmotile and non-sporulating bacterium. The strain described in this study was isolated from infections amongst American soldiers of certain islands of the North and West Pacific. This is the first completed sequence of a member of the genus Arcanobacterium and the ninth type strain genome from the family Actinomycetaceae. The 1,986,154 bp long genome with its 1,821 protein-coding and 64 RNA genes is a part of the Genomic Encyclopedia of Bacteria and Archaea project.

Keywords:

obligate parasitehuman pathogenpharyngeal lesionsskin lesionsfacultative anaerobeActinomycetaceaeActinobacteriaGEBA

Introduction

Strain 11018T (= DSM 20595 = CCM 5947 = ATCC 9345 = NBRC 15585) is the type strain of the species A. haemolyticum, which is the type species of its genus Arcanobacterium [1]. Arcanobacterium is one of six genera in the family Actinomycetaceae [2-4]. The genus currently consists of nine validly described species. The strain was first described in 1946 by MacLean as ‘Corynebacterium haemolyticum’ [5]. Based on chemical features and the presence of unique phenotypic characteristics, the strain was subsequently transferred to the new genus Arcanobacterium as A. haemolyticum [1] and emended by Lehnen et al. in 2006 [6]. The generic name drives from the Latin word ‘arcanus’, meaning ‘secretive’ and the Latin word ‘bacterium’, a small rod, meaning ‘secretive bacterium’ [1]. The species epithet is derived from the Latin word ‘haema’ meaning ‘blood’ and the Neo-Latin word ‘lyticus’ meaning ‘able to loose or able to dissolve’ referring to blood-dissolving or hemolytic when the cells grow on blood agar [1]. There are many medical case reports that A. haemolyticum is occasionally isolated in patients with brain abscess [7-9], cellulitis [10,11], endocarditis [12], meningitis [13], peritonitis [14], post-traumatic ankle joint infection [15], septic arthritis [16], septicemia [17], sinusitis [11], soft tissue infections [18], venous ulcer infection [19], vertebral osteomyelitis [20] and wound infection [21,22]. Only rarely are cases reported in animals, where pathogenicity of A. haemolyticum has not been well documented [23-25]. Here we present a summary classification and a set of features for A. haemolyticum strain 11018T, together with the description of the complete genomic sequencing and annotation.

Classification and features

Strain 11018T is an obligate parasite of the pharynx of human and farm animals; occasionally it causes pharyngeal or skin lesions [26]. The strain was isolated from infections in American soldiers [5]. The 16S rRNA gene sequence of strain 11018T (AJ234059) is 99% identical to six culturable strains that were reported in GenBank (status July 2010). Five strains were isolated from infected horses [23]. Another culturable strain, Tr2-2X-1 (FJ477385), was isolated from gasoline contaminated soil. The 16S rRNA gene of strain 11018T shares 93.3-97.9% sequence identity with the sequences of the type strains from the other members of the genus Arcanobacterium [27]. The next closest relative outside of the genus Arcanobacterium is Dermacoccus barathri MT2.1T (92.3% sequence similarity) [27]. No phylotypes from environmental screening or metagenomic surveys could be linked to A. haemolyticum or even the genus Arcanobacterium, indicating a rare occurrence of these species in the habitats screened thus far (as of July 2010). A representative genomic 16S rRNA sequence of A. haemolyticum 11018T was compared using BLAST with the most resent release of the Greengenes database [28] and the relative frequencies of taxa and keywords, weighted by BLAST scores, were determined. The five most frequent genera were Arcanobacterium (42.4%), Dermacoccus (12.6%), Actinomyces (10.8%), Terrabacter (9.9%) and Sanguibacter (5.7%). The five most frequent keywords within the labels of environmental samples were 'skin' (6.6%), 'human' (5.0%), 'feedlot' (4.6%), 'elbow' (3.4%) and 'microbiota' (3.3%). The BLAST keywords analysis supports the biological insights into A. haemolyticum strain 11018T as described above.

Figure 1 shows the phylogenetic neighborhood of A. haemolyticum strain 11018T in a 16S rRNA based tree. The sequences of the four 16S rRNA gene copies in the genome differ from each other by up to two nucleotides, and differ by up to five nucleotides from the previously published sequence generated from CIP 103370 (AJ234059) which contains one ambiguous base call.

Figure 1

Phylogenetic tree highlighting the position of A. haemolyticum strain 11018T relative to the type strains of the other species within the genus Arcanobacterium and to the type strains of the other genera within the family Actinomycetaceae. The trees were inferred from 1,388 aligned characters [29,30] of the 16S rRNA gene sequence under the maximum likelihood criterion [31] and rooted in accordance with the current taxonomy. The branches are scaled in terms of the expected number of substitutions per site. Numbers above branches are support values from 1,000 bootstrap replicates [32] if larger than 60%. Lineages with type strain genome sequencing projects registered in GOLD [33] are shown in blue, published genomes in bold.

The cells of strain 11018T are slender or irregular rods (0.3-0.8 × 1.0-5.0 µm) [Table 1 and Figure 2]. The cells are Gram-positive, nonmotile, not acid-fast and without endospores [1]. In young cultures, cells may show clubbed ends sometimes arranged in V formation, but there are no filaments. In older cultures, cells segment into short, irregular rods and cocci [1]. Strain 11018T is facultatively anaerobic. The cells grow slowly on nutrient agar, but grow better on horse blood agar, giving small, convex, translucent colonies surrounded by a zone of complete hemolysis after two days at 37°C [1]. The selective medium for this strain was developed by Coman [39] and contains 5% sheep blood and 3.5% of NaCl. Cell growth is enhanced by the addition of CO2 [1]. The optimum growth temperature is 37°C [1,26]. Cells do not withstand heating at 60°C for 15 min [1,5]. Strain 11018T is chemoorganotrophic and requires nutritionally rich media for growth [1,26]. The fermentative metabolism of this strain produces acid but does not produce gas from glucose and several other carbohydrates on which growth occurs [1,26]. Acid production is mainly acetic, lactic and succinic acids [1,26]. Catalase, nitrate reduction and gelatine hydrolysis reactions are negative [6]. Strain 11018T produces N-acetyl-β-galactosidase, alkaline phosphatase, extracellular DNase, β-galactosidase, α-glucosidase and pyrazinamidase. It does not produce acid phosphatase, α-chymotrypsin, cystine arylamidase, esterase (C4), esterase lipase (C8), α-fucosidase, α-galactosidase, β-glucosidase, β-glucuronidase, leucine arylamidase, lipase (C14), α-mannosidase, naphthol-AS-BI-phosphohydrolase, trypsin, valine arylamidase and urease [1,6]. Strain 11018T is not able to ferment adonitol, L-arabitol, erythritol, D-fructose, glycerol, glycogen, D-mannitol and D-xylose. It is resistant to oxytetracycline (30µg per disc) but susceptible to nalidixic acid (30µg per disc), sulfamethoxazole trimethoprim (25µg per disc), amikacin (10µg per disc) or cefoxitin (30µg per disc) [1,42].

Table 1

Classification and general features of A. haemolyticum strain 11018T according to the MIGS recommendations [34].

MIGS ID

   Property

   Term

      Evidence code

   Current classification

   Domain Bacteria

      TAS [35]

   Phylum Actinobacteria

      TAS [36]

   Class Actinobacteria

      TAS [3]

   Subclass Actinobacteridae

      TAS [3,4]

   Order Actinomycetales

      TAS [2-5,37]

   Suborder Actinomycineae

      TAS [3,4]

   Family Actinomycetaceae

      TAS [2-5,37]

   Genus Arcanobacterium

      TAS [1,6,38]

   Species Arcanobacterium haemolyticum

      TAS [1,5,38]

   Type strain 11018

      TAS [1]

   Gram stain

   positive

      TAS [1]

   Cell shape

   slender, irregular rods (0.3-0.8 ×1.0-5.0 µm)

      TAS [1]

   Motility

   none

      TAS [1]

   Sporulation

   none

      TAS [1]

   Temperature range

   not reported

   Optimum temperature

   37°C

      TAS [1]

   Salinity

   3.5%

      TAS [39]

MIGS-22

   Oxygen requirement

   facultatively anaerobic

      TAS [1]

   Carbon source

   carbohydrates

      TAS [1,5,6]

   Energy source

   chemoorganotroph

      TAS [26]

MIGS-6

   Habitat

   pharynx of humans and farm animals

      TAS [26]

MIGS-15

   Biotic relationship

   obligate parasite

      TAS [26]

MIGS-14

   Pathogenicity

   pharyngeal or skin lesions

      TAS [26]

   Biosafety level

   2

      TAS [40]

   Isolation

   infections amongst American soldiers

      TAS [5]

MIGS-4

   Geographic location

   North and West Pacific

      TAS [5]

MIGS-5

   Sample collection time

   1946 or before

      TAS [1,5]

MIGS-4.1

   Latitude

   not reported

MIGS-4.2

   Longitude

   not reported

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 evidence). These evidence codes are from of the Gene Ontology project [41]. If the evidence code is IDA, then the property was directly observed by one of the authors or an expert mentioned in the acknowledgements

Figure 2

Scanning electron micrograph of A. haemolyticum strain 11018T

Chemotaxonomy

Strain 11018T possesses peptidoglycan type A5α based on L-Lys-L-Lys-D-Glu (unpublished, Norbert Weiss [43]). The predominant menaquinone is MK-9(H4) (85%) complemented by 15% MK-8(H4) [6]. The major cellular fatty acids when grown on blood agar at 35°C are straight-chain unsaturated acids C18:1 ω9c (37.0%), and saturated acids C18:0 (24.7%), C16:0 (22.5%) [6], which is similar to the cellular fatty acids spectrum reported from cells grown on sheep blood agar [31]: C18:1 cis9 (29%), C16:0 (23%), C18:2 (18%), C18:0 (17%), C10:0 (3%) and C14:0 (2%).

Genome sequencing and annotation

Genome project history

This organism was selected for sequencing on the basis of its phylogenetic position [44], and is part of the Genomic Encyclopedia of Bacteria and Archaea project [45]. The genome project is deposited in the Genome OnLine Database [33] and the complete genome sequence is deposited in GenBank. Sequencing, finishing and annotation were performed by the DOE Joint Genome Institute (JGI). A summary of the project information is shown in Table 2.

Table 2

Genome sequencing project information

   MIGS ID

    Property

    Term

   MIGS-31

    Finishing quality

    Finished

   MIGS-28

    Libraries used

    Three genomic libraries:    454 pyrosequence standard,    PE (12.5 kb insert size) libraries    and one Illumina standard library

   MIGS-29

    Sequencing platforms

    454 GS FLX Titanium, Illumina GAii

   MIGS-31.2

    Sequencing coverage

    83.8 × pyrosequence, 36.8 x Illumina

   MIGS-30

    Assemblers

    Newbler version 2.0.0-PostRelease-    11/04/2008, phrap, Velvet

   MIGS-32

    Gene calling method

    Prodigal 1.4, GenePRIMP

    INSDC ID

    CP002045

    Genbank Date of Release

    June 4, 2010

    GOLD ID

    Gc01291

    NCBI project ID

    37925

    Database: IMG-GEBA

    646564505

   MIGS-13

    Source material identifier

    DSM 20595

    Project relevance

    Tree of Life, GEBA

Growth conditions and DNA isolation

A. haemolyticum strain 11018T, DSM 20595, was grown anaerobically in DSMZ medium 104 (PYG modified medium) [46] at 37°C. DNA was isolated from 1-1.5 g of cell paste using MasterPure Gram Positive DNA Purification Kit (Epicentre MGP04100), with a modified protocol for cell lysis, st/LALM, as described in Wu et al. [45].

Genome sequencing and assembly

The genome was sequenced using a combination of Illumina and 454 sequencing platforms. All general aspects of library construction and sequencing can be found at the JGI website (Web Site). Pyrosequencing reads were assembled using the Newbler assembler version 2.0.0-PostRelease-11/04/2008 (Roche). The initial Newbler assembly consisted of 116 contigs in 28 scaffolds and was converted into a phrap assembly by making fake reads from the consensus, collecting the read pairs in the 454 paired end library. Illumina GAii sequencing data was assembled with Velvet [47] and the consensus sequences were shredded into 1.5 kb overlapped fake reads and assembled together with the 454 data. Draft assemblies were based on 166.4 Mb 454 draft and all of the 454 paired end data. Newbler parameters are -consed -a 50 -l 350 -g -m -ml 20.

The Phred/Phrap/Consed software package (Web Site) was used for sequence assembly and quality assessment in the following finishing process. After the shotgun stage, reads were assembled with parallel phrap (High Performance Software, LLC). Possible mis-assemblies were corrected with gapResolution (Web Site), Dupfinisher [48], or sequencing cloned bridging PCR fragments with subcloning or transposon bombing (Epicentre Biotechnologies, Madison, WI) [49]. Gaps between contigs were closed by editing in Consed, by PCR and by Bubble PCR primer walks (J.-F. Chang, unpublished). A total of 140 additional reactions were necessary to close gaps and to raise the quality of the finished sequence. Illumina reads were also used to improve the final consensus quality using an in-house developed tool - the Polisher [50]. The error rate of the completed genome sequence is less than 1 in 100,000. Together, the combination of the Illumina and 454 sequencing platforms provided 120.6 ×coverage of the genome. The final assembly contains 2.03 million Illumina reads and 0.52 million pyrosequencing reads.

Genome annotation

Genes were identified using Prodigal [51] as part of the Oak Ridge National Laboratory genome annotation pipeline, followed by a round of manual curation using the JGI GenePRIMP pipeline [52]. The predicted CDSs were translated and used to search the National Center for Biotechnology Information (NCBI) nonredundant database, UniProt, TIGRFam, Pfam, PRIAM, KEGG, COG, and InterPro databases. Additional gene prediction analysis and functional annotation was performed within the Integrated Microbial Genomes - Expert Review (IMG-ER) platform [53].

Genome properties

The genome consists of a 1,986,154 bp long chromosome with a 53.1% GC content (Table 3 and Figure 3). Of the 1,885 genes predicted, 1,821 were protein-coding genes, and 64 RNAs; 90 pseudogenes were also identified. The majority of the protein-coding genes (68.5%) were assigned with a putative function while the remaining ones were annotated as hypothetical proteins. The distribution of genes into COGs functional categories is presented in Table 4.

Table 3

Genome Statistics

Attribute

   Value

   % of Total

Genome size (bp)

   1,986,154

   100.00%

DNA coding region (bp)

   1,744,192

   87.82%

DNA G+C content (bp)

   1,055,308

   53.13%

Number of replicons

   1

Extrachromosomal elements

   0

Total genes

   1,885

   100.00%

RNA genes

   64

   3.40%

rRNA operons

   4

Protein-coding genes

   1,821

   96.60%

Pseudo genes

   90

   4.77%

Genes with function prediction

   1,292

   68.54%

Genes in paralog clusters

   154

   8.17%

Genes assigned to COGs

   1,308

   69.39%

Genes assigned Pfam domains

   1,402

   74.38%

Genes with signal peptides

   391

   20.74%

Genes with transmembrane helices

   492

   26.10%

CRISPR repeats

   1

Figure 3

Graphical circular map of the genome. From outside to the center: Genes on forward strand (color by COG categories), Genes on reverse strand (color by COG categories), RNA genes (tRNAs green, rRNAs red, other RNAs black), GC content, GC skew.

Table 4

Number of genes associated with the general COG functional categories

Code

   Value

  %age

    Description

J

   136

  9.7

    Translation, ribosomal structure and biogenesis

A

   1

  0.1

    RNA processing and modification

K

   99

  7.1

    Transcription

L

   119

  8.5

    Replication, recombination and repair

B

   0

  0.0

    Chromatin structure and dynamics

D

   21

  1.5

    Cell cycle control, cell division, chromosome partitioning

Y

   0

  0.0

    Nuclear structure

V

   36

  2.6

    Defense mechanisms

T

   51

  3.6

    Signal transduction mechanisms

M

   75

  5.4

    Cell wall/membrane/envelope biogenesis

N

   0

  0.0

    Cell motility

Z

   0

  0.0

    Cytoskeleton

W

   0

  0.0

    Extracellular structures

U

   27

  1.9

    Intracellular trafficking and secretion, and vesicular transport

O

   56

  4.0

    Posttranslational modification, protein turnover, chaperones

C

   86

  6.1

    Energy production and conversion

G

   125

  8.9

    Carbohydrate transport and metabolism

E

   77

  5.5

    Amino acid transport and metabolism

F

   58

  4.1

    Nucleotide transport and metabolism

H

   56

  4.0

    Coenzyme transport and metabolism

I

   34

  2.4

    Lipid transport and metabolism

P

   93

  6.6

    Inorganic ion transport and metabolism

Q

   12

  0.9

    Secondary metabolites biosynthesis, transport and catabolism

R

   152

  10.9

    General function prediction only

S

   87

  6.2

    Function unknown

-

   577

  30.6

    Not in COGs

Declarations

Acknowledgements

We would like to gratefully acknowledge the help of Gabriele Gehrich-Schröter for growing A. haemolyticum cultures and Susanne Schneider for DNA extraction and quality analysis (both at DSMZ). This work was performed under the auspices of the US Department of Energy Office of Science, Biological and Environmental Research Program, and by the University of California, Lawrence Berkeley National Laboratory under contract No. DE-AC02-05CH11231, Lawrence Livermore National Laboratory under Contract No. DE-AC52-07NA27344, and Los Alamos National Laboratory under contract No. DE-AC02-06NA25396, UT-Battelle and Oak Ridge National Laboratory under contract DE-AC05-00OR22725, as well as German Research Foundation (DFG) INST 599/1-1 and SI 1352/1-2 and Thailand Research Fund Royal Golden Jubilee Ph.D. Program No. PHD/0019/2548 for MY.


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References

  1. Collins MD, Jones D and Schofield GM. Reclassification of 'Corynebacterium haemolyticum' (MacLean, Liebow & Rosenberg) in the genus Arcanobacterium gen.nov. as Arcanobacterium haemolyticum nom.rev., comb.nov. J Gen Microbiol. 1982; 128:1279-1281PubMed
  2. Buchanan RE. Studies in the Nomenclature and Classification of the Bacteria: VIII. The Subgroups and Genera of the Actinomycetales. J Bacteriol. 1918; 3:403-406PubMed
  3. Stackebrandt E, Rainey FA and Ward-Rainey NL. Proposal for a new hierarchic classification system, Actinobacteria classis nov. Int J Syst Bacteriol. 1997; 47:479-491 View Article
  4. Zhi XY, Li WJ and Stackebrandt E. An update of the structure and 16S rRNA gene sequence-based definition of higher ranks of the class Actinobacteria, with the proposal of two new suborders and four new families and emended descriptions of the existing higher taxa. Int J Syst Evol Microbiol. 2009; 59:589-608 View ArticlePubMed
  5. MacLean PD, Liebow AA and Rosenberg AA. A hemolytic Corynebacterium resembling Corynebacterium ovis and Corynebacterium pyrogenes in man. J Infect Dis. 1946; 79:69-90PubMed
  6. Lehnen A, Busse H-J, Frölich K, Krasinska M, Kämpfer P and Speck S. Arcanobacterium bialowiezense sp. nov. and Arcanobacterium bonasi sp. nov., isolated from the prepuce of European bison bulls (Bison bonasus) suffering from balanoposthitis, and emended description of the genus Arcanobacterium Collins et al. 1983. Int J Syst Evol Microbiol. 2006; 56:861-866 View ArticlePubMed
  7. Altmann G and Bogokovsky B. Brain abscess due to Corynebacterium haemolyticum. Lancet. 1973; 301:378-379 View ArticlePubMed
  8. Vargas J, Hernandez M, Silvestri C, Jimenez O, Guevara N, Carballo M, Rojas N, Riera J, Alayo E and Fernandez M. Brain abscess due to Arcanobacterium haemolyticum after dental extraction. Clin Infect Dis. 2006; 42:1810-1811 View ArticlePubMed
  9. Washington JA, Martin WJ and Spiekerman RE. Brain abscess with Corynebacterium hemolyticum: report of a case. Am J Clin Pathol. 1971; 56:212-215PubMed
  10. Dobinsky S, Noesselt T, Rucker A, Maerker J and Mack D. Three cases of Arcanobacterium haemolyticum associated with abscess formation and cellulitis. Eur J Clin Microbiol Infect Dis. 1999; 18:804-806 View ArticlePubMed
  11. Limjoco-Antonio AD, Janda WM and Schreckenberger PC. Arcanobacterium haemolyticum sinusitis and orbital cellulitis. Pediatr Infect Dis J. 2003; 22:465-467 View ArticlePubMed
  12. Worthington MG, Daly BD and Smith FE. Corynebacterium hemolyticum endocarditis on a native valve. South Med J. 1985; 78:1261-1262PubMed
  13. Minárik T, Sufliarsky J, Trupl J and Krcmery V. Arcanobacterium haemolyticum invasive infections, including meningitis in cancer patients. BMC. J Infect. 1997; 34:91 View ArticlePubMed
  14. Farmer AD, Bruckner Holt CE, Le Roux G and Butterworth JR. Spontaneous bacterial peritonitis due to Arcanobacterium haemolyticum. BMC. J Infect. 2007; 54:516 View ArticlePubMed
  15. Hoosen AA, Rasool MN and Roux L. Posttraumatic ankle joint infection with Arcanobacterium haemolyticum: a case report. J Infect Dis. 1990; 162:780-781PubMed
  16. Goyal R, Singh NP and Mathur M. Septic arthritis due to Arcanobacterium haemolyticum. Indian J Med Microbiol. 2005; 23:63-65 View ArticlePubMed
  17. Ben-Yaacob D, Waron M, Boldur I, Gil I and Sompolinsky D. Septicemia due to Corynebacterium haemolyticum. Isr J Med Sci. 1984; 20:431-433PubMed
  18. Tan TY, Ng SY, Thomas H and Chan BK. Arcanobacterium haemolyticum bacteraemia and soft-tissue infections: case report and review of the literature. J Infect. 2006; 53:e69-e74 View ArticlePubMed
  19. Pânzaru C and Taranu T. Venous ulcer infection caused by Arcanobacterium haemolyticum. Roum Arch Microbiol Immunol. 2001; 60:323-327PubMed
  20. Ceilley RI. Foot ulceration and vertebral osteomyelitis with Corynebacterium haemolyticum. Arch Dermatol. 1977; 113:646-647 View ArticlePubMed
  21. Barker KF, Renton NE, Lee PY and James DH. Arcanobacterium haemolyticum wound infection. J Infect. 1992; 24:214-215 View ArticlePubMed
  22. Ritter E, Kaschner A, Becker C, Becker-Boost E, Wirsing von Konig CH and Finger H. Isolation of Arcanobacterium haemolyticum from an infected foot wound. Eur J Clin Microbiol Infect Dis. 1993; 12:473-474 View ArticlePubMed
  23. Hassan AA, Ulbegi-Mohyla H, Kanbar T, Alber J, Lammler C, Abdulmawjood A, Zschock M and Weiss R. Phenotypic and genotypic characterization of Arcanobacterium haemolyticum isolates from infections of horses. J Clin Microbiol. 2009; 47:124-128 View ArticlePubMed
  24. Richardson A and Smith PJ. Herd fertility and Corynebacterium haemolyticum in bovine semen. Vet Rec. 1968; 83:156-157PubMed
  25. Roberts RJ. Isolation of Corynebacterium haemolyticum from a case of ovine pneumonia. Vet Rec. 1969; 84:490PubMed
  26. Holt JG, Krieg NR, Sneath PHA, Staley JT, Williams ST. 1994. Bergey's manual of determinative bacteriology, 9th ed. Williams & Wilkins, Baltimore.
  27. Chun J, Lee JH, Jung Y, Kim M, Kim S, Kim BK and Lim YW. EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int J Syst Evol Microbiol. 2007; 57:2259-2261 View ArticlePubMed
  28. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P and Andersen GL. Greengenes, a chimera-checked 16S rRNA Gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006; 72:5069-5072 View ArticlePubMed
  29. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000; 17:540-552PubMed
  30. Lee C, Grasso C and Sharlow MF. Multiple sequence alignment using partial order graphs. Bioinformatics. 2002; 18:452-464 View ArticlePubMed
  31. Stamatakis A, Hoover P and Rougemont J. A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol. 2008; 57:758-771 View ArticlePubMed
  32. Pattengale ND, Alipour M, Bininda-Emonds ORP, Moret BME and Stamatakis A. How many bootstrap replicates are necessary? Lect Notes Comput Sci. 2009; 5541:184-200 View Article
  33. Liolios K, Chen IM, Mavromatis K, Tavernarakis N, Hugenholtz P, Markowitz VM and Kyrpides NC. The Genomes On Line Database (GOLD) in 2009: status of genomic and metagenomic projects and their associated metadata. Nucleic Acids Res. 2010; 38:D346-D354 View ArticlePubMed
  34. Field D, Garrity G, Gray T, Morrison N, Selengut J, Sterk P, Tatusova T, Thomson N, Allen MJ and Angiuoli SV. The minimum information about a genome sequence (MIGS) specification. Nat Biotechnol. 2008; 26:541-547 View ArticlePubMed
  35. Woese CR, Kandler O and Wheelis ML. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA. 1990; 87:4576-4579 View ArticlePubMed
  36. Garrity GM, Holt JG. The Road Map to the Manual. In: Garrity GM, Boone DR, Castenholz RW (eds), Bergey's Manual of Systematic Bacteriology, Second Edition, Volume 1, Springer, New York, 2001, p. 119-169.
  37. Skerman VBD, McGowan V and Sneath PHA. Approved Lists of Bacterial Names. Int J Syst Bacteriol. 1980; 30:225-420 View Article
  38. Validation List no. 10. Validation of the publication of new names and new combinations previously effectively published outside the IJSB. Int J Syst Bacteriol. 1983; 33:438-440 View Article
  39. Coman G, Panzaru C and Dahorea C. The isolation of Arcanobacterium haemolyticum from the pharyngeal exudate of children. Bacteriol Virusol Parazitol Epidemiol. 1996; 41:141-144PubMed
  40. Classification of bacteria and archaea in risk groups. TRBA 466.
  41. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS and Eppig JT. Gene Ontology: tool for the unification of biology. Nat Genet. 2000; 25:25-29 View ArticlePubMed
  42. Schofield GM and Schaal KP. A numerical taxonomic study of members of the Actinomycetaceae and related taxa. J Gen Microbiol. 1981; 127:237-259PubMed
  43. DSMZ. 2001. Catalogue of Strains, 7th ed. German Collection of Microorganisms and Cell Cultures, Braunschweig.
  44. Klenk H-P and Göker M. En route to a genome-based classification of Archaea and Bacteria? Syst Appl Microbiol. 2010; 33:175-182 View ArticlePubMed
  45. Wu D, Hugenholtz P, Mavromatis K, Pukall R, Dalin E, Ivanova NN, Kunin V, Goodwin L, Wu M and Tindall BJ. A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature. 2009; 462:1056-1060 View ArticlePubMed
  46. List of growth media used at DSMZ: Web Site
  47. Zerbino DR and Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 2008; 18:821-829 View ArticlePubMed
  48. Cliff S. Han, Patrick Chain. 2006. Finishing repeat regions automatically with Dupfinisher. In: Proceeding of the 2006 international conference on bioinformatics & computational biology. Hamid R Arabnia & Homayoun Valafar (eds), CSREA Press. June 26-29, 2006: 141-146.
  49. Sims D, Brettin T, Detter JC, Han C, Lapidus A, Copeland A, Glavina Del Rio T, Nolan M, Chen F and Lucas S. Complete genome sequence of Kytococcus sedentarius type strain (541T). Stand Genomic Sci. 2009; 1:12-20 View Article
  50. Lapidus A, LaButti K, Foster B, Lowry S, Trong S, Goltsman E. POLISHER: An effective tool for using ultra short reads in microbial genome assembly and finishing. AGBT, Marco Island, FL, 2008.
  51. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW and Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics. 2010; 11:119 View ArticlePubMed
  52. Pati A, Ivanova NN, Mikhailova N, Ovchinnikova G, Hooper SD, Lykidis A and Kyrpides NC. GenePRIMP: a gene prediction improvement pipeline for prokaryotic genomes. Nat Methods. 2010; 7:455-457 View ArticlePubMed
  53. Markowitz VM, Ivanova NN, Chen IMA, Chu K and Kyrpides NC. IMG ER: a system for microbial genome annotation expert review and curation. Bioinformatics. 2009; 25:2271-2278 View ArticlePubMed