Open Access

Complete genome sequence of Haloterrigena turkmenica type strain (4kT)

  • Elisabeth Saunders1, 2,
  • Brian J. Tindall3,
  • Regine Fähnrich3,
  • Alla Lapidus1,
  • Alex Copeland1,
  • Tijana Glavina Del Rio1,
  • Susan Lucas1,
  • Feng Chen1,
  • Hope Tice1,
  • Jan-Fang Cheng1,
  • Cliff Han1, 2,
  • John C. Detter1, 2,
  • David Bruce1, 2,
  • Lynne Goodwin1, 2,
  • Patrick Chain1, 2,
  • Sam Pitluck1,
  • Amrita Pati1,
  • Natalia Ivanova1,
  • Konstantinos Mavromatis1,
  • Amy Chen4,
  • Krishna Palaniappan4,
  • Miriam Land1, 5,
  • Loren Hauser1, 5,
  • Yun-Juan Chang1, 5,
  • Cynthia D. Jeffries1, 5,
  • Thomas Brettin1, 5,
  • Manfred Rohde6,
  • Markus Göker3,
  • James Bristow1,
  • Jonathan A. Eisen1, 7,
  • Victor Markowitz4,
  • Philip Hugenholtz1,
  • Hans-Peter Klenk3 and
  • Nikos C. Kyrpides1
Standards in Genomic Sciences20102:2010107

DOI: 10.4056/sigs.681272

Published: 28 February 2010

Abstract

Haloterrigena turkmenica (Zvyagintseva and Tarasov 1987) Ventosa et al. 1999, comb. nov. is the type species of the genus Haloterrigena in the euryarchaeal family Halobacteriaceae. It is of phylogenetic interest because of the yet unclear position of the genera Haloterrigena and Natrinema within the Halobacteriaceae, which created some taxonomic problems historically. H. turkmenica, was isolated from sulfate saline soil in Turkmenistan, is a relatively fast growing, chemoorganotrophic, carotenoid-containing, extreme halophile, requiring at least 2 M NaCl for growth. Here we describe the features of this organism, together with the complete genome sequence, and annotation. This is the first complete genome sequence of the genus Haloterrigena, but the eighth genome sequence from a member of the family Halobacteriaceae. The 5,440,782 bp genome (including six plasmids) with its 5,287 protein-coding and 63 RNA genes is part of the Genomic Encyclopedia of Bacteria and Archaea project.

Keywords

extreme halophile thermophile free-living aerobic non-pathogenic carotenoids-containing Halobacteriaceae GEBA

Introduction

Strain 4kT (= DSM 5511 = ATCC 51198 = VKM B-1734) is the type strain of the species Haloterrigena turkmenica, which is the type species of the genus Haloterrigena [1,2]. The strain was initially described in 1987 as Halococcus turkmenicus VKM B-1734 (basonym) by Zvyagintseva and Tarasov [3]. In 1999, Ventosa et al. proposed to transfer H. turkmenicus 4k as the type strain of the species H. turkmenica to the new genus Haloterrigena [1], whose name means salt, halos, (-requiring) and born from the earth, terrigena. Inconsistent data published on sequence similarity and DNA-DNA hybridization for some Haloterrigena and Natrinema strains created some confusion and taxonomic problems initially, but the problems were largely resolved in 2003 by Tindall [4], pointing to uncertainty about strain history. It has been suggested that the discrepancies may also be a result of 16S rDNA interoperon heterogeneity [5]. Published data appears to indicate that both strains GSL-11 and JCM 9743 (formally included in the species H. turkmenica by Ventosa et al. [1]) may be members of the genus Natrinema [4,6]. Those strains will not be considered further here.

There are no reliable reports of other strains of H. turkmenica having been isolated. 16S rRNA sequence identity with the other seven type strains in the genus, which were mainly isolated from salt lakes, range from 98.0% for H. salina [7] to 94.4% for H. longa [6]. The sequence similarity to the Natrinema type strains is somewhere in-between, 95.2-96.4% [8], underlining the taxonomic problems [4]. The sequence similarity to phylotypes in environmental metagenomic libraries was not above 87%, indicating a rather poor representation of closely related strains in the habitats analyzed (status January 2010). Here we present a summary classification and a set of features for H. turkmenica strain 4kT, together with the description of the complete genome sequencing and annotation.

Classification and features

Figure 1 shows the phylogenetic neighborhood of H. turkmenica strain 4kT in a 16S rRNA based tree. The three 16S rRNA gene sequences in the genome differ from each other by up to two nucleotides, and differ by up to six nucleotides from the previously published 16S rRNA sequence (AB004878) generated from DSM 5511. The difference between the genome data and the previously reported 16S rRNA gene sequences is most likely due to sequencing errors in the previously reported sequence data. As expected, Haloterrigena and Natrinema strains appear as intermixed in the tree, indicating a paraphyletic status of Haloterrigena (within which Natronorubrum and Natrinema branch off) and of Natrinema (within which H. longa is placed) [18].
Figure 1.

Phylogenetic tree highlighting the position of H. turkmenica strain 4kT relative to the other species within the genera Haloterrigena and Natrinema and the type strains of the other genera within the family Halobacteriaceae. The tree was inferred from 1,368 aligned characters [9,10] of the 16S rRNA sequence under the maximum likelihood criterion [11] and rooted with Natronomonas pharaonis [12]. The branches are scaled in terms of the expected number of substitutions per site. Numbers above branches are support values from 800 bootstrap replicates [13] if larger than 60%. Strains with a genome sequencing project registered in GOLD [14] are printed in blue; published genomes in bold, e.g. the recently published GEBA genomes from Halogeometricum borinquense [15], Halorhabdus utahensis [16], and Halomicrobium mukohataei [17].

H. turkmenica cells occur mostly as single cells, rarely in pairs or tetrads [1]. They are described as Gram-negative, ovoid to coccoid, 1.5–2 µm in diameter [1], but can also be rod-shaped (Figure 2 and Table 1) [1]. Neither spores, nor flagella, nor lipid granules were reported. Colonies are pigmented red or light pink due of the presence of C5O-carotenoids [1]. Stain 4kT is chemoorganotrophic and aerobic, and requires at least 2 M NaCl [1]. Detailed physiological characteristics were described by Zvyagintseva and Tarasov [3]. The G+C content of DNA was reported to be 59.2-60-2 mol % (Thermal denaturation method [1]), which is significantly less than the 64.3% found in the genome. At optimal growth temperatures, H. turkmenica is the fastest growing member of the Halobacteriaceae, with only 1.5 hours generation time [26]. Besides the chemical characterization of siderophores [29], there are no published reports on the molecular biology of H. turkmenica.
Figure 2.

Scanning electron micrograph of H. turkmenica strain 4kT

Table 1.

Classification and general features of H. turkmenica 4kT according to the MIGS recommendations [19]

MIGS ID

Property

Term

Evidence code

 

Current classification

Domain Archaea

TAS [20]

 

Phylum Euryarchaeota

TAS [21,22]

 

Class Halobacteria

TAS [23]

 

Order Halobacteriales

TAS [24]

 

Family Halobacteriacea

TAS [25]

 

Genus Haloterrigena

TAS [1]

 

Species Haloterrigena turkmenica

TAS [1]

 

Type strain 4k

TAS [3]

 

Gram stain

negative

TAS [1]

 

Cell shape

rods

TAS [1]

 

Motility

nonmotile

IDA

 

Sporulation

non-sporulating

NAS

 

Temperature range

29–57°C

TAS [26]

 

Optimum temperature

51°C

TAS [26]

 

Salinity

extreme halophile, requires at least 2% (w/v) NaCl

TAS [1]

MIGS-22

Oxygen requirement

aerobic

TAS [1]

 

Carbon source

yeast extract

NAS

 

Energy source

chemoorganotroph

TAS [1]

MIGS-6

Habitat

soil

TAS [1]

MIGS-15

Biotic relationship

free living

NAS

MIGS-14

Pathogenicity

none

NAS

 

Biosafety level

1

TAS [27]

 

Isolation

sulfate saline soil

TAS [3]

MIGS-4

Geographic location

Ashkhabad, Turkmenistan

TAS [3]

MIGS-5

Sample collection time

about or before 1987

TAS [3]

MIGS-4.1

Latitude,

37.950,

NAS

MIGS-4.2

Longitude

58.380

MIGS-4.3

Depth

unknown

 

MIGS-4.4

Altitude

unknown

 

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

Both diphytanyl moieties (C20, C20) and phytanyl-sesterterpanyl moieties (C20, C25) are present in polar lipids [1]. The presence of both phytanyl and esterterpanyl side chains implies the presence of three different prenyl transferases involved in lipid biosynthesis, which are probably chain length specific as well as stereospecific for the incorporation of the isoprenoid side chains into the glycerol backbone [30]. The presence of significant levels of both the diphytanyl moieties (C20, C20) and phytanyl-esterterpanyl moieties (C20, C25) is characteristic of all members examined of this evolutionary branch of the family Halobacteriaceae. Membrane polar lipids are glycerol-diether analogues of PG, PGP-Me and the disulfated digylcosyl diether lipid S2-DGD (mannose-2,6 disulfate 1→2 glucose-glycerol diether) [31], the characteristic glycolipid of Natrialba asiatica [32]. The presence of respiratory lipoquinones have not been reported, but it may be predicted that MK-8 and MK-8 (VIII-H2) should be present, since this is a feature of all members of the family Halobacteriaceae examined to date.

Genome sequencing and annotation information

Genome project history

This organism was selected for sequencing on the basis of its phylogenetic position, and is part of the Genomic Encyclopedia of Bacteria and Archaea project [33]. The genome project is deposited in the Genomes OnLine Database [14] and the complete genome sequence in GenBank. Sequencing, finishing and annotation were performed by the DOE Joint Genome Institute (JGI). A summary of the project information is shown in Table 2.
Table 2.

Genome sequencing project information

MIGS ID

Property

Term

MIGS-31

Finishing quality

Finished

MIGS-28

Libraries used

Three genomic libraries: one Sanger 8 kb pMCL200 library, one 454 pyrosequence standard library and one Illumina standard library

MIGS-29

Sequencing platforms

ABI3730, 454 GS FLX, and Illumina GA

MIGS-31.2

Sequencing coverage

6.9× Sanger; 19.9× pyrosequence

MIGS-30

Assemblers

Newbler version 1.1.03.24, phrap

MIGS-32

Gene calling method

Prodigal 1.4, GenePRIMP

 

Genbank ID

CP001860 (chromosome)

 

CP001861–CP001866 (plasmids)

 

Genbank Date of Release

January 19, 2010

 

GOLD ID

Gc01189

 

NCBI project ID

30411

 

Database: IMG-GEBA

2501939622

MIGS-13

Source material identifier

DSM 5511

 

Project relevance

Tree of Life, GEBA

Growth conditions and DNA isolation

H. turkmenica 4kT, DSM 5511, was grown in DSMZ medium 372 (Halobacteria medium) [34] at 37°C. DNA was isolated from 1–1.5 g of cell paste using Qiagen Genomic 500 DNA Kit (Qiagen, Hilden, Germany) with lysis modification L according to Wu et al. [33].

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 at the JGI can be found at the JGI website (http://www.jgi.doe.gov/). 454 Pyrosequencing reads were assembled using the Newbler assembler version 1.1.03.24 (Roche). Large Newbler contigs were broken into 6,060 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 [35]. A total of 1,183 Sanger finishing reads were produced to close gaps, to resolve repetitive regions, and to raise the quality of the finished sequence. Illumina reads were used to improve the final consensus quality using an in-house developed tool (the Polisher). 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 26.8× coverage of the genome. The final assembly contains 33,433 Sanger reads and 394,632 pyrosequencing reads.

Genome annotation

Genes were identified using Prodigal [36] as part of the Oak Ridge National Laboratory genome annotation pipeline, followed by a round of manual curation using the JGI GenePRIMP pipeline [37]. 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 (http://img.jgi.doe.gov/er) platform [38].

Genome properties

The genome is 5,440,782 bp long and comprises one main circular chromosome of 3,889,038 bp length and six circular plasmids of 15.8 to 698.5 kbp length, with an overall GC content of 64.3% (Table 3 and Figures 3 and 4). Of the 5,350 genes predicted, 5,287 were protein coding genes, and 63 RNAs; 174 pseudogenes were also identified. The majority of the protein-coding genes (60.1%) 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 chromosome. 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.

Figure 4.

Graphical circular map of the six plasmids: pHTUR01 (A), pHTUR02 (B), pHTUR03 (C), pHTUR04 (D), pHTUR05 (E), pHTUR06 (F). Plasmids not drawn to scale.

Table 3.

Genome Statistics

Attribute

Value

% of Total

Genome size (bp)

5,440,782

100.00%

DNA coding region (bp)

4,524,412

83.16%

DNA G+C content (bp)

3,496,479

64.26%

Number of replicons

7

 

Extrachromosomal elements

6

 

Total genes

5,350

100.00%

RNA genes

63

1.18%

rRNA operons

3

 

Protein-coding genes

5,287

98.82%

Pseudo genes

174

3.25%

Genes with function prediction

3,213

60.06%

Genes in paralog clusters

1,706

31.89%

Genes assigned to COGs

3,259

60.92%

Genes assigned Pfam domains

3,208

59.96%

Genes with signal peptides

625

11.68%

Genes with transmembrane helices

1,140

21.31%

CRISPR repeats

1

 
Table 4.

Number of genes associated with the general COG functional categories

Code

Value

%age

Description

J

178

3.4

Translation, ribosomal structure and biogenesis

A

1

0.0

RNA processing and modification

K

190

3.6

Transcription

L

150

2.8

Replication, recombination and repair

B

3

0.1

Chromatin structure and dynamics

D

35

0.7

Cell cycle control, mitosis and meiosis

Y

0

0.0

Nuclear structure

V

44

0.8

Defense mechanisms

T

161

3.0

Signal transduction mechanisms

M

125

2.4

Cell wall/membrane biogenesis

N

29

0.5

Cell motility

Z

0

0.0

Cytoskeleton

W

0

0.0

Extracellular structures

U

26

0.5

Intracellular trafficking and secretion

O

141

2.7

Posttranslational modification, protein turnover, chaperones

C

258

4.9

Energy production and conversion

G

221

4.2

Carbohydrate transport and metabolism

E

349

6.6

Amino acid transport and metabolism

F

78

1.5

Nucleotide transport and metabolism

H

189

3.6

Coenzyme transport and metabolism

I

176

3.3

Lipid transport and metabolism

P

224

4.2

Inorganic ion transport and metabolism

Q

87

1.6

Secondary metabolites biosynthesis, transport and catabolism

R

630

11.9

General function prediction only

S

321

6.1

Function unknown

-

2,091

39.5

Not in COGs

Declarations

Acknowledgements

We would like to gratefully acknowledge the help of Susanne Schneider (DSMZ) for DNA extraction and quality analysis. This work was performed under the auspices of the US Department of Energy’s Office of Science, Biological and Environmental Research Program, and by the University of California, Lawrence Berkeley National Laboratory under contract No. DE-AC02-05CH11231, Lawrence Livermore National Laboratory under Contract No. DE-AC52-07NA27344, and Los Alamos National Laboratory under contract No. DE-AC02-06NA25396, as well as German Research Foundation (DFG) INST 599/1-1.

Authors’ Affiliations

(1)
DOE Joint Genome Institute
(2)
Bioscience Division, Los Alamos National Laboratory
(3)
DSMZ - German Collection of Microorganisms and Cell Cultures GmbH
(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. Ventosa A, Gutiérrez MC, Kamekura M, Dyall-Smith ML. Proposal to transfer Halococcus turkmenicus, Halobacterium trapanicum JCM 9743 and strain GSL-11 to Haloterrigena turkmenica gen. nov., comb. nov. Int J Syst Bacteriol 1999; 49:131–136. PubMedView ArticlePubMedGoogle Scholar
  2. Oren A, Arahal DR, Ventosa A. Emended descriptions of the genera of the family Halobacteriaceae. Int J Syst Evol Microbiol 2009; 59:637–642. PubMed doi:10.1099/ijs.0.008904-0View ArticlePubMedGoogle Scholar
  3. Zvyagintseva IS, Tarasov AL. Extreme halophilic bacteria from saline soils. Mikrobiologiia 1987; 56:839–844.Google Scholar
  4. Tindall BJ. Taxonomic problems arising in the genera Haloterrigena and Natrinema. Int J Syst Evol Microbiol 2003; 53:1697–1698. PubMed doi:10.1099/ijs.0.02529-0View ArticlePubMedGoogle Scholar
  5. Walsh DA, Bapteste E, Kamekura M, Doolittle WF. Evolution of the RNA polymerase BSubunit Gene (rpoB’) in Halobacteriales: a complementary molecular marker to the SSU rRNA Gene. Mol Biol Evol 2004; 21:2340–2351. PubMed doi:10.1093/molbev/msh248View ArticlePubMedGoogle Scholar
  6. Cui HL, Tohty D, Zhou PJ, Liu SJ. Haloterrigena longa sp. nov. and Haloterrigena limicola sp. nov., extremely halophilic archaea isolated from a salt lake. Int J Syst Evol Microbiol 2006; 56:1837–1840. PubMed doi:10.1099/ijs.0.64372-0View ArticlePubMedGoogle Scholar
  7. Gutiérrez MC, Castillo AM, Kamekura M, Ventosa A. Haloterrigena salina sp. nov., an extremely halophilic archaeon isolated from a salt lake. Int J Syst Evol Microbiol 2008; 58:2880–2884. PubMed doi:10.1099/ijs.0.2008/001602-0View ArticlePubMedGoogle Scholar
  8. 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
  9. 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
  10. 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
  11. 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
  12. Falb M, Pfeiffer F, Palm P, Rodewald K, Hickmann V, Tittor J, Oesterhelt D. Living with two extremes: conclusions from the genome sequence of Natronomonas pharaonis. Genome Res 2005; 15:1336–1343. PubMed doi:10.1101/gr.3952905PubMed CentralView ArticlePubMedGoogle Scholar
  13. Pattengale ND, Alipour M, Bininda-Emonds ORP, Moret BME, Stamatakis A. How many bootstrap replicates are necessary? Lect Notes Comput Sci 2009; 5541:184–200. doi:10.1007/978-3-642-02008-7_13View ArticleGoogle Scholar
  14. 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
  15. Malfatti S, Tindall BJ, Schneider S, Fähnrich R, Lapidus A, LaButtii K, Copeland A, Glavina Del Rio T, Nolan M, Chen F, et al. Complete genome sequence of Halogeometricum borinquense type strain (PR3T). Stand Genomic Sci 2009; 1:150–158. doi:10.4056/sigs.23264PubMed CentralView ArticlePubMedGoogle Scholar
  16. Anderson I, Tindall BJ, Pomrenke H, Göker M, Lapidus A, Nolan M, Copeland A, Glavina Del Rio T, Chen F, Tice H, et al. Complete genome sequence of Halorhabdus utahensis type strain (AX-2T). Stand Genomic Sci 2009; 1:218–225. doi:10.4056/sigs.31864PubMed CentralView ArticlePubMedGoogle Scholar
  17. Tindall BJ, Schneider S, Lapidus A, Copeland A, Glavina Del Rio T, Nolan M, Lucas S, Chen F, Tice H, Cheng JF, et al. Complete genome sequence of Halomicrobium mukohataei type strain (arg-2T). Stand Genomic Sci 2009; 1:270–277. doi:10.4056/sigs.42644PubMed CentralView ArticlePubMedGoogle Scholar
  18. Farris JS. Formal definitions of paraphyly and polyphyly. Syst Zool 1974; 23:548–554. doi:10.2307/2412474View ArticleGoogle Scholar
  19. Field D, Garrity G, Gray T, Morrison N, Selengut J, Sterk P, Tatusova T, Thompson N, Allen MJ, Anguiuoli SV, et al. Towards a richer description of our complete collection of genomes and metagenomes: the “Minimum Information about a Genome Sequence” (MIGS) specification. Nat Biotechnol 2008; 26:541–547. PubMed doi:10.1038/nbt1360PubMed CentralView ArticlePubMedGoogle Scholar
  20. 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
  21. Garrity GM, Holt JG. Phylum AII. Euryarchaeota phy. nov. In: Bergey’s Manual of Systematic Bacteriology, vol. 1. 2nd ed. Edited by: Garrity, GM, Boone, DR and Castenholz, RW. Springer, New York; 2001:211–355.View ArticleGoogle Scholar
  22. List Editor. Validation of publication of new names and new combinations previously effectively published outside the IJSEM. Validation List no. 85. Int J Syst Evol Microbiol 2002; 52:685–690. PubMed doi:10.1099/ijs.0.02358-0
  23. Garrity GM, Lilburn TG, Cole JR, Harrison SH, Euzeby J, Tindall BJ. “Part 1 - The Archaea, Phyla Crenarchaeota and Euryarchaeota” Taxonomic Outline of the Bacteria and Archaea. 2007. www.taxonomicoutline.org.
  24. Grant WD, Larsen H. Group III. Extremely halophilic archaeobacteria. Order Halobacteriales ord. nov. In: Staley JT, Bryant MP, Pfennig N & Holt JG (eds) Bergey’s Manual of Systematic Bacteriology, First edition, Vol 3, The Williams & Watkins Co., Baltimore, 1989, pp 2216–2228.Google Scholar
  25. Gibbons NE. Family V. Halobacteriaceae fam. nov. In: Buchanan RE & Gibbons NE (eds) Bergey’s Manual of Determinative Bacteriology, eighth edition, The Williams & Watkins Co., Baltimore, 1974, pp 279.Google Scholar
  26. Robinson JL, Pyzyna B, Atrasz RG, Handerson CA, Morrill KL, Burd AM, Desoucy E, Fogleman RE, III, Naylor JB, Steele SM, et al. Growth kinetics of extremely halophilic Archaea (family Halobacteriaceae) as revealed by Arrhenius plots. J Bacteriol 2005; 187:923–929. PubMed doi:10.1128/JB.187.3.923-929.2005PubMed CentralView ArticlePubMedGoogle Scholar
  27. Biological Agents. Technical rules for biological agents www.baua.de TRBA 466.
  28. 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
  29. Dave BP, Anshuman K, Hajela P. Siderophores of halophilic Archaea and their chemical characterization. Indian J Exp Biol 2006; 44:340–344.PubMedGoogle Scholar
  30. Tachibana A. A novel prenyltransferase, farnesylgeranyl diphosphate synthase, from the haloalkaliphilic archaeon, Natronobacterium pharaonis. FEBS Lett 1994; 341:291–294. PubMed doi:10.1016/0014-5793(94)80475-3View ArticlePubMedGoogle Scholar
  31. Kamekura M, Dyall-Smith ML, Upasani V, Ventosa A, Kates M. Diversity of alkaliphilic halobacteria: proposals for the transfer of Natronobacterium vacuolatum, Natronobacterium magadii, and Natronobacterium pharaonis to the genus Halorubrum, Natrialba, and Natronomonas gen. nov., respectively, as Halorubrum vacuolatum comb. nov., Natrialba magadii comb. nov., and Natronomonas pharaonis comb. nov., respectively. Int J Syst Bacteriol 1997; 47:853–857. PubMedView ArticlePubMedGoogle Scholar
  32. Kamekura M, Dyall-Smith ML. Taxonomy of the family Halobacteriaceae and the description of two new genera Halorubrobacterium and Natrialba. J Gen Appl Microbiol 1995; 41:333–350. doi:10.2323/jgam.41.333View ArticleGoogle Scholar
  33. Wu D, Hugenholtz P, Mavromatis K, Pukall R, Dalin E, Ivanova N, Kunin V, Goodwin L, Wu M, Tindall BJ. A phylogeny-driven genomic encyclopedia of Bacteria and Archaea. Nature 2009; 462:1056–1060. PubMed doi:10.1038/nature08656PubMed CentralView ArticlePubMedGoogle Scholar
  34. List of growth media used at DSMZ: http://www.dsmz.de/microorganisms/media_list.php.
  35. Sims D, Brettin T, Detter JC, Han C, Lapidus A, Copeland A, Glavina Del Rio T, Nolan M, Chen F, Lucas S, et al. Complete genome of Kytococcus sedentarius type strain (541T). Stand Genomic Sci 2009; 1:12–20. doi:10.4056/sigs.761PubMed CentralView ArticlePubMedGoogle Scholar
  36. Hyatt D, Chen GL, LoCascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Genomics (In press).Google Scholar
  37. 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 (In press); http://geneprimp.jgi-psf.org/.
  38. 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