Open Access

Complete genome sequence of Brachyspira murdochii type strain (56-150T)

  • Amrita Pati1,
  • Johannes Sikorski2,
  • Sabine Gronow2,
  • Christine Munk3,
  • Alla Lapidus1,
  • Alex Copeland1,
  • Tijana Glavina Del Tio1,
  • Matt Nolan1,
  • Susan Lucas1,
  • Feng Chen1,
  • Hope Tice1,
  • Jan-Fang Cheng1,
  • Cliff Han1, 3,
  • John C. Detter1, 3,
  • David Bruce1, 3,
  • Roxanne Tapia3,
  • Lynne Goodwin1, 3,
  • Sam Pitluck1,
  • Konstantinos Liolios1,
  • Natalia Ivanova1,
  • Konstantinos Mavromatis1,
  • Natalia Mikhailova1,
  • Amy Chen4,
  • Krishna Palaniappan4,
  • Miriam Land1, 5,
  • Loren Hauser1, 5,
  • Yun-Juan Chang1, 5,
  • Cynthia D. Jeffries1, 5,
  • Stefan Spring2,
  • Manfred Rohde6,
  • Markus Göker2,
  • James Bristow1,
  • Jonathan A. Eisen1, 7,
  • Victor Markowitz4,
  • Philip Hugenholtz1,
  • Nikos C. Kyrpides1 and
  • Hans-Peter Klenk2
Standards in Genomic Sciences20102:2030260

DOI: 10.4056/sigs.831993

Published: 30 June 2010

Abstract

Brachyspira murdochii Stanton et al. 1992 is a non-pathogenic, host-associated spirochete of the family Brachyspiraceae. Initially isolated from the intestinal content of a healthy swine, the ‘group B spirochaetes’ were first described as Serpulina murdochii. Members of the family Brachyspiraceae are of great phylogenetic interest because of the extremely isolated location of this family within the phylum ‘Spirochaetes’. Here we describe the features of this organism, together with the complete genome sequence and annotation. This is the first completed genome sequence of a type strain of a member of the family Brachyspiraceae and only the second genome sequence from a member of the genus Brachyspira. The 3,241,804 bp long genome with its 2,893 protein-coding and 40 RNA genes is a part of the Genomic Encyclopedia of Bacteria and Archaea project.

Keywords

host-associated non-pathogenic motile anaerobic Gram-negative Brachyspiraceae Spirochaetes GEBA

Introduction

Strain 56–150T (= DSM 12563 = ATCC 51284 = CIP 105832) is the type strain of the species Brachyspira murdochii. This strain was first described as Serpulina murdochii [1,2], and later transferred to the genus Brachyspira [3]. The genus Brachyspira currently consists of seven species, with Brachyspira aalborgi as the type species [4,5]. The genus Brachyspira is the only genus in the not yet formally described family ‘Brachyspiraceae’ [6,7]. The generic name derives from ‘brachys’, Greek for short, and ‘spira’, Latin for a coil, a helix, to mean ‘a short helix’ [5]. The species name for B. murdochii derives from the city of Murdoch, in recognition of work conducted at Murdoch University in Western Australia, where the type strain was identified [1]. Some species of the genus Brachyspira cause swine dysentery and porcine intestinal spirochetosis. Swine dysentery is a severe, mucohemorrhagic disease that sometimes leads to death of the animals [1]. B. murdochii is generally not considered to be a pathogen, although occasionally it has been seen in association with colitis in pigs [3,8], and was also associated with clinical problems on certain farms [911].

In 1992, a user-friendly and robust novel PCR-based restriction fragment length polymorphism analysis of the Brachyspira nox-gene was developed, which allows one to identify, with high specificity, members of B. murdochii using only two restriction endonucleases [12]. More recently, a multi-locus sequence typing scheme was developed that facilitates the identification of Brachyspira species and reveals the intraspecies diversity of B. murdochii [13] (see also http://pubmlst.org/brachyspira/).

Only one genome of a member of the family ‘Brachyspiraceae’ been sequenced to date: B. hyodysenteriae strain WA1 [14],. It is an intestinal pathogen of pigs. Based on 16S rRNA sequence this strain is 0.8% different from strain 56–150T. Here we present a summary classification and a set of features for B. murdochii 56–150T, together with the description of the complete genomic sequencing and annotation.

Classification and features

Brachyspira species colonize the lower intestinal tract (cecum and colons) of animals and humans [6]. The type of B. murdochii, 56–150T, was isolated from a healthy swine in Canada [1,15]. Other isolates have been obtained from wild rats in Ohio, USA, from laboratory rats in Murdoch, Western Australia [16], and from the joint fluid of a lame pig [17]. Further isolates have been obtained from the feces or gastrointestinal tract of pigs in Canada, Tasmania, Queensland, and Western Australia [2,15]. The type strains of the other species of the genus Brachyspira share 95.9-99.4% 16S rRNA sequence identity with strain 56–150T. GenBank contains 16S rRNA sequences for about 250 Brachyspira isolates, all of which share at least 96% sequence identity with strain 56–150T [18]. The closest related type strain of a species outside of the Brachyspira, but within the order Spirochaetales, is Turneriella parva [19], which exhibits only 75% 16S rRNA sequence similarity [18]. 16S rRNA sequences from environmental samples and metagenomic surveys do not exceed 78–79% sequence similarity to strain 56–150T, with the sole exception of one clone from a metagenome analysis of human diarrhea [20], indicating that members of the species, genus and even family are poorly represented in the habitats outside of various animal intestines screened thus far (status March 2010).

Figure 1 shows the phylogenetic neighborhood of B. murdochii 56–150T in a 16S rRNA based tree. The sequence of the single 16S rRNA gene in the genome sequence is identical with the previously published 16S rRNA gene sequence generated from DSM 12563 (AY312492).
Figure 1.

Phylogenetic tree highlighting the position of B. murdochii 56–150T relative to the other type strains within the genus and to the type strains of the other genera within the class Spirochaetes (excluding members of the Spirochaetaceae). The tree was inferred from 1,396 aligned characters [21,22] of the 16S rRNA gene sequence under the maximum likelihood criterion [23] 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 if [24] larger than 60%. Lineages with type strain genome sequencing projects registered in GOLD [25] are shown in blue, published genomes in bold.

The cells of B. murdochii 56-l50T were 5–8 by 0.35–0.4 µm in size (Table 1 and Figure 2), and each cell possessed 22 to 26 flagella (11 to 13 inserted at each end) [1]. In brain/heart infusion broth containing 10% calf serum (BHIS) under an N2-O2 (99::l) atmosphere, strain 56–150T had optimum growth temperatures of 39 to 42°C (shortest population doubling times and highest final population densities) [1]. In BHIS broth at 39°C, the doubling times of strain 56–150T were 2 to 4 h, and the final population densities were 0.5 x l09 to 2.0 x l09 cells/ml. Strain 56–150T did not grow at 32 or 47°C [1].
Figure 2.

Scanning electron micrograph of B. murdochii 56–150T

Table 1.

Classification and general features of B. murdochii 56–150T according to the MIGS recommendations [26]

MIGS ID

Property

Term

Evidence code

 

Current classification

Domain Bacteria

TAS [27]

 

Phylum Spirochaetes

TAS [28]

 

Class Spirochaetes

TAS [28]

 

Order Spirochaetales

TAS [29,30]

 

Family Brachyspiraceae

TAS [31]

 

Genus Brachyspira

TAS [5]

 

Species Brachyspira murdochii

TAS [1]

 

Type strain 56–150

TAS [1]

 

Gram stain

negative

TAS [1]

 

Cell shape

helical cells with regular coiling pattern

TAS [1]

 

Motility

motile (periplasmic flagella)

TAS [1]

 

Sporulation

non-sporulating

TAS [1]

 

Temperature range

does not grow at 32°C or 47°C

TAS [1]

 

Optimum temperature

39°C

TAS [1]

 

Salinity

unknown

TAS

MIGS-22

Oxygen requirement

anaerobic, aerotolerant

TAS [1]

 

Carbon source

soluble sugars

TAS [1]

 

Energy source

chemoorganotrophic

TAS [1]

MIGS-6

Habitat

animal intestinal tract

TAS [6]

MIGS-15

Biotic relationship

host-associated

TAS [32]

MIGS-14

Pathogenicity

no

TAS [33]

 

Biosafety level

1

TAS [34]

 

Isolation

swine

TAS [15]

MIGS-4

Geographic location

Quebec, Canada

TAS [15]

MIGS-5

Sample collection time

1992

TAS [15]

MIGS-4.1

Latitude

52.939

TAS [1]

MIGS-4.2

Longitude

−73.549

TAS [1]

MIGS-4.3

Depth

not reported

TAS

MIGS-4.4

Altitude

not reported

TAS

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 [35]. If the evidence code is IDA, then the property was directly observed by one of the authors or an expert mentioned in the acknowledgements.

Substrates that support growth of strain 56–150T in HS broth (basal heart infusion broth containing 10% fetal calf serum) include glucose, fructose, sucrose, N-acetylglucosamine, pyruvate, L-fucose, cellobiose, trehalose, maltose, mannose, and lactose, but not galactose, D-fucose, glucosamine, ribose, raffinose, rhamnose, or xylose [1]. In HS broth supplemented with 0.4% glucose under an N2-O2 (99:l) atmosphere, the metabolic end products of strain 56–150T are acetate, butyrate, ethanol, CO2, and H2. Strain 56–150T produces more H2 than CO2 [1], which is indicative of NADH-ferredoxin oxidoreductase reaction [6]. The ethanol is likely to be formed from acetyl-CoA by the enzymes acetaldehyde dehydrogenase and alcohol dehydrogenase [6]. Strain 56–150T is weakly hemolytic, negative for indole production, does not hydrolyze hippurate, is negative for α-galactosidase and α-glucosidase activity, but positive for β-glucosidase activity [1]. Strain 56–150T is anaerobic but aerotolerant [1].

Minimal inhibitory concentrations have been determined for strain 56–150T for tiamulin hydrogen fumarate, tylosin tartrate, erythromycin, clindamycin hydrochloride, virginiamycin, and carbadox [36]. Several strains of B. murdochii have been described to be naturally resistant against the rifampicin [7,32]. Also, a ring test for quality assessment for diagnostics and antimicrobial susceptibility testing of the genus Brachyspira has been reported [37].

Chemotaxonomy

At present there are no reports on the chemotaxonomy of B. murdochii. However, some data are available for B. innocens (formerly classified as Treponema innocens [6]), the species that is currently most closely related to B. murdochii [13]. B. innocens cellular phospholipids and glycolipids were found to contain acyl (fatty acids with ester linkage) with alkenyl (unsaturated alcohol with ether linkage) side chains [6,38]. The glycolipid of B. innocens contains monoglycosyldiglyceride (MGDG) and, in most strains, acylMGDG is also found, with galactose as the predominant sugar moiety [38].

Genome sequencing and annotation

Genome project history

This organism was selected for sequencing on the basis of its phylogenetic position [39], and is part of the Genomic Encyclopedia of Bacteria and Archaea project [40]. The genome project is deposited in the Genome OnLine Database [25] 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

Four genomic libraries: two Sanger 6kb and 8 kb pMCL200 library, one fosmid library, one 454 standard library

MIGS-29

Sequencing platforms

ABI3730, 454 GS FLX

MIGS-31.2

Sequencing coverage

19.7× Sanger; 48.9× pyrosequence

MIGS-30

Assemblers

Newbler version 1.1.02.15, phrap

MIGS-32

Gene calling method

Prodigal 1.4, GenePRIMP

 

INSDC ID

CP001959

 

Genbank Date of Release

May 13, 2010

 

GOLD ID

Gc01276

 

NCBI project ID

29543

 

Database: IMG-GEBA

2502422316

MIGS-13

Source material identifier

DSM 12563

 

Project relevance

Tree of Life, GEBA

Growth conditions and DNA isolation

B. murdochii, strain 56–150T, DSM 12563, was grown anaerobically in DSMZ medium 840 (Serpulina murdochii medium) [41] at 37°C. DNA was isolated from 0.5–1 g of cell paste using Qiagen Genomic 500 DNA Kit (Qiagen, Hilden, Germany) with lysis modification st/L according to Wu et al. [40].

Genome sequencing and assembly

The genome was sequenced using a combination of Sanger and 454 sequencing platforms. All general aspects of library construction and sequencing performed can be found at the JGI website (http://www.jgi.doe.gov/). In total, 861,386 Pyrosequencing reads were assembled using the Newbler assembler version 1.1.02.15 (Roche). Large Newbler contigs were broken into 3,554 overlapping fragments of 1,000 bp and entered into assembly as pseudo-reads. The sequences were assigned quality scores based on Newbler consensus q-scores with modifications to account for overlap redundancy and adjust inflated q-scores. A hybrid 454/Sanger assembly was made using the parallel phrap assembler (High Performance Software, LLC). Possible misassemblies were corrected with Dupfinisher or transposon bombing of bridging clones [42]. A total of 300 Sanger finishing reads were produced to close gaps, to resolve repetitive regions, and to raise the quality of the finished sequence. The error rate of the completed genome sequence is less than 1 in 100,000. Together, the combination of the Sanger and 454 sequencing platforms provided 68.6× coverage of the genome. The final assembly contains 79,829 Sanger reads and 861,386 pyrosequencing reads.

Genome annotation

Genes were identified using Prodigal [43] as part of the Oak Ridge National Laboratory genome annotation pipeline, followed by a round of manual curation using the JGI GenePRIMP pipeline [44]. The predicted CDSs were translated and used to search the National Center for Biotechnology Information (NCBI) nonredundant database, UniProt, TIGR-Fam, 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 [45].

Genome properties

The genome is 3,241,804 bp long and comprises one main circular chromosome with an overall GC content of 27.8% (Table 3 and Figure 3). Of the 2,893 genes predicted, 2,853 were protein-coding genes, and 40 RNAs. A total of 44 pseudogenes were identified. The majority of the protein-coding genes (66.2%) were assigned a putative function while those remaining were annotated as hypothetical proteins. The distribution of genes into COGs functional categories is presented in Table 4.
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 3.

Genome Statistics

Attribute

value

% of Total

Genome size (bp)

3,241,804

100.00%

DNA coding region (bp)

2,841,470

87.65%

DNA G+C content (bp)

899,647

27.75%

Number of replicons

1

 

Extrachromosomal elements

0

 

Total genes

2,893

100.00%

RNA genes

40

1.38%

rRNA operons

1

 

Protein-coding genes

2,893

98.62%

Pseudo genes

44

1.52%

Genes with function prediction

1,914

66.16%

Genes in paralog clusters

610

21.09%

Genes assigned to COGs

1,815

62.74%

Genes assigned Pfam domains

1,973

68.20%

Genes with signal peptides

577

19.94%

Genes with transmembrane helices

737

25.48%

CRISPR repeats

2

 
Table 4.

Number of genes associated with the general COG functional categories

Code

value

%age

Description

J

134

6.6

Translation, ribosomal structure and biogenesis

A

1

0.0

RNA processing and modification

K

81

4.0

Transcription

L

104

5.2

Replication, recombination and repair

B

0

0.0

Chromatin structure and dynamics

D

20

1.0

Cell cycle control, cell division, chromosome partitioning

Y

0

0.0

Nuclear structure

V

44

2.2

Defense mechanisms

T

116

5.8

Signal transduction mechanisms

M

143

7.1

Cell wall/membrane/envelope biogenesis

N

100

5.0

Cell motility

Z

0

0.0

Cytoskeleton

W

0

0.0

Extracellular structures

U

51

2.5

Intracellular trafficking secretion, and vesicular transport

O

62

3.1

Posttranslational modification, protein turnover, chaperones

C

111

5.5

Energy production and conversion

G

143

7.1

Carbohydrate transport and metabolism

E

185

9.2

Amino acid transport and metabolism

F

56

2.8

Nucleotide transport and metabolism

H

67

3.3

Coenzyme transport and metabolism

I

53

2.6

Lipid transport and metabolism

P

99

4.9

Inorganic ion transport and metabolism

Q

20

1.0

Secondary metabolites biosynthesis, transport and catabolism

R

286

14.2

General function prediction only

S

143

7.1

Function unknown

-

1,078

37.3

Not in COGs

Declarations

Acknowledgements

We would like to gratefully acknowledge the help of Sabine Welnitz for growing B. murdochii cells 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, 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.

Authors’ Affiliations

(1)
DOE Joint Genome Institute
(2)
DSMZ - German Collection of Microorganisms and Cell Cultures GmbH
(3)
Bioscience Division, Los Alamos National Laboratory
(4)
Biological Data Management and Technology Center, Lawrence Berkeley National Laboratory
(5)
Oak Ridge National Laboratory
(6)
HZI - Helmholtz Centre for Infection Research
(7)
University of California Davis Genome Center

References

  1. Stanton TB, Fournie-Amazouz E, Postic D, Trott DJ, Grimont PAD, Baranton G, Hampson DJ, Saint Girons I. Recognition of two new species of intestinal spirochetes: Serpulina intermedia sp. nov. and Serpulina murdochii sp. nov. Int J Syst Bacteriol 1997; 47:1007–1012. PubMed doi:10.1099/00207713-47-4-1007View ArticlePubMedGoogle Scholar
  2. Lee JI, Hampson DJ. Genetic characterisation of intestinal spirochaetes and their association with disease. J Med Microbiol 1994; 40:365–371. PubMed doi:10.1099/00222615-40-5-365View ArticlePubMedGoogle Scholar
  3. Hampson DJ, La T. Reclassification of Serpulina intermedia and Serpulina murdochii in the genus Brachyspira as Brachyspira intermedia comb. nov. and Brachyspira murdochii comb. nov. Int J Syst Evol Microbiol 2006; 56:1009–1012. PubMed doi:10.1099/ijs.0.64004-0View ArticlePubMedGoogle Scholar
  4. Euzéby JP. List of bacterial names with standing in nomenclature: A folder available on the Internet. Int J Syst Bacteriol 1997; 47:590–592. PubMed doi:10.1099/00207713-47-2-590View ArticlePubMedGoogle Scholar
  5. Hovind-Hougen K, Birch-Andersen A, Henrik-Nielsen R, Orholm M, Pedersen JO, Teglbjaerg PS, Thaysen EH. Intestinal spirochetosis: morphological characterization and cultivation of the spirochete Brachyspira aalborgi gen. nov., sp. nov. J Clin Microbiol 1982; 16:1127–1136. PubMedPubMed CentralPubMedGoogle Scholar
  6. Stanton TB. 2006. The genus Brachyspira. In M Dworkin, S Falkow, E Rosenberg, KH Schleifer E Stackebrandt (eds), The Prokaryotes, 3. ed, vol. 7. Springer, New York, p. 330–356.View ArticleGoogle Scholar
  7. Paster BJ, Dewhirst FE. Phylogenetic foundation of spirochetes. J Mol Microbiol Biotechnol 2000; 2:341–344. PubMedPubMedGoogle Scholar
  8. Weissenböck H, Maderner A, Herzog AM, Lussy H, Nowotny N. Amplification and sequencing of Brachyspira spp. specific portions of nox using paraffin-embedded tissue samples from clinical colitis in Austrian pigs shows frequent solitary presence of Brachyspira murdochii. Vet Microbiol 2005; 111:67–75. PubMed doi:10.1016/j.vetmic.2005.09.002View ArticlePubMedGoogle Scholar
  9. Stephens CP, Hampson DJ. Prevalence and disease association of intestinal spirochaetes in chickens in eastern Australia. 1999; 28:447–454.Google Scholar
  10. Stephens CP, Oxberry SL, Phillips ND, La T, Hampson DJ. The use of multilocus enzyme electrophoresis to characterise intestinal spirochaetes (Brachyspira spp.) colonising hens in commercial flocks. Vet Microbiol 2005; 107:149–157. PubMed doi:10.1016/j.vetmic.2005.01.011View ArticlePubMedGoogle Scholar
  11. Feberwee A, Hampson DJ, Phillips ND, La T, van der Heijden HMJF, Wellenberg GJ, Dwars RM, Landman WJM. Identification of Brachyspira hyodysenteriae and other pathogenic Brachyspira species in chickens from laying flocks with diarrhea or reduced production or both. J Clin Microbiol 2008; 46:593–600. PubMed doi:10.1128/ICM.01829-07PubMed CentralView ArticlePubMedGoogle Scholar
  12. Rohde J, Rothkamp A, Gerlach GF. Differentiation of porcine Brachyspira species by a novel nox PCR-based restriction fragment length polymorphism analysis. J Clin Microbiol 2002; 40:2598–2600. PubMed doi:10.1128/JCM.40.7.2598-2600.2002PubMed CentralView ArticlePubMedGoogle Scholar
  13. Råsbäck T, Johansson KE, Jansson DS, Fellstrom C, Alikhani MY, La T, Dunn DS, Hampson DJ. Development of a multilocus sequence typing scheme for intestinal spirochaetes within the genus Brachyspira. Microbiology 2007; 153:4074–4087. PubMed doi:10.1099/mic.0.2007/008540-0View ArticlePubMedGoogle Scholar
  14. Bellgard MI, Eanchanthuek P, La T, Ryan K, Moolhuijzen P, Albertyn Z, Shaban B, Motro Y, Dunn DS, Schibeci D, et al. Genome sequence of the pathogenic intestinal spirochaete Brachyspira hyodysenteriae reveals adapations to its lifestyle in the porcine large intestions. PLoS ONE 2009; 4:e4641. PubMed doi:10.1371/journal.pone.0004641PubMed CentralView ArticlePubMedGoogle Scholar
  15. Lee JI, Hampson DJ, Lymbery AJ, Harders SJ. The porcine intestinal spirochaetes: identification of new genetic groups. Vet Microbiol 1993; 34:273–285. PubMed doi:10.1016/0378-1135(93)90017-2View ArticlePubMedGoogle Scholar
  16. Trott DJ, Atyeo RF, Lee JI, Swayne DA, Stoutenbgurg JW, Hampson DJ. Genetic relatedness amongst intestinal spirochaetes isolated from rate and birds. Lett Appl Microbiol 1996; 23:431–436. PubMed doi:10.1111/j.1472-765X.1996.tb01352.xView ArticlePubMedGoogle Scholar
  17. Hampson DJ, Robertson ID, Oxberry SL. Isolation of Serpulina murdochii from the joint fluid of a lame pig. Aust Vet J 1999; 77:48. PubMed doi:10.1111/j.1751-0813.1999.tb12430.xView ArticlePubMedGoogle Scholar
  18. Chun J, Lee JH, Jung Y, Kim M, Kim S, Kim BK, 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. PubMed doi:10.1099/ijs.0.64915-0View ArticlePubMedGoogle Scholar
  19. Levett PN, Morey RE, Galloway R, Steigerwalt AG, Ellis WA. Reclassification of Leptospira parva Hovind-Hougen et al. 1982 as Turneriella parva gen. nov., comb. nov. Int J Syst Evol Microbiol 2005; 55:1497–1499. PubMed doi:10.1099/ijs.0.63088-0View ArticlePubMedGoogle Scholar
  20. Finkbeiner SR, Allred AF, Tarr PI, Klenin EJ, Kirkwood CD, Wang D. Metagenomic analysis of human iarrhea: viral detection and discovery. PLoS Pathog 2008; 4:e1000011. PubMed doi:10.1371/journal.ppat.1000011PubMed CentralView ArticlePubMedGoogle Scholar
  21. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000; 17:540–552. PubMedView ArticlePubMedGoogle Scholar
  22. Lee C, Grasso C, Sharlow MF. Multiple sequence alignment using partial order graphs. Bioinformatics 2002; 18:452–464. PubMed doi:10.1093/bioinformatics/18.3.452View ArticlePubMedGoogle Scholar
  23. Stamatakis A, Hoover P, Rougemont J. A Rapid Bootstrap algorithm for the RAxML web servers. Syst Biol 2008; 57:758–771. PubMed doi:10.1080/10635150802429642View ArticlePubMedGoogle Scholar
  24. Pattengale ND, Alipour M, Bininda-Emonds ORP, Stamatakis A. How many bootstrap replicates are necessary? Lect Notes Comput Sci 2009; 5541:184–200. doi:10.1007/978-3-642-02008-713View ArticleGoogle Scholar
  25. Liolios K, Chen IM, Mavromatis K, Tavernarakis N, Hugenholtz P, Markowitz VM, 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. PubMed doi:10.1093/nar/gkp848PubMed CentralView ArticlePubMedGoogle Scholar
  26. Field D, Garrity G, Gray T, Morrison N, Selengut J, Sterk P, Tatusova T, Thomson N, Allen MJ, Angiuoli SV, et al. The minimum information about a genome sequence (MIGS) specification. Nat Biotechnol 2008; 26:541–547. PubMed doi:10.1038/nbt1360PubMed CentralView ArticlePubMedGoogle Scholar
  27. Woese CR, Kandler O, 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. PubMed doi:10.1073/pnas.87.12.4576PubMed CentralView ArticlePubMedGoogle Scholar
  28. 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 11 — The Bacteria: Phyla “Planctomycetes”, “Chlamydiae”, “Spirochaetes”, “Fibrobacteres”, “Acidobacteria”, “Bacteroidetes”, “Fusobacteria”, “Verrucomicrobia”, “Dictyoglomi”, “Gemmatimonadetes”, and “Lentisphaerae”. http://www.taxonomicoutline.org/index.php/toba/article/viewFile/188/220 2007.
  29. Skerman VBD, McGowan V, Sneath PHA. Approved Lists of Bacterial Names. Int J Syst Bacteriol 1980; 30:225–420. doi:10.1099/00207713-30-1-225View ArticleGoogle Scholar
  30. Buchanan RE. Studies in the nomenclature and classification of Bacteria. II. The primary subdivisions of the Schizomycetes. J Bacteriol 1917; 2:155–164. PubMedPubMed CentralPubMedGoogle Scholar
  31. Paster BJ, Dewhirst FE. Phylogenetic foundation of spirochetes. J Mol Microbiol Biotechnol 2000; 2:341–344. PubMedPubMedGoogle Scholar
  32. Imachi H, Sakai S, Hirayama H, Nakagawa S, Nunoura T, Takai K, Horikoshi K. Exilispira thermophila gen. nov., sp. nov., an anaerobic, thermophilic spirochaete isolated from a deep-sea hydrothermal vent chimney. Int J Syst Evol Microbiol 2008; 58:2258–2265. PubMed doi:10.1099/ijs.0.65727-0View ArticlePubMedGoogle Scholar
  33. Stanton TB, Postic D, Jensen NS. Serpulina alvinipulli sp. nov., a new Serpulina species that is enteropathogenic for chickens. Int J Syst Bacteriol 1998; 48:669–676. PubMed doi:10.1099/00207713-48-3-669View ArticlePubMedGoogle Scholar
  34. Classification of Bacteria and Archaea in risk groups. www.baua.de TRBA 466.
  35. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, et al. Gene Ontology: tool for the unification of biology. Nat Genet 2000; 25:25–29. PubMed doi:10.1038/75556PubMed CentralView ArticlePubMedGoogle Scholar
  36. Karlsson M, Fellstrom C, Gunnarsson A, Landen A, Franklin A. Antimicrobial susceptibility testing of porcine brachyspira (Serpulina) species isolates. J Clin Microbiol 2003; 41:2596–2604. PubMed doi:10.1128/JCM.41.6.2596-2604.2003PubMed CentralView ArticlePubMedGoogle Scholar
  37. Råsbäck T, Fellström C, Bergsjø B, Cizek A, Collin K, Gunnarsson A, Jensen SM, Mars A, Thomson J, Vyt P, et al. Assessment of diagnostics and antimicrobial susceptibility testing of Brachyspira species using a ring test. Vet Microbiol 2005; 109:229–243. PubMed doi:10.1016/j.vetmic.2005.05.009View ArticlePubMedGoogle Scholar
  38. Matthews HM, Kinyon JM. Cellular lipid comparisons between strains of Treponema hyodysenteriae and Treponema innocens. Int J Syst Bacteriol 1984; 34:160–165. doi:10.1099/00207713-34-2-160View ArticleGoogle Scholar
  39. Klenk HP, Göker M. En route to a genome-based classification of Archaea and Bacteria? Syst Appl Microbiol (In press).Google Scholar
  40. Wu D, Hugenholtz P, Mavromatis K, Pukall R, Dalin E, Ivanova NN, Kunin V, Goodwin L, Wu M, Tindall BJ, et al. A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature 2009; 462:1056–1060. PubMed doi:10.1038/nature08656PubMed CentralView ArticlePubMedGoogle Scholar
  41. List of growth media used at DSMZ: http://www.dsmz.de/microorganisms/media_list.php
  42. Sims D, Brettin T, Detter J, Han C, Lapidus A, Copeland A, Glavina Del Rio T, Nolan M, Chen F, Lucas S, et al. Complete genome sequence of Kytococcus sedentarius type strain (541T). Stand Genomic Sci 2009; 1:12–20. doi:10.4056/sigs.761PubMed CentralView ArticlePubMedGoogle Scholar
  43. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal Prokaryotic Dynamic Programming Genefinding Algorithm. BMC Bioinformatics 2010; 11:119. PubMed doi:10.1186/1471-2105-11-119PubMed CentralView ArticlePubMedGoogle Scholar
  44. Pati A, Ivanova N, Mikhailova N, Ovchinikova G, Hooper SD, Lykidis A, Kyrpides NC. GenePRIMP: A Gene Prediction Improvement Pipeline for microbial genomes. Nat Methods (Epub). doi:10.1038/nmeth.1457Google Scholar
  45. Markowitz VM, Ivanova NN, Chen IMA, Chu K, Kyrpides NC. IMG ER: a system for microbial genome annotation expert review and curation. Bioinformatics 2009; 25:2271–2278. PubMed doi:10.1093/bioinformatics/btp393View ArticlePubMedGoogle Scholar

Copyright

© The Author(s) 2010