Open Access

Draft genome sequence of Amphibacillus jilinensis Y1T, a facultatively anaerobic, alkaliphilic and halotolerant bacterium

  • Hong Cheng1,
  • Ming-Xu Fang1, 2,
  • Xia-Wei Jiang1, 3,
  • Min Wu1Email author,
  • Xu-Fen Zhu1,
  • Gang Zheng4 and
  • Zhi-Jian Yang1
Standards in Genomic Sciences20138:8030491

DOI: 10.4056/sigs.4107829

Published: 30 July 2013

Abstract

The genus Amphibacillus was established in 1990, and seven additional species were described in the past two decades. Amphibacillus jilinensis Y1T is a facultatively anaerobic and alkaliphilic bacterium isolated from a soda lake in China. Here we describe the structural and genetic features of the draft genome about the type strain Y1T (3,831,075 bp, with a G+C content of 37.27%). This is the first genome report of the Amphibacillus genus.

Keywords

Amphibacillus facultative anaerobe alkaliphilic bacterium halotolerant soda lake two-component systems

Introduction

The genus Amphibacillus belongs to the family Bacillaceae and was established in 1990 [1]. Currently the genus comprises eight validly published species: A. xylanus [1], A. indicireducens [2], A. cookii [3], A. marinus [4], A. jilinensis [5], A. sediminis [6], A. fermentum and A. tropicus [7]. All are Gram-positive, moderately alkaliphilic, facultatively anaerobic rods [5,6]. All can grow at pH 9.0 and one can grow at pH 12.0 [24,6]. Amphibacillus jilinensis Y1T (=CGMCC 1.5123T =JCM 16149T) was isolated from a soda lake in Jilin province, China, and grows at pH range from 7.5 to 10.5 with an optimum at 9.0 [5]. Strain Y1T can utilize a large spectrum of substrates as sources of carbon and energy, can grow both aerobically and anaerobically, and tolerate Na+ up to 2.8 M. In this genus, three species have been sequenced. A finished genome sequence is Amphibacillus xylanus NBRC 15112 (NCBI Accession Number AP012050) and two incomplete sequences are A. jilinensis Y1T (NCBI Accession Number AMWI00000000) and Amphibacillus sediminis Shu-P-Ggiii25-2 (NCBI BioProject ID PRJDB405) according to the GOLD records [8,9]. Here we report this draft genome of A. jilinensis Y1T, the first genome from genus Amphibacillus to be sequenced.

Classification and features

A sediment sample was collected from a soda lake (44°45′N, 123°34′E) in Jilin province, China, in November 2007. There is no freshwater river to flow into the lake. Atmospheric water and groundwater are the only water sources of this lake. The lake is rich in Na+ (257.2 mg/l), CO32- (50.7 mg/l), Cl- (10.1 mg/l), HCO3- (6.5 mg/l) and SO42- (4.4 mg/l), with the pH of the water sample in the same geographical location being 10.0 [5]. The strain Y1T was isolated from enrichment cultures of sediment sample by the Hungate roll-tube technique [10] under a gas phase of O2-free N2 [1,5].

Comparative 16S rRNA gene sequence analysis by BLASTN [11,12] using the NCBI-NR/NT database revealed 93.4-98.8% sequence similarity to members of the genus Amphibacillus. Neighbor-Joining phylogenetic analysis based on Tamura-Nei model indicated the taxonomic status of strain Y1T is clearly classified into the same branch with genus Amphibacillus, and the most closely related genus is Halolactibacillus (Figure 1). A. jilinensis Y1T can tolerant high salinity but can also survive without Na+. Growth occurs under either aerobic or anaerobic conditions. The optimal growth condition of strain Y1T occurs in medium JY with 0.5 M Na+ (0.06 M NaHCO3 and 0.44 M NaCl) [5]. The optimum pH is 9.0, with a growth range of pH 7.5–10.5. No growth was observed at pH 7.0 or 11.0. Strain Y1T is mesophilic, with a temperature range of 15–45 ̱C and optimum growth at 32 ̱C [Table 1]. Cell morphology, motility and sporulation were examined by using transmission electron (H-600, Hitachi) microscopy. Cells of strain Y1T are straight rods with petritrichous flagella, which have a diameter ranging 0.4–0.6 µm and a length of 2.0–3.2 µm (Figure 2a). In the late-exponential and stationary phases of growth, the rods can form terminal endospores (Figure 2b).
Figure 1.

Phylogenetic tree highlighting the position of A. jilinensis strain Y1T relative to other type strains within the Amphibacillus genus and with the relative Halolactibacillus genus. The strains and their corresponding Genbank accession numbers are shown following the organism name and indicated in parentheses. Three strains have their corresponding NCBI genome project IDs and sequencing status [8,13] listed here: PRJNA42371 of A. xylanus DSM 6626T, complete; PRJNA171498 of A. jilinensis Y1T, Draft; PRJDB405 of A. sediminis Shu-P-Ggiii25-2T, in progress. The phylogenetic tree uses 16S rRNA gene sequences aligned by the CLUSTALW [14], and phylogenetic inferences were made using Neighbor-joining method based on Tamura-Nei model within the MEGA5 software [15]. Numbers at the branching nodes are percentages of bootstrap values based on 1,000 replications. The scale bar indicates a 1% substitution per nucleotide position. Bacillus subtilis DSM 10T was used as an outgroup.

Figure 2a.

Transmission electron micrograph of cells of strain Y1T, showing a longitudinal ultrathin section of a cell forming a spore. Bar: 0.2 εm (a).

Figure 2b.

Transmission electron micrograph of cells of strain Y1T, showing a longitudinal ultrathin section of the peritrichous flagella in the stationary phase of growth. Bar: 0.5 εm (b).

Table 1.

Classification and general features of A. jilinensis Y1T according to the MIGS recommendations [16]

MIGS ID

Property

Term

Evidence codea

 

Current classification

Domain: Bacteria

TAS [17]

 

Phylum: Firmicutes

TAS [1820]

 

Class: Bacilli

TAS [21,22]

 

Order: Bacillales

TAS [23,24]

 

Family: Bacillaceae

TAS [23,25]

 

Genus: Amphibacillus

TAS [1,2,6]

 

Species: Amphibacillus jilinensis

 
  

Type strain: strain Y1T = CGMCC 1.5123 = JCM 16149

TAS [5]

 

Gram stain

positive

IDA

 

Cell shape

rods

IDA

 

Motility

motile

IDA

 

Sporulation

sporulating

IDA

 

Temperature range

15–45°C

IDA

 

Optimum temperature

32°C

IDA

 

Carbon source

L-arabinose, cellobiose, D-fructose, D-galactose, D-glucose, lactose, maltose, mannose, D-mannitol, melibiose, D-raffinose, rhamnose, D-sorbitol, sucrose, trehalose and D-xylose.

IDA

 

Energy source

yeast extract, sucrose, glucose

IDA

 

Terminal electron receptor

Unknown

IDA

MIGS-6

Habitat

aquatic, fresh water, soda lakes, sediment

IDA

MIGS-6.3

Salinity

The water contains Na+ (257.2 mg/l), CO32−(50.7 mg/l), Cl (10.1 mg/l), HCO3 (6.5 mg/l) and SO42− (4.4 mg/l), with the pH 10.0

IDA

MIGS-22

Oxygen

unknown

IDA

MIGS-15

Biotic relationship

free living

IDA

MIGS-14

Pathogenicity

unknown

 

MIGS-4

Geographic location

a soda lake in Jinli Province, P.R. China

IDA

MIGS-5

Sample collection time

November, 2007

IDA

MIGS-4.1

Latitude

44°45′N

IDA

MIGS-4.2

Longitude

123°34′E

IDA

MIGS-4.3

Depth

Sediment

IDA

MIGS-4.4

Altitude

148 m above sea level

IDA

a) Evidence codes - 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 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 the Gene Ontology project [26,27]. If the evidence code is IDA, then the property should have been directly observed, for the purpose of this specific publication, for a live isolate by one of the authors, or an expert or reputable institution mentioned in the acknowledgements.

Genome sequencing information

Genome project history

The genome of A. jilinensis was selected for next-generation sequencing on the consideration of its facultatively anaerobic characterization and as a new member in genus Amphibacillus. This is the first genome report for any of the eight Amphibacillus species. Two others are the subject of ongoing own genome projects. This Whole Genome Shotgun project of A. jilinensis was deposited at DDBJ/EMBL/GenBank under the accession AMWI00000000 and consists of 83 contigs (further assembling constructed these contigs into 30 scaffolds). Table 2 presents the project information and its association with MIGS version 2.0 compliance [16].
Table 2.

Project information

MIGS ID

Property

Term

MIGS-31

Finishing quality

High-quality draft

MIGS-28

Libraries used

One pair-end 500 bp library and one pair-end 2 Kb library

MIGS-29

Sequencing platforms

Illumina HiSeq 2000

MIGS-31.2

Fold coverage

130 × (based on 500 bp library), 65 × (based on 2 Kb library)

MIGS-30

Assemblers

SOAPdenovo

MIGS-32

Gene calling method

RAST

 

Genbank ID

AMWI00000000

 

Genbank Date of Release

October 18, 2012

 

GOLD ID

Gi20767

 

Project relevance

Microbial pathway & resources

Growth conditions and DNA isolation

A. jilinensis Y1T was cultivated aerobically in modified JY medium, which contains (per liter distilled water) 2.0 g yeast extract (Difco), 5.0 g sucrose, 0.2 g KCl, 0.2 g KH2PO4, 0.1 g MgCl2. 6H2O, 0.5 g NH4Cl, 0.1 g CaCl2, 0.06 M NaHCO3 and 0.44 M NaCl, final pH 9.0 at 32°C for 3 days [5]. Genomic DNA was extracted using the method described by Marmur [28]. The yield, purity and the concentration of genomic DNA was judged by the 0.7% agarose gel electrophoresis with λ-Hind III digest DNA Marker (TaKaRa, Dalian, China) and measured by the NanoDrop 1000 Spectrophotometer (Thermo Fisher Scientific Inc., USA). About 736.6 εg genomic DNA at the concentration 744 ng/εl was obtained.

Genome sequencing and assembly

Genomic DNA sequencing of A. jilinensis Y1T was performed using Solexa paired-end sequencing technology (HiSeq2000 system, Illumina, Inc., USA) [29] with a whole-genome shotgun (WGS) strategy, with a 500 bp-span paired-end library (500 Mb available reads, 130-fold genome coverage) and a 2,000 bp-span paired-end library (250 Mb available reads, 65-fold genome coverage). All these clean reads were assembled into 83 contigs (the minimum length is 231 bp) and 30 scaffolds (the minimum length is 542 bp) using the SOAPdenovo v.1.05 [30,31,50]. The quality of the sequencing reads data was estimated by G+C content and sequencing depth correlation analysis.

Genome annotation

The tRNAs and rRNAs were identified using tRNAscan-SE [32], RNAmmer [33] and Rfam database [34]; The open reading frames (ORFs) and the functional annotation of translated ORFs were predicted and achieved by using the RAST server online [35,51]. Classification of some predicted genes and pathways were analyzed using COGs [36,37] and KEGG [3840] databases. Meanwhile, we used the InterPro [41,42] to obtain the GO annotation with the database of Pfam [43].

Genome properties

The draft genome sequence of A. jilinensis Y1T revealed a genome size of 3,836,603 bp (scaffold length) and a G+C content of 37.27%. These scaffolds contain 3,649 coding sequences (CDSs), 51 tRNAs (removed 3 Pseudo tRNAs) and incomplete rRNA operons (two 5 S rRNA and one 16 S rRNA). A total of 2,683 protein-coding genes (67.72%) were assigned a predicted function (Table 3) and genes have been categorized into COGs functional groups (Table 4).
Table 3.

Genome statistics of A. jilinensis Y1T

Attribute

Value

% of totala

Genome size (bp)

3,836,603

-

DNA coding region (bp)

3,169,605

82.61

DNA G+C content (bp)

1,429,902

37.27

Total genesb

3,705

100.00

RNA genes

56

1.51

Protein-coding genes

3,649

98.49

Genes assigned to COGs

2,683

73.52

a) The total is based on either the size of the genome in base pairs or the total number of protein coding genes in the annotated genome.

b) Includes 1,092 hypothetical proteins and 19 unknown functional proteins by RAST subsystem annotation.

Table 4.

Number of genes associated with the general COG functional categories

Code

Value

%agea

Description

J

162

5.37

Translation

K

282

9.34

Transcription

L

201

6.66

Replication, recombination and repair

D

37

1.23

Cell cycle control, mitosis and meiosis

V

88

2.92

Defense mechanisms

T

184

6.10

Signal transduction mechanisms

M

149

4.94

Cell wall/membrane biogenesis

N

72

2.39

Cell motility

U

42

1.39

Intracellular trafficking and secretion

O

90

2.98

Posttranslational modification, protein turnover, chaperones

C

106

3.51

Energy production and conversion

G

359

11.90

Carbohydrate transport and metabolism

E

244

8.08

Amino acid transport and metabolism

F

72

2.39

Nucleotide transport and metabolism

H

79

2.62

Coenzyme transport and metabolism

I

57

1.89

Lipid transport and metabolism

P

159

5.27

Inorganic ion transport and metabolism

Q

36

1.19

Secondary metabolites biosynthesis, transport and catabolism

R

338

11.20

General function prediction only

S

261

8.65

Function unknown

-

966

26.47

Not in COGs

aThe total is based on the total number of genes which categorized into COGs functional groups in the annotated genome.

Insights from the genome sequence

The genomic annotation results suggest that strain Y1T can adapt to an extremely basic environments. A large number of genes related to carbohydrate metabolism can encode proteins that provide a stable energy supply to maintain the lower internal pH despite the high external pH [44]. Several cation/proton antiporters were found in the genome, which are also crucial for the maintenance of internal pH [45]. However, the lower number of these genes in Y1T when compared to Bacillus pseudofirmus OF4 [44] may imply another way of importing protons into the cell. Meanwhile, as a facultatively anaerobic bacterium, 27 oxidative stress related genes are found in the predicted annotations, such as manganese superoxide dismutase (EC 1.15.1.1), superoxide dismutase [Cu-Zn] precursor (EC 1.15.1.1), organic hydroperoxide resistance transcriptional regulator and CoA-disulfide reductase (EC 1.8.1.14). For facultatively anaerobic strains, these superoxide dismutases (SODs) may be critical because the systems can help to regulate intracellular oxidative stress when the cells grow during aerobic respiration, and can also be used in the treatment of disease, study of pharmacological activity [46] and in the cosmetic industry. It also contains 34 two-component system genes that encode response regulators and sensor histidine kinases. The two-component systems appear to be used to respond to a wide variety of stimuli, including the presence of nutrients, antibiotics and chemoattractants in the environment, changes in osmolarity, temperature, pH, etc [47,48]. This is especially true in strain Y1T, in which these systems are thought to be used for recognizing environmental pH, and regulating its internal osmotic stress to survive various environments [49]. According to the database Pfam [43], there are also 9 CRISPRs-associated (Cas) proteins or Cas protein families in this genome of A. jilinensis.

Conclusion

Strain Y1T is the fifth member of the genus Amphibacillus to be described and is the first for which a genome sequence report is available. These data will provide a new perspective of how microorganisms adapt to anoxic and alkaline environments, and may also provide a pool of functional enzymes that work at higher pH.

Notes

Declarations

Acknowledgements

We thank Xiao-Yue Wu for her work in isolation and characterization of this new bacterial species and Xin-Qi Zhang for her professional advice. This work was supported by the Chinese Natural Science Foundation (grant no. 31170001) and Zhoushan Science and Technology Projects (no. 2012C33024 & no. 2011C31013).

Authors’ Affiliations

(1)
College of Life Sciences, Zhejiang University
(2)
Department of Molecular and Cellular Biochemistry, Indiana University
(3)
State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, First Affiliated Hospital, College of Medicine, Zhejiang University
(4)
Ocean Research Center of Zhoushan, Zhejiang University

References

  1. Niimura Y, Koh E, Yanagida F, Suzuki KI, Komagata K, Kozaki M. Amphibacillus xylanus gen. nov., sp. nov., a facultatively anaerobic sporeforming xylan-digesting bacterium which lacks cytochrome, quinone, and catalase. Int J Syst Bacteriol 1990; 40:297–301. http://dx.doi.org/10.1099/00207713-40-3-297View ArticleGoogle Scholar
  2. Hirota K, Aino K, Nodasaka Y, Morita N, Yumoto I. Amphibacillus indicireducens sp. nov., a facultatively alkaliphile that reduces an indigo dye. Int J Syst Evol Microbiol 2013; 63:464–469. PubMed http://dx.doi.org/10.1099/ijs.0.037622-0View ArticlePubMedGoogle Scholar
  3. Pugin B, Blamey JM, Baxter BK, Wiegel J. Amphibacillus cookii sp. nov., a facultatively aerobic, sporeforming, moderate halophilic, alkalithermotolerant bacterium from Great Salt Lake, Utah. Int J Syst Evol Microbiol 2012; 62:2090–2096. PubMed http://dx.doi.org/10.1099/ijs.0.034629-0View ArticlePubMedGoogle Scholar
  4. Ren B, Yang N, Wang J, Ma XL, Wang Q, Xie F, Guo H, Liu ZH, Pugin BÆ, Zhang LX. Amphibacillus marinus sp. nov., a new member of the genus Amphibacillus isolated from the South China Sea. Int J Syst Evol Microbiol 2013; 63:1485–1491. PubMed http://dx.doi.org/10.1099/ijs.0.045807-0View ArticlePubMedGoogle Scholar
  5. Wu XY, Zheng G, Zhang WW, Xu XW, Wu M, Zhu XF. Amphibacillus jilinensis sp. nov., a facultatively anaerobic, alkaliphilic bacillus from a soda lake. Int J Syst Evol Microbiol 2010; 60:2540–2543. PubMed http://dx.doi.org/10.1099/ijs.0.018259-0View ArticlePubMedGoogle Scholar
  6. An SY, Ishikawa S, Kasai H, Goto K, Yokota A. Amphibacillus sediminis sp. nov., an endospore-forming bacterium isolated from lake sediment in Japan. Int J Syst Evol Microbiol 2007; 57:2489–2492. PubMed http://dx.doi.org/10.1099/ijs.0.64926-0View ArticlePubMedGoogle Scholar
  7. Zhilina T, Garnova E, Tourova T, Kostrikina N, Zavarzin G. Amphibacillus fermentum sp. nov. and Amphibacillus tropicus sp. nov., New Alkaliphilic, Facultatively Anaerobic, Saccharolytic Bacilli from Lake Magadi. Microbiology 2001; 70:825–837. PubMedPubMedGoogle Scholar
  8. Pagani I, Liolios K, Jansson J, Chen IMA, Smirnova T, Nosrat B, Markowitz VM, Kyrpides NC. The Genomes OnLine Database (GOLD) v. 4: status of genomic and metagenomic projects and their associated metadata. Nucleic Acids Res 2012; 40(D1):D571–D579. PubMed http://dx.doi.org/10.1093/nar/gkr1100PubMed CentralView ArticlePubMedGoogle Scholar
  9. Genomes On Line Database. http://www.genomesonline.org
  10. Humane R. A roll tube method for cultivation of strict anaerobes. METHODS IN MICROBIOLOGY, VOLUME 3B 1969;3:117.View ArticleGoogle Scholar
  11. Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL. NCBI BLAST: a better web interface. Nucleic Acids Res 2008; 36(suppl 2):W5. PubMed http://dx.doi.org/10.1093/nar/gkn201PubMed CentralView ArticlePubMedGoogle Scholar
  12. McGinnis S, Madden TL. BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Res 2004; 32(suppl 2):W20–W25. PubMed http://dx.doi.org/10.1093/nar/gkh435PubMed CentralView ArticlePubMedGoogle Scholar
  13. Liolios K, Chen IMA, 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(suppl 1):D346–D354. PubMed http://dx.doi.org/10.1093/nar/gkp848PubMed CentralView ArticlePubMedGoogle Scholar
  14. Thompson JD, Gibson TJ, Higgins DG. Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics 2002. PubMed http://dx.doi.org/10.1002/0471250953.bi0203s00
  15. 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 http://dx.doi.org/10.1093/molbev/msr121PubMed CentralView ArticlePubMedGoogle Scholar
  16. Field D, Garrity G, Gray T, Morrison N, Selengut J, Sterk P, Tatusova T, Thomson N, Allen MJ, Angiuoli SV. The minimum information about a genome sequence (MIGS) specification. Nat Biotechnol 2008; 26:541–547. PubMed http://dx.doi.org/10.1038/nbt1360PubMed CentralView ArticlePubMedGoogle Scholar
  17. 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 http://dx.doi.org/10.1073/pnas.87.12.4576PubMed CentralView ArticlePubMedGoogle Scholar
  18. Gibbons NE, Murray RGE. Proposals Concerning the Higher Taxa of Bacteria. Int J Syst Bacteriol 1978; 28:1–6. http://dx.doi.org/10.1099/00207713-28-1-1View ArticleGoogle Scholar
  19. 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
  20. 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
  21. List Editor. 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. http://dx.doi.org/10.1099/ijs.0.022855-0
  22. Ludwig W, Schleifer KH, 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
  23. Skerman VBD, McGowan V, Sneath PHA. Approved Lists of Bacterial Names. Int J Syst Bacteriol 1980; 30:225–420. http://dx.doi.org/10.1099/00207713-30-1-225View ArticleGoogle Scholar
  24. Prévot AR. In: Hauderoy P, Ehringer G, Guillot G, Magrou. J., Prévot AR, Rosset D, Urbain A (eds), Dictionnaire des Bactéries Pathogènes, Second Edition, Masson et Cie, Paris, 1953, p. 1–692.Google Scholar
  25. Fischer A. Untersuchungen über bakterien. Jahrbücher für Wissenschaftliche Botanik 1895; 27:1–163.Google Scholar
  26. 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. The Gene Ontology Consortium. Nat Genet 2000; 25:25–29. PubMed http://dx.doi.org/10.1038/75556PubMed CentralView ArticlePubMedGoogle Scholar
  27. Gene Ontology project. http://www.geneontology.org/GO.evidence.shtml
  28. Marmur J, Doty P. Determination of the base composition of deoxyribonucleic acid from its thermal denaturation temperature. J Mol Biol 1962; 5:109–118. PubMed http://dx.doi.org/10.1016/S0022-2836(62)80066-7View ArticlePubMedGoogle Scholar
  29. Bentley DR, Balasubramanian S, Swerdlow HP, Smith GP, Milton J, Brown CG, Hall KP, Evers DJ, Barnes CL, Bignell HR. Accurate whole human genome sequencing using reversible terminator chemistry. Nature 2008; 456:53–59. PubMed http://dx.doi.org/10.1038/nature07517PubMed CentralView ArticlePubMedGoogle Scholar
  30. Li R, Zhu H, Ruan J, Qian W, Fang X, Shi Z, Li Y, Li S, Shan G, Kristiansen K, et al. De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 2010; 20:265–272. PubMed http://dx.doi.org/10.1101/gr.097261.109PubMed CentralView ArticlePubMedGoogle Scholar
  31. Li R, Li Y, Kristiansen K, Wang J. SOAP: short oligonucleotide alignment program. Bioinformatics 2008; 24:713. PubMed http://dx.doi.org/10.1093/bioinformatics/btn025View ArticlePubMedGoogle Scholar
  32. Lowe TM, Eddy S. 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
  33. Lagesen K, Hallin P. Rødland EA, Staerfeldt HH, Rognes T, Ussery DW. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 2007; 35:3100. PubMed http://dx.doi.org/10.1093/nar/gkm160PubMed CentralView ArticlePubMedGoogle Scholar
  34. Griffiths-Jones S, Bateman A, Marshall M, Khanna A, Eddy SR. Rfam: an RNA family database. Nucleic Acids Res 2003; 31:439. PubMed http://dx.doi.org/10.1093/nar/gkg006PubMed CentralView ArticlePubMedGoogle Scholar
  35. Aziz RK, Bartels D, Best A, DeJongh M, Disz T, Edwards R, Formsma K, Gerdes S, Glass E, Kubal M. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 2008; 9:75. PubMed http://dx.doi.org/10.1186/1471-2164-9-75PubMed CentralView ArticlePubMedGoogle Scholar
  36. Tatusov RL, Natale D, Garkavtsev I, Tatusova T, Shankavaram U, Rao B, Kiryutin B, Galperin M, Fedorova N, Koonin E. The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 2001; 29:22–28. PubMed http://dx.doi.org/10.1093/nar/29.1.22PubMed CentralView ArticlePubMedGoogle Scholar
  37. 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 http://dx.doi.org/10.1093/nar/28.1.33PubMed CentralView ArticlePubMedGoogle Scholar
  38. Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T. KEGG for linking genomes to life and the environment. Nucleic Acids Res 2008(36 Database):D480 — 484.Google Scholar
  39. Moriya Y, Itoh M, Okuda S, Kanehisa M. KAAS: KEGG automatic annotation server. Genome Informatics 2005; 5:2005.Google Scholar
  40. Kanehisa M, Goto S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 2000; 28:27. PubMed http://dx.doi.org/10.1093/nar/28.1.27PubMed CentralView ArticlePubMedGoogle Scholar
  41. Zdobnov EM, Apweiler R. InterProScan Can integration platform for the signature-recognition methods in InterPro. Bioinformatics 2001; 17:847. PubMed http://dx.doi.org/10.1093/bioinformatics/17.9.847View ArticlePubMedGoogle Scholar
  42. Apweiler R, Attwood TK, Bairoch A, Bateman A, Birney E, Biswas M, Bucher P, Cerutti L, Corpet F, Croning MDR. The InterPro database, an integrated documentation resource for protein families, domains and functional sites. Nucleic Acids Res 2001; 29:37. PubMed http://dx.doi.org/10.1093/nar/29.1.37PubMed CentralView ArticlePubMedGoogle Scholar
  43. Bateman A, Coin L, Durbin R, Finn RD, Hollich V, Griffiths Jones S, Khanna A, Marshall M, Moxon S, Sonnhammer ELL. The Pfam protein families database. Nucleic Acids Res 2004; 32(suppl 1):138D. PubMed http://dx.doi.org/10.1093/nar/gkh121View ArticleGoogle Scholar
  44. Janto B, Ahmed A, Ito M, Liu J, Hicks DB, Pagni S, Fackelmayer OJ, Smith TA, Earl J, Elbourne LD, et al. Genome of alkaliphilic Bacillus pseudofirmus OF4 reveals adaptations that support the ability to grow in an external pH range from 7.5 to 11.4. Environ Microbiol 2011; 13:3289–3309. PubMed http://dx.doi.org/10.1111/j.1462-2920.2011.02591.xPubMed CentralView ArticlePubMedGoogle Scholar
  45. Horikoshi K. Alkaliphiles: some applications of their products for biotechnology. [table of contents.]. Microbiol Mol Biol Rev 1999; 63:735–750. PubMedPubMed CentralPubMedGoogle Scholar
  46. Muscoli C, Cuzzocrea S, Riley DP, Zweier JL, Thiemermann C, Wang ZQ, Salvemini D. On the selectivity of superoxide dismutase mimetics and its importance in pharmacological studies. Br J Pharmacol 2003; 140:445–460. PubMed http://dx.doi.org/10.1038/sj.bjp.0705430PubMed CentralView ArticlePubMedGoogle Scholar
  47. Wolanin PM, Thomason PA, Stock JB. Histidine protein kinases: key signal transducers outside the animal kingdom. Genome Biol 2002; 3:S3013. PubMed http://dx.doi.org/10.1186/gb-2002-3-10-reviews3013View ArticleGoogle Scholar
  48. Attwood PV, Piggott M, Zu X, Besant P. Focus on phosphohistidine. Amino Acids 2007; 32:145–156. PubMed http://dx.doi.org/10.1007/s00726-006-0443-6View ArticlePubMedGoogle Scholar
  49. Krell T, Lacal J, Busch A, Silva-Jiménez H, Guazzaroni ME, Ramos JL. Bacterial sensor kinases: diversity in the recognition of environmental signals. Annu Rev Microbiol 2010; 64:539–559. PubMed http://dx.doi.org/10.1146/annurev.micro.112408. 134054View ArticlePubMedGoogle Scholar
  50. SOAP. denovo v.1.05. http://soap.genomics.org.cn/soapdenovo.html
  51. RAST server online. http://rast.nmpdr.org

Copyright

© The Author(s) 2013