Open Access

Genome sequence of the moderately halophilic bacterium Salinicoccus carnicancri type strain CrmT (= DSM 23852T)

  • Dong-Wook Hyun
  • , Tae Woong Whon
  • , Yong-Joon Cho
  • , Jongsik Chun
  • , Min-Soo Kim
  • , Mi-Ja Jung
  • , Na-Ri Shin
  • , Joon-Yong Kim
  • , Pil Soo Kim
  • , Ji-Hyun Yun
  • , Jina Lee
  • , Sei Joon Oh
  • and Jin-Woo Bae
Corresponding author

DOI: 10.4056/sigs.3967649

Received: 03 June 2013

Accepted: 03 June 2013

Published: 15 June 2013

Abstract

Salinicoccus carnicancri Jung et al. 2010 belongs to the genus Salinicoccus in the family Staphylococcaceae. Members of the Salinicoccus are moderately halophilic and originate from various salty environments. The halophilic features of the Salinicoccus suggest their possible uses in biotechnological applications, such as biodegradation and fermented food production. However, the genus Salinicoccus is poorly characterized at the genome level, despite its potential importance. This study presents the draft genome sequence of S. carnicancri strain CrmT and its annotation. The 2,673,309 base pair genome contained 2,700 protein-coding genes and 78 RNA genes with an average G+C content of 47.93 mol%. It was notable that the strain carried 72 predicted genes associated with osmoregulation, which suggests the presence of beneficial functions that facilitate growth in high-salt environments.

Keywords:

moderately halophilicSalinicoccus carnicancriStaphylococcaceae

Introduction

The genus Salinicoccus in the family Staphylococcaceae was first proposed by Ventosa et al. (1990) and is defined as moderately halophilic, aerobic, Gram-positive, non-motile, non-sporulating, and heterotrophic cocci [1]. The genus name is derived from the Latin adjective salinus, saline, and the Greek masculine noun kokkos, meaning a grain or berry, i.e., saline coccus [2]. Most species in the genus Salinicoccus have been found in salty environments, such as fermented foods [3-5], solar salterns [1,6], salt mines [7,8], a salt lake [9], and saline soils [10,11]. All type strains of Salinicoccus species were characterized as halotolerant organisms, where NaCl concentrations of 2–20% (wt/vol) were suitable for growth [12-14].

These moderately halophilic bacteria can survive in salt-rich environments and grow optimally at 5–20% (wt/vol) NaCl [15]. These bacteria can utilize compatible solutes or osmolytes, such as carbohydrates, amino acid, polyols, betaines, and ectoines, by regulating their osmotic concentrations in high-salt content environmental conditions [16,17]. Therefore, these organisms may have biotechnological importance with possible applications in food biotechnology for the production of fermented food [18], in environmental biotechnology for the biodegradation of organic pollutants and the production of alternative energy [19].

Strain CrmT (= DSM 23852 = JCM 15796 = KCTC 13301) is the type strain of the species Salinicoccus carnicancri. This strain was isolated from a traditional Korean fermented seafood, known as ‘ganjang-gejang,’ which is made from raw crabs preserved in soy sauce [20]. The species name was derived from the Latin nouns caro carnis, flesh, and cancer -cri, a crab, i.e., the flesh of a crab [2]. The strain can grow in 0–20% (wt/vol) NaCl with optimal growth at 12% (wt/vol) NaCl [20]. The present study summarizes the features of S. carnicancri strain CrmT and provides an analysis of its draft genome sequence, which is the first reported genome sequence of a species in the genus Salinicoccus.

Classification and features

A taxonomic analysis was conducted based on the 16S rRNA gene sequence. The representative 16S rRNA gene sequence of strain S. carnicancri CrmT was compared with the most recent release of the EzTaxon-e database [21]. The multiple sequence alignment program CLUSTAL W [22] was used to generate alignments with other gene sequences collected from databases. The alignments were trimmed and converted to the MEGA format before phylogenetic analysis. Phylogenetic consensus trees were constructed based on the aligned gene sequences using the neighbor-joining [23], maximum-parsimony [24], and maximum-likelihood [25] methods with 1,000 randomly selected bootstrap replicates using MEGA version 5 [26]. The phylogenetic analysis based on the 16S rRNA gene sequence showed that strain CrmT was most closely related to Salinicoccus halodurans W24T with 96.99% similarity. The phylogenetic consensus tree based on the 16S rRNA gene sequences indicated that strain CrmT was clustered within a branch containing other species in the genus Salinicoccus (Figure 1).

Figure 1

Phylogenetic consensus tree based on 16S rRNA gene sequences showing the relationship between Salinicoccus carnicancri strain CrmT and the type strains of other species in the genus Salinicoccus. The type strain of Staphylococcus aureus was used as an outgroup. The GenBank accession numbers for the 16S rRNA genes of each strain are shown in parentheses. Filled diamonds indicate identical branches present in the phylogenetic consensus trees constructed using the neighbor-joining (NJ), maximum-parsimony (MP), and maximum-likelihood (ML) algorithms. The numbers at the nodes represent the bootstrap values as percentages of 1,000 replicates and values <70% are not shown at the branch points. The scale bar represents 0.01 nucleotide change per nucleotide position.

Strain CrmT (Table 1) was isolated from the fermented seafood ganjang-gejang during a project that investigated microbial communities in fermented foods, i.e., the Next-Generation BioGreen 21 Program (No. PJ008208) in Korea. Ganjang-gejang, with a NaCl (w/v) concentration of 24.5%, was produced by preserving scabbard crabs in soy sauce, garlic, and onions at –5°C for 4–5 days.

Table 1

Classification and general features of Salinicoccus carnicancri strain CrmT according to the MIGS recommendations [27].

MIGS ID

   Property

    Term

   Evidence code

    Domain Bacteria

   TAS [28]

    Phylum Firmicutes

   TAS [29-31]

    Class Bacilli

   TAS [32,33]

   Current classification

    Order Bacillales

   TAS [34,35]

    Family Staphylococcaceae

   TAS [36,37]

    Genus Salinicoccus

   TAS [1,38]

    Species Salinicoccus carnicancri

   TAS [20]

    Type strain CrmT

   TAS [20]

   Gram stain

    Positive

   TAS [20]

   Cell shape

    Cocci

   TAS [20]

   Motility

    Non-motile

   TAS [20]

   Sporulation

    Non-sporulating

   TAS [20]

   Temperature range

    4–45°C

   TAS [20]

   Optimum temperature

    30–37°C

   TAS [20]

   Salinity range

    0–20% (w/v)

   TAS [20]

   Optimum salinity

    12% (w/v)

   TAS [20]

   pH range

    6–11

   TAS [20]

   Optimum pH

    7–8

   TAS [20]

   Carbon source

    Heterotroph

   TAS [20]

   Energy source

    Not reported

MIGS-6

   Habitat

    Fermented seafood (marinated crab)

   TAS [20]

MIGS-6.1

   Temperature

    –5 to 5°C

   IDA

MIGS-6.3

   Salinity

    20%

   IDA

MIGS-22

   Oxygen

    Aerobic

   TAS [20]

MIGS-15

   Biotic relationship

    Free-living

   TAS [20]

MIGS-14

   Pathogenicity

    Unknown

   Biosafety level

    1

MIGS-23.1

   Isolation

    The traditional Korean fermented seafood ‘ganjang-gejang’ (Crabs preserved in soy sauce)

   TAS [20]

MIGS-4

   Geographic location

    Republic of Korea

   TAS [20]

MIGS-5

   Sample collection time

    August, 2010

   NAS

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, as follows: IDA: inferred from direct assay; TAS: traceable author statement (i.e., a direct report exists in the literature); NAS: non-traceable author statement (i.e., not observed directly in a living, isolated sample, but based on a generally accepted property of the species, or anecdotal evidence). These evidence codes are from the Gene Ontology project [39].

S. carnicancri strain CrmT is a Gram-positive, moderately halophilic, non-motile, non-sporulating, and aerobic heterotrophic coccus with a diameter of 1.0–2.5 μm [20]. Figure 2 shows the morphological features of strain CrmT, which were obtained by scanning electron microscopy (SEM). Colonies were ivory-colored [20]. Growth occurred at 4–45°C, with an optimum of 30–37°C, and at pH values of 6.0–11.0, with an optimum of 7.0–8.0. The salinity range suitable for growth was 0–20% (w/v) NaCl, with an optimum of 12% (w/v) NaCl [20]. Strain CrmT contains menaquinone MK-6 as the predominant respiratory quinone [20]. The major fatty acids (>10% of total fatty acid) are anteiso-C15:0 (40.61%), iso-C15:0 (22.0%), and anteiso-C17:0 (12.12%) [20]. The major cellular polar lipids are phosphatidylglycerol and diphosphatidylglycerol [20]. Glycine and lysine are the major amino acid constituents of the cell-wall hydrolysate [20].

Figure 2

Scanning electron microscopy images of S. carnicancri CrmT obtained using a SUPRA VP55 (Carl Zeiss) at an operating voltage of 15kV. The scale bars represents 200 nm (left) and 1 μm (right), respectively.

Genome sequencing and annotation

Genome project history

S. carnicancri strain CrmT was selected for sequencing because of its environmental potential as part of the Next-Generation BioGreen 21 Program (No.PJ008208). The genome project is deposited in the Genomes OnLine Database [40] and the genome sequence is deposited in GenBank. Sequencing and annotation were performed by ChunLab Inc., South Korea. 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

    Improved high-quality draft

MIGS-28

    Libraries used

    454 PE library (8 kb insert size) and Illumina library

MIGS-28.2

    Number of reads

    7,434,400 sequencing reads

MIGS-29

    Sequencing platforms

    454 GS FLX Titanium, Illumina Hiseq, and PacBio RS system

MIGS-31.2

    Sequencing coverage

    443.60-fold coverage (12.1 × 454 pyrosequencing, 408.4 × Illumina, and 23.1 × PacBio)

MIGS-30

    Assemblers

    gsAssembler 2.6, CLC Genomics Workbench 5.0

MIGS-32

    Gene calling method

    GLIMMER 3.02

    Genbank ID

    ANAM01000000

    Genbank Date of Release

    January 2, 2013

    GOLD ID

    Gi21266

    NCBI project ID

    175941

    Database: IMG-ER

    2521172676

    Source material identifier

    DSM 23852, JCM 15796, KCTC 13301

    Project relevance

    Environmental and biotechnological

Growth conditions and DNA isolation

S. carnicancri strain CrmT was grown aerobically in marine 2216 (Marine medium, BBL), supplemented with 10% (w/v) NaCl at 30°C. Genomic DNA was extracted using a Wizard Genomic DNA Purification Kit (Promega A1120), according to the manufacturer’s instructions.

Genome sequencing and assembly

The genome of S. carnicancri CrmT was sequenced using a combination of a 454 Genome Sequencer FLX Titanium system (Roche Diagnostics) with an 8 kb paired end library, an Illumina Hiseq system with a 150 base pair (bp) paired end library, and a PacBio RS system (Pacific Biosciences). A total of 7,434,400 sequencing reads (443.6-fold genome coverage) were obtained using the Roche 454 system (187,030 reads; 12.1-fold coverage), Ilumina Hiseq system (7,219,019 reads; 408.4-fold coverage), and PacBio RS system (28,351 reads; 23.1-fold coverage) combined. The Roche 454 pyrosequencing and Illumina sequencing reads were assembled using Roche gsAssembler 2.6 (Roche Diagnostics) and CLCbio CLC Genomics Workbench 5.0 (CLCbio), respectively. Table 2 shows the project information and its associated MIGS version 2.0 compliance levels [27].

Genome annotation

The open reading frames (ORFs) of the assembled genome were predicted using a combination of the Rapid Annotation using Subsystem Technology (RAST) pipeline [41] and the GLIMMER 3.02 modeling software package [42]. Comparisons of the predicted ORFs using the SEED [43], NCBI COG [44], NCBI Refseq [45], CatFam [46], Ez-Taxon-e [21], and Pfam [47] databases were conducted during gene annotation. RNAmmer 1.2 [48] and tRNAscan-SE 1.23 [49] were used to find rRNA genes and tRNA genes, respectively. Additional gene prediction analyses and functional annotation were performed using the Integrated Microbial Genomes - Expert Review (IMG-ER) platform [50].

Genome properties

The draft genome sequence of S. carnicancri CrmT was 2,673,309 bp, which comprised three scaffolds that included 12 contigs. The G+C content was 47.93 mol% (Figure 3 and Table 3). RAST and GLIMMER predicted 2,778 coding sequences (CDSs) in the genome. Of the predicted ORFs, 2,700 ORFs were assigned to protein-coding genes. A total of 2,298 genes (82.72%) were assigned putative functions, whereas the remaining genes were annotated as hypothetical proteins. The genome contained 78 ORFs assigned to RNA genes, including 61 predicted tRNA genes, nine rRNA genes (three 5S rRNA, three 16S rRNA, and three 23S rRNA genes), and eight other RNA genes. The distributions of genes in the COG functional categories are presented in Table 4.

Figure 3

Graphical map of the largest scaffold, C792_Scaffold00001.1, which represented >99.6% of the chromosome. The smaller scaffolds of the chromosome are not shown. From bottom to top: genes on the forward strand (colored according to COG categories), genes on the reverse strand (colored according to COG categories), RNA genes (tRNAs = green, rRNAs = red, and other RNAs = black), GC content, and GC skew.

Table 3

Genome statistics.

Attribute

      Value

     % of totala

Genome size (bp)

      2,673,309

     100.00%

DNA coding region (bp)

      2,420,461

     90.54%

DNA G+C content (bp)

      1,279,282

     47.93%

Total genes

      2,778

     100%

RNA genes

      78

     2.81%

rRNA operons

      9

     0.32%

Protein-coding genes

      2,700

     97.19%

Genes with predicted functions

      2,298

     82.72%

Genes in paralog clusters

      1,850

     66.59%

Genes assigned to COGs

      2,255

     81.17%

Genes assigned Pfam domains

      2,333

     83.98%

Genes with signal peptides

      437

     15.73%

Genes with transmembrane helices

      679

     24.44%

CRISPR repeats

      1

aThe total is based on either the size of the genome (bp) or the total number of protein-coding genes in the annotated genome.

Table 4

Numbers of genes associated with the 25 general COG functional categories.

Code

   Value

   %agea

    Description

J

   152

   5.6

    Translation

A

   0

   0.0

    RNA processing and modification

K

   194

   7.2

    Transcription

L

   120

   4.4

    Replication, recombination, and repair

B

   1

   0.0

    Chromatin structure and dynamics

D

   27

   1.0

    Cell cycle control, mitosis, and meiosis

Y

   0

   0.0

    Nuclear structure

V

   38

   1.4

    Defense mechanisms

T

   75

   2.8

    Signal transduction mechanisms

M

   126

   4.7

    Cell-wall/membrane biogenesis

N

   6

   0.2

    Cell motility

Z

   0

   0.0

    Cytoskeleton

W

   0

   0.0

    Extracellular structures

U

   35

   1.3

    Intracellular trafficking and secretion

O

   71

   2.6

    Posttranslational modification, protein turnover, and chaperones

C

   148

   5.5

    Energy production and conversion

G

   189

   7.0

    Carbohydrate transport and metabolism

E

   241

   8.9

    Amino acid transport and metabolism

F

   77

   2.9

    Nucleotide transport and metabolism

H

   120

   4.4

    Coenzyme transport and metabolism

I

   83

   3.1

    Lipid transport and metabolism

P

   152

   5.6

    Inorganic ion transport and metabolism

Q

   53

   2.0

    Secondary metabolites biosynthesis, transport, and catabolism

R

   346

   12.8

    General function prediction only

S

   215

   8.0

    Function unknown

-

   231

   8.6

    Not in COGs

aThe total is based on the total number of protein-coding genes in the annotated genome.

Insights from the genome sequence

S. carnicancri CrmT encoded 72 predicted genes associated with the biosynthesis of compatible solutes and the transport of osmolytes, such as choline-glycine betaine transporter (BetT) and periplasmic glycine betaine/choline-binding lipoprotein of an ABC-type transport system (OpuBC). Potentially, these genes are key factors that allow S. carnicancri to adapt to high-salt environments (e.g., salt-fermented food) by regulating the osmotic concentration. Further studies are required to elucidate the osmoregulation mechanism, which could facilitate biotechnological applications of this halophilic bacterium.

Declarations

Acknowledgements

We gratefully acknowledge the help of Dr. Seong Woon Roh and Mr. Hae-Won Lee during SEM analysis (Jeju Center, Korea Basic Science Institute, Korea). This work was supported by a grant from the Next-Generation BioGreen 21 Program (No.PJ008208), Rural Development Administration, Republic of Korea.


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References

  1. Ventosa AM, Ruizberraquero MC and Kocur F. M. Salinicoccus roseus gen. nov, sp. nov, a new moderately halophilic gram-positive coccus. Syst Appl Microbiol. 1990; 13:29-33 View Article
  2. Euzeby JP. List of Bacterial Names with Standing in Nomenclature: a folder available on the Internet. Int J Syst Bacteriol. 1997; 47:590-592 View ArticlePubMed
  3. França L, Rainey FA, Nobre MF and da Costa MS. Salinicoccus salsiraiae sp. nov.: a new moderately halophilic gram-positive bacterium isolated from salted skate. Extremophiles. 2006; 10:531-536 View ArticlePubMed
  4. Aslam Z, Lim JH, Im WT, Yasir M, Chung YR and Lee ST. Salinicoccus jeotgali sp. nov., isolated from jeotgal, a traditional Korean fermented seafood. Int J Syst Evol Microbiol. 2007; 57:633-638 View ArticlePubMed
  5. Pakdeeto A, Tanasupawat S, Thawai C, Moonmangmee S, Kudo T and Itoh T. Salinicoccus siamensis sp. nov., isolated from fermented shrimp paste in Thailand. Int J Syst Evol Microbiol. 2007; 57:2004-2008 View ArticlePubMed
  6. Ventosa A, Marquez MC, Weiss N and Tindall BJ. Transfer of Marinococcus hispanicus to the genus Salinicoccus as Salinicoccus hispanicus comb. Nov. Syst Appl Microbiol. 1992; 15:530-534 View Article
  7. Chen YG, Cui XL, Pukall R, Li HM, Yang YL, Xu LH, Wen ML, Peng Q and Jiang CL. Salinicoccus kunmingensis sp. nov., a moderately halophilic bacterium isolated from a salt mine in Yunnan, south-west China. Int J Syst Evol Microbiol. 2007; 57:2327-2332 View ArticlePubMed
  8. Chen YG, Cui XL, Wang YX, Zhang YQ, Li QY, Liu ZX, Wen ML, Peng Q and Li WJ. Salinicoccus albus sp. nov., a halophilic bacterium from a salt mine. Int J Syst Evol Microbiol. 2009; 59:874-879 View ArticlePubMed
  9. Gao M, Wang L, Chen SF, Zhou YG and Liu HC. Salinicoccus kekensis sp. nov., a novel alkaliphile and moderate halophile isolated from Keke Salt Lake in Qinghai, China. Anton Leeuw Int J G. 2010; 98:351-357 View ArticlePubMed
  10. Wang X, Xue Y, Yuan S, Zhou C and Ma Y. Salinicoccus halodurans sp. nov., a moderate halophile from saline soil in China. Int J Syst Evol Microbiol. 2008; 58:1537-1541 View ArticlePubMed
  11. Chen YG, Cui XL, Li WJ, Xu LH, Wen ML, Peng Q and Jiang CL. Salinicoccus salitudinis sp. nov., a new moderately halophilic bacterium isolated from a saline soil sample. Extremophiles. 2008; 12:197-203 View ArticlePubMed
  12. Kampfer P, Arun AB, Busse HJ, Young CC, Lai WA, Rekha PD and Chen WM. Salinicoccus sesuvii sp. nov., isolated from the rhizosphere of Sesuvium portulacastrum. Int J Syst Evol Microbiol. 2011; 61:2348-2352 View ArticlePubMed
  13. Qu Z, Li Z, Zhang X and Zhang XH. Salinicoccus qingdaonensis sp. nov., isolated from coastal seawater during a bloom of green algae. Int J Syst Evol Microbiol. 2012; 62:545-549 View ArticlePubMed
  14. Ramana CV, Srinivas A, Subhash Y, Tushar L, Mukherjee T, Kiran PU, Sasikala C. Salinicoccus halitifaciens sp. nov., a novel bacterium participating in halite formation. Anton Leeuw Int J G 2013.
  15. DasSarma SAP. Halophiles. In Encyclopedia of Life Sciences, Nature Publishing Group 2002;Volume 8:458-466.
  16. Galinski EA. Compatible Solutes of Halophilic Eubacteria - Molecular Principles, Water-Solute Interaction, Stress Protection. Experientia. 1993; 49:487-496 View Article
  17. Roberts MF. Organic compatible solutes of halotolerant and halophilic microorganisms. Saline Syst. 2005; 1:5 View ArticlePubMed
  18. Margesin R and Schinner F. Potential of halotolerant and halophilic microorganisms for biotechnology. Extremophiles. 2001; 5:73-83 View ArticlePubMed
  19. Le Borgne S, Paniagua D and Vazquez-Duhalt R. Biodegradation of organic pollutants by halophilic bacteria and archaea. J Mol Microbiol Biotechnol. 2008; 15:74-92 View ArticlePubMed
  20. Jung MJ, Kim MS, Roh SW, Shin KS and Bae JW. Salinicoccus carnicancri sp. nov., a halophilic bacterium isolated from a Korean fermented seafood. Int J Syst Evol Microbiol. 2010; 60:653-658 View ArticlePubMed
  21. Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH and Yi H. Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol. 2012; 62:716-721 View ArticlePubMed
  22. Thompson JD, Higgins DG and Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994; 22:4673-4680 View ArticlePubMed
  23. Saitou N and Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987; 4:406-425PubMed
  24. Kluge AGFF. Quantitative phyletics and the evolution of anurans. Syst Zool. 1969; 18:1-32 View Article
  25. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol. 1981; 17:368-376 View ArticlePubMed
  26. Tamura K, Peterson D, Peterson N, Stecher G, Nei M and Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011; 28:2731-2739 View ArticlePubMed
  27. 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
  28. 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
  29. Gibbons NEMR. Proposals concerning the higher taxa of bacteria. Int J Syst Bacteriol. 1978; 28:1-6 View Article
  30. 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.
  31. Murray RGE. The Higher Taxa, or, a Place for Everything...? In: Holt JG (ed), Bergey's Manual of Systematic Bacteriology, First Edition, Volume 1, The Williams and Wilkins Co., Baltimore, 1984, p. 31-34.
  32. Ludwig WSK, Whitman WB. Class I. Bacilli class nov. In: De Vos P, Garrity G, Jones D, Krieg NR, Ludwig W, Rainey FA, Schleifer KH, Whitman WB (eds). Bergey's Manual of Systematic Bacteriology, Second Edition, Volume 3, Springer-Verlag, New York 2009:p. 19-20.
  33. List of new names and new combinations previously effectively, but not validly, pub-lished. List no. 132. Int J Syst Evol Microbiol. 2010; 60:469 View Article
  34. Prévot AR. Dictionnaire des Bactéries Pathogènes. In Hauduroy, Ehringer, Guillot, Magrou, Prévot, Rossetti and Urbain (eds) 2nd edition. Masson, Paris, 1953:1-692.
  35. Skerman VBDMV. Sneath PHA Approved Lists of Bacterial Names. Int J Syst Bacteriol. 1980; 30:225-420 View Article
  36. . List of new names and new combinations previously effectively, but not validly, published. List no. 132. Int J Syst Evol Microbiol. 2010; 60:469-472 View Article
  37. Schleifer KH, Bell JA. Family VIII. Staphylococcaceae fam. nov. In: De Vos P, Garrity G, Jones D, Krieg NR, Ludwig W, Rainey FA, Schleifer KH, Whitman WB (eds), Bergey's Manual of Systematic Bacteriology, Second Edition, Volume 3, Springer-Verlag, New York, 2009, p. 392.
  38. . Validation List no. 34. Validation of the publication of new names and new combinations previously effectively published outside the IJSB. Int J Syst Bacteriol. 1990; 40:320-321 View Article
  39. 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 View ArticlePubMed
  40. 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
  41. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM and Kubal M. The RAST Server: rapid annotations using subsystems technology. BMC Genomics. 2008; 9:75 View ArticlePubMed
  42. Delcher AL, Bratke KA, Powers EC and Salzberg SL. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics. 2007; 23:673-679 View ArticlePubMed
  43. Overbeek R, Begley T, Butler RM, Choudhuri JV, Chuang HY, Cohoon M, de Crecy-Lagard V, Diaz N, Disz T and Edwards R. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res. 2005; 33:5691-5702 View ArticlePubMed
  44. Tatusov RL, Galperin MY, Natale DA and Koonin EV. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res. 2000; 28:33-36 View ArticlePubMed
  45. Pruitt KD, Tatusova T, Brown GR and Maglott DR. NCBI Reference Sequences (RefSeq): current status, new features and genome annotation policy. Nucleic Acids Res. 2012; 40:D130-D135 View ArticlePubMed
  46. Yu C, Zavaljevski N, Desai V and Reifman J. Genome-wide enzyme annotation with precision control: catalytic families (CatFam) databases. Proteins. 2009; 74:449-460 View ArticlePubMed
  47. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G and Forslund K. The Pfam protein families database. Nucleic Acids Res. 2010; 38:D211-D222 View ArticlePubMed
  48. Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T and Ussery DW. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 2007; 35:3100-3108 View ArticlePubMed
  49. Lowe TM and Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 1997; 25:955-964PubMed
  50. Markowitz VM, Mavromatis K, Ivanova NN, Chen IM, Chu K and Kyrpides NC. IMG ER: a system for microbial genome annotation expert review and curation. Bioinformatics. 2009; 25:2271-2278 View ArticlePubMed