Open Access

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

  • Dong-Wook Hyun1,
  • Tae Woong Whon1,
  • Yong-Joon Cho2,
  • Jongsik Chun2,
  • Min-Soo Kim1,
  • Mi-Ja Jung1,
  • Na-Ri Shin1,
  • Joon-Yong Kim1,
  • Pil Soo Kim1,
  • Ji-Hyun Yun1,
  • Jina Lee1,
  • Sei Joon Oh1 and
  • Jin-Woo Bae1Email author
Standards in Genomic Sciences20138:8020255

Published: 15 June 2013


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.


moderately halophilic Salinicoccus carnicancri Staphylococcaceae


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 [35], 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 [1214].

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].




Evidence code


Current classification

Domain Bacteria

TAS [28]


Phylum Firmicutes

TAS [2931]


Class Bacilli

TAS [32,33]


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


TAS [20]


Cell shape


TAS [20]




TAS [20]




TAS [20]


Temperature range


TAS [20]


Optimum temperature


TAS [20]


Salinity range

0–20% (w/v)

TAS [20]


Optimum salinity

12% (w/v)

TAS [20]


pH range


TAS [20]


Optimum pH


TAS [20]


Carbon source


TAS [20]


Energy source

Not reported




Fermented seafood (marinated crab)

TAS [20]



−5 to 5°C









TAS [20]


Biotic relationship


TAS [20]





Biosafety level





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

TAS [20]


Geographic location

Republic of Korea

TAS [20]


Sample collection time

August, 2010




Not reported




Not reported




Not reported




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.





Finishing quality

Improved high-quality draft


Libraries used

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


Number of reads

7,434,400 sequencing reads


Sequencing platforms

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


Sequencing coverage

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



gsAssembler 2.6, CLC Genomics Workbench 5.0


Gene calling method



Genbank ID



Genbank Date of Release

January 2, 2013





NCBI project ID



Database: IMG-ER



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.



% of totala

Genome size (bp)



DNA coding region (bp)



DNA G+C content (bp)



Total genes



RNA genes



rRNA operons



Protein-coding genes



Genes with predicted functions



Genes in paralog clusters



Genes assigned to COGs



Genes assigned Pfam domains



Genes with signal peptides



Genes with transmembrane helices



CRISPR repeats



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.












RNA processing and modification








Replication, recombination, and repair




Chromatin structure and dynamics




Cell cycle control, mitosis, and meiosis




Nuclear structure




Defense mechanisms




Signal transduction mechanisms




Cell-wall/membrane biogenesis




Cell motility








Extracellular structures




Intracellular trafficking and secretion




Posttranslational modification, protein turnover, and chaperones




Energy production and conversion




Carbohydrate transport and metabolism




Amino acid transport and metabolism




Nucleotide transport and metabolism




Coenzyme transport and metabolism




Lipid transport and metabolism




Inorganic ion transport and metabolism




Secondary metabolites biosynthesis, transport, and catabolism




General function prediction only




Function unknown




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.



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.

Authors’ Affiliations

Department of Life and Nanopharmaceutical Sciences and Department of Biology, Kyung Hee University
ChunLab, Inc., Seoul National University


  1. Ventosa AM, Ruizberraquero MC, Kocur F.M. Salinicoccus roseus gen. nov, sp. nov, a new moderately halophilic gram-positive coccus. Syst Appl Microbiol 1990; 13:29–33. ArticleGoogle Scholar
  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. PubMed ArticlePubMedGoogle Scholar
  3. França L, Rainey FA, Nobre MF, da Costa MS. Salinicoccus salsiraiae sp. nov.: a new moderately halophilic gram-positive bacterium isolated from salted skate. Extremophiles 2006; 10:531–536. PubMed ArticlePubMedGoogle Scholar
  4. Aslam Z, Lim JH, Im WT, Yasir M, Chung YR, Lee ST. Salinicoccus jeotgali sp. nov., isolated from jeotgal, a traditional Korean fermented seafood. Int J Syst Evol Microbiol 2007; 57:633–638. PubMed ArticlePubMedGoogle Scholar
  5. Pakdeeto A, Tanasupawat S, Thawai C, Moonmangmee S, Kudo T, Itoh T. Salinicoccus siamensis sp. nov., isolated from fermented shrimp paste in Thailand. Int J Syst Evol Microbiol 2007; 57:2004–2008. PubMed ArticlePubMedGoogle Scholar
  6. Ventosa A, Marquez MC, Weiss N, Tindall BJ. Transfer of Marinococcus hispanicus to the genus Salinicoccus as Salinicoccus hispanicus comb. nov. Syst Appl Microbiol 1992; 15:530–534. ArticleGoogle Scholar
  7. Chen YG, Cui XL, Pukall R, Li HM, Yang YL, Xu LH, Wen ML, Peng Q, 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. PubMed ArticlePubMedGoogle Scholar
  8. Chen YG, Cui XL, Wang YX, Zhang YQ, Li QY, Liu ZX, Wen ML, Peng Q, Li WJ. Salinicoccus albus sp. nov., a halophilic bacterium from a salt mine. Int J Syst Evol Microbiol 2009; 59:874–879. PubMed ArticlePubMedGoogle Scholar
  9. Gao M, Wang L, Chen SF, Zhou YG, 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. PubMed ArticleGoogle Scholar
  10. Wang X, Xue Y, Yuan S, Zhou C, Ma Y. Salinicoccus halodurans sp. nov., a moderate halophile from saline soil in China. Int J Syst Evol Microbiol 2008; 58:1537–1541. PubMed ArticlePubMedGoogle Scholar
  11. Chen YG, Cui XL, Li WJ, Xu LH, Wen ML, Peng Q, Jiang CL. Salinicoccus salitudinis sp. nov., a new moderately halophilic bacterium isolated from a saline soil sample. Extremophiles 2008; 12:197–203. PubMed ArticlePubMedGoogle Scholar
  12. Kampfer P, Arun AB, Busse HJ, Young CC, Lai WA, Rekha PD, Chen WM. Salinicoccus sesuvii sp. nov., isolated from the rhizosphere of Sesuvium portulacastrum. Int J Syst Evol Microbiol 2011; 61:2348–2352. PubMed ArticlePubMedGoogle Scholar
  13. Qu Z, Li Z, Zhang X, 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. PubMed ArticlePubMedGoogle Scholar
  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.Google Scholar
  15. DasSarma SAP. Halophiles. In Encyclopedia of Life Sciences, Nature Publishing Group 2002;Volume 8:458–466.Google Scholar
  16. Galinski EA. Compatible Solutes of Halophilic Eubacteria — Molecular Principles, Water-Solute Interaction, Stress Protection. Experientia 1993; 49:487–496. ArticleGoogle Scholar
  17. Roberts MF. Organic compatible solutes of halotolerant and halophilic microorganisms. Saline Syst 2005; 1:5. PubMed CentralView ArticlePubMedGoogle Scholar
  18. Margesin R, Schinner F. Potential of halotolerant and halophilic microorganisms for biotechnology. Extremophiles 2001; 5:73–83. PubMed ArticlePubMedGoogle Scholar
  19. Le Borgne S, Paniagua D, Vazquez-Duhalt R. Biodegradation of organic pollutants by halophilic bacteria and archaea. J Mol Microbiol Biotechnol 2008; 15:74–92. PubMed ArticlePubMedGoogle Scholar
  20. Jung MJ, Kim MS, Roh SW, Shin KS, Bae JW. Salinicoccus carnicancri sp. nov., a halophilic bacterium isolated from a Korean fermented seafood. Int J Syst Evol Microbiol 2010; 60:653–658. PubMed ArticlePubMedGoogle Scholar
  21. Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, Yi H, et al. 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. PubMed ArticlePubMedGoogle Scholar
  22. Thompson JD, Higgins DG, 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. PubMed CentralView ArticlePubMedGoogle Scholar
  23. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425. PubMedPubMedGoogle Scholar
  24. Kluge AGFF. Quantitative phyletics and the evolution of anurans. Syst Zool 1969; 18:1–32. ArticleGoogle Scholar
  25. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981; 17:368–376. PubMed ArticlePubMedGoogle Scholar
  26. 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; 28:2731–2739. PubMed CentralView ArticlePubMedGoogle Scholar
  27. 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 CentralView ArticlePubMedGoogle Scholar
  28. 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 CentralView ArticlePubMedGoogle Scholar
  29. Gibbons NEMR. Proposals concerning the higher taxa of bacteria. Int J Syst Bacteriol 1978; 28:1–6. ArticleGoogle Scholar
  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.View ArticleGoogle Scholar
  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.Google Scholar
  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.Google Scholar
  33. List of new names and new combinations previously effectively, but not validly, published. List no. 132. Int J Syst Evol Microbiol 2010; 60:469.
  34. Prévot AR. Dictionnaire des Bactéries Pathogènes. In Hauduroy, Ehringer, Guillot, Magrou, Prévot, Rossetti and Urbain (eds) 2nd edition. Masson, Paris, 1953:1–692.Google Scholar
  35. Skerman VBDMV. Sneath PHA Approved Lists of Bacterial Names. Int J Syst Bacteriol 1980; 30:225–420. ArticleGoogle Scholar
  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.
  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.Google Scholar
  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.
  39. 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. PubMed CentralView ArticlePubMedGoogle Scholar
  40. 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 CentralView ArticlePubMedGoogle Scholar
  41. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, et al. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 2008; 9:75. PubMed CentralView ArticlePubMedGoogle Scholar
  42. Delcher AL, Bratke KA, Powers EC, Salzberg SL. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 2007; 23:673–679. PubMed CentralView ArticlePubMedGoogle Scholar
  43. Overbeek R, Begley T, Butler RM, Choudhuri JV, Chuang HY, Cohoon M, de Crecy-Lagard V, Diaz N, Disz T, Edwards R, et al. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res 2005; 33:5691–5702. PubMed CentralView ArticlePubMedGoogle Scholar
  44. Tatusov RL, Galperin MY, Natale DA, Koonin EV. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 2000; 28:33–36. PubMed CentralView ArticlePubMedGoogle Scholar
  45. Pruitt KD, Tatusova T, Brown GR, Maglott DR. NCBI Reference Sequences (RefSeq): current status, new features and genome annotation policy. Nucleic Acids Res 2012; 40:D130–D135. PubMed CentralView ArticlePubMedGoogle Scholar
  46. Yu C, Zavaljevski N, Desai V, Reifman J. Genome-wide enzyme annotation with precision control: catalytic families (CatFam) databases. Proteins 2009; 74:449–460. PubMed ArticlePubMedGoogle Scholar
  47. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, et al. The Pfam protein families database. Nucleic Acids Res 2010; 38:D211–D222. PubMed CentralView ArticlePubMedGoogle Scholar
  48. Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T, Ussery DW. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 2007; 35:3100–3108. PubMed CentralView ArticlePubMedGoogle Scholar
  49. Lowe TM, Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997; 25:955–964. PubMedPubMed CentralView ArticlePubMedGoogle Scholar
  50. Markowitz VM, Mavromatis K, Ivanova NN, Chen IM, Chu K, Kyrpides NC. IMG ER: a system for microbial genome annotation expert review and curation. Bioinformatics 2009; 25:2271–2278. PubMed ArticlePubMedGoogle Scholar


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