Open Access

Complete genome sequence of the Antarctic Halorubrum lacusprofundi type strain ACAM 34

  • Iain J. Anderson1,
  • Priya DasSarma2Email author,
  • Susan Lucas1,
  • Alex Copeland1,
  • Alla Lapidus1,
  • Tijana Glavina Del Rio1,
  • Hope Tice1,
  • Eileen Dalin1,
  • David C. Bruce3,
  • Lynne Goodwin3,
  • Sam Pitluck1,
  • David Sims3,
  • Thomas S. Brettin3,
  • John C. Detter3,
  • Cliff S. Han3,
  • Frank Larimer1, 4,
  • Loren Hauser1, 4,
  • Miriam Land1, 4,
  • Natalia Ivanova1,
  • Paul Richardson1,
  • Ricardo Cavicchioli5,
  • Shiladitya DasSarma2,
  • Carl R. Woese6 and
  • Nikos C. Kyrpides1
Standards in Genomic Sciences201611:70

https://doi.org/10.1186/s40793-016-0194-2

Received: 7 July 2016

Accepted: 3 September 2016

Published: 10 September 2016

Abstract

Halorubrum lacusprofundi is an extreme halophile within the archaeal phylum Euryarchaeota. The type strain ACAM 34 was isolated from Deep Lake, Antarctica. H. lacusprofundi is of phylogenetic interest because it is distantly related to the haloarchaea that have previously been sequenced. It is also of interest because of its psychrotolerance. We report here the complete genome sequence of H. lacusprofundi type strain ACAM 34 and its annotation. This genome is part of a 2006 Joint Genome Institute Community Sequencing Program project to sequence genomes of diverse Archaea.

Keywords

Archaea Halophile Halorubrum Extremophile Cold adaptation Tree of life

Introduction

Halorubrum lacusprofundi is an extremely halophilic archaeon belonging to the class Halobacteria within the phylum Euryarchaeota . The species is represented by the type strain, ACAM 34 (= DSM 5036 = ATCC 49239 = JCM 8891), and a second strain, ACAM 32, both of which were isolated from Deep Lake, Antarctica [1]. This organism was first described as Halobacterium lacusprofundi but was later transferred to the genus Halorubrum [2]. Members of the genus Halorubrum have been found not only in Antarctica, but also in Africa [3], Asia [4], and North America [5], where they are usually found in saline lakes or salterns. Most members of the genus are neutrophiles, but some are haloalkaliphiles [6, 7]. H. lacusprofundi (Fig. 1) was proposed for sequencing as part of a 2006 Joint Genome Institute Community Sequencing Program project because of its ability to grow at low temperature and its phylogenetic distance from other halophiles with sequenced genomes (Fig. 2).
Fig. 1

Photomicrograph of H. lacusprofundi type strain ACAM 34 cells. The cells were grown in Franzmann et al. [1] medium. The image was taken using a phase microscope (Nikon Labphot) with 1000× magnification. The scale bar represents 10 μm

Fig. 2

Phylogenetic tree of DNA-directed RNA polymerase subunit A’ of select haloarchaea. Sequence alignment and tree construction were carried out with Clustal W [39]. The tree was visualized with njplot [40]. Positions with gaps were excluded during tree construction. Methanosarcina acetivorans was used as the outgroup. The numbers indicate bootstrap values based on 1000 replicates

Organism information

Classification and features

Halorubrum lacusprofundi ACAM 34 was isolated from a water-sediment sample from Deep Lake, Antarctica [1]. The water-sediment sample was incubated in the light at 18 °C, and after 3 months developed a reddish color. H. lacusprofundi was isolated from the sample by streaking on Deep Lake vitamin agar, which was composed of Lake Deep water with 1 g/L yeast extract, 15 g/L agar, and vitamin solution. The physiological characteristics of H. lacusprofundi were described as follows [1]. Cells were pleomorphic. Motility was not observed, and no flagella were present. Cells grew at a temperature range of −1 °C to 40 °C with an optimal growth temperature of 36 °C [8]. Growth was observed at NaCl concentration of 1.5 M to 4.5 M with an optimum salt concentration of 3.5 M. Cells lysed in distilled water. The optimum magnesium concentration for growth was 0.1 M. No growth was observed at magnesium concentrations of 0 M or 1.0 M. Ammonium could not be used as a nitrogen source; complex media such as yeast extract or peptone was required. Growth was stimulated by addition of glucose, galactose, mannose, ribose, lactose, glycerol, succinate, lactate, formate, acetate, propionate, and ethanol. Growth was not stimulated by addition of glycine. Acid was not produced from sugars.

Genome sequencing information

Genome project history

H. lacusprofundi was selected for sequencing based upon its phylogenetic position relative to other haloarchaea and its cold tolerance (Table 1). It is part of a 2006 Joint Genome Institute Community Sequencing Program project that included six diverse archaeal genomes. Sequencing was done at the JGI Production Genomics Facility. Finishing was done at Los Alamos National Laboratory. Annotation was done at Oak Ridge National Laboratory and JGI. The complete genome sequence was finished in September, 2008 and was released to the public in GenBank in February, 2009. A summary of the project information is shown in Table 2.
Table 1

Classification and general features of Halorubrum lacusprofundi ACAM 34T [31]

MIGS ID

Property

Term

Evidence codea

 

Classification

Domain

Archaea

TAS [32]

 

Phylum

Euryarchaeota

TAS [33, 34]

 

Class

Halobacteria

TAS [35]

 

Order

Halobacteriales

TAS [36]

 

Family

Halobacteriaceae

TAS [37]

 

Genus

Halorubrum

TAS [3]

 

Species

Halorubrum lacusprofundi

TAS [1]

 

Gram stain

Unknown

 
 

Cell shape

Pleomorphic

TAS [1]

 

Motility

Non-motile

TAS [1]

 

Sporulation

Nonsporulating

NAS

 

Temperature range

−1–40 °C

TAS [1]

 

Optimum temperature

36 °C

TAS [1]

 

pH range, optimum

Unknown

 
 

Carbon source

Sugars, organic acids, ethanol

TAS [1]

MIGS-6

Habitat

Saline lake

TAS [1]

MIGS-6.3

Salinity

10–25 % NaCl

TAS [1]

MIGS-22

Oxygen requirement

Aerobic

TAS [1]

MIGS-15

Biotic relationship

Free-living

TAS [1]

MIGS-14

Pathogenicity

Non-pathogen

NAS

MIGS-4

Geographic location

Deep Lake, Antarctica

TAS [1]

MIGS-5

Sample collection

1988

TAS [1]

MIGS-4.1 MIGS-4.2

Latitude-Longitude

Unknown

 

MIGS-4.4

Altitude

Unknown

 

aEvidence 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 [38]

Table 2

Project information

MIGS ID

Property

Term

MIGS-31

Finishing quality

Finished

MIGS-28

Libraries Used

3 kb, 8 kb, and fosmid DNA

MIGS-29

Sequencing platforms

ABI3730

MIGS-31.2

Fold coverage

12.5×

 

Sequencing quality

Less than one error per 50 kb

MIGS-30

Assemblers

Phrap

MIGS-32

Gene calling method

CRITICA, GLIMMER, GenePRIMP

 

Locus tag

Hlac

 

GenBank IDs

CP001365, CP001366, CP001367

 

GenBank date of release

February 4, 2009

 

GOLD ID

Gc00952

 

BIOPROJECT

PRJNA18455

 

NCBI project ID

18455

 

IMG Taxon ID

643692025

MIGS-13

Source material identifier

ATCC 49239, DSM 5036

 

Project relevance

Tree of Life, cold adaptation

Growth conditions and genomic DNA preparation

H. lacusprofundi ATCC 49239 was grown in Franzmann medium (180 g NaCl, 75 g MgCl2 · 6H2O, 7.4 g MgSO4 · 7H2O, 7.4 g KCl, 1 g CaCl2 · 2H2O, 10 g C4H4O4Na2 · 6H2O per liter, pH 7.4 with addition of 10 ml vitamin solution) [1]. The vitamin solution contained 0.1 g biotin, 0.1 g cyanocobalamin, and 0.1 g thiamine HCl per liter. Cells were grown with shaking at 220 rpm at 4 °C with illumination.

The DNA extraction method was modified from [9]. Cells were grown to OD600 = 0.8, collected by centrifugation at 8000 rpm for 10 min at 4 °C, resuspended in 1/20 volume basal salts and lysed by addition of 2 volumes of deionized water and mixing at room temperature. Next, proteinase K was added to a final concentration of 100 μg/ml, mixed gently, and incubated for 1 h at 37 °C. The lysate was extracted using an equal volume of phenol, mixed gently by inverting at room temperature for 5 min, and then spinning at 8000 g for 15 min at 4 °C. The aqueous and interphase was collected and the phenol extraction was repeated twice more. The aqueous and interphase were then dialyzed against TE overnight at 4 °C with one change of buffer. The dialyzed solution was collected and RNase A was added to a final concentration of 50 μg/ml, the solution was mixed and incubated for 2 h at 37 °C with gentle shaking. Proteinase K was added to a final concentration of 100 μg/ml, mixed and incubated for an additional hour at 37 °C. The RNase A and proteinase K steps were repeated. The DNA was then dialyzed overnight against TE at 4 °C with one buffer change.

Genome sequencing and assembly

The genome of H. lacusprofundi was sequenced at the Joint Genome Institute using a combination of 3 kb, 8 kb, and fosmid DNA libraries. All general aspects of library construction and sequencing were performed at the JGI [10]. Draft assemblies were based on 40,800 total reads. All libraries provided 12.5× coverage. The Phred/Phrap/Consed software package was used for sequence assembly and quality assessment [1113]. After the shotgun stage, reads were assembled with parallel phrap (High Performance Software, LLC). Possible mis-assemblies were corrected with Dupfinisher [14] or transposon bombing of bridging clones (Epicentre Biotechnologies, Madison, WI). Gaps between contigs were closed by editing in Consed, custom primer walk or PCR amplification (Roche Applied Science, Indianapolis, IN). A total of 1722 additional reactions were necessary to close gaps and to raise the quality of the finished sequence. The completed genome sequence of H. lacusprofundi contains 54,250 reads, achieving an average of 11.8× and 13.8× coverage in the chromosomes per base with an error rate of less than 1 in 50,000 bp.

Genome annotation

Protein-coding genes were identified using a combination of CRITICA [15] and Glimmer [16] followed by a round of manual curation using the JGI GenePRIMP pipeline [17]. GenePRIMP points out cases where gene start sites may be incorrect based on alignment with homologous proteins. It also highlights genes that appear to be broken into two or more pieces, due to a premature stop codon or frameshift, and genes that are disrupted by transposable elements. All of these types of broken and interrupted genes are labeled as pseudogenes. Genes that may have been missed by the gene calling programs are also identified in intergenic regions. The predicted CDSs were translated and used to search the National Center for Biotechnology Information nonredundant database, UniProt, TIGRFam, Pfam, PRIAM, KEGG, COG, and Interpro databases. Signal peptides were identified with SignalP [18], and transmembrane helices were determined with TMHMM [19]. CRISPR elements were identified with the CRISPR Recognition Tool [20]. Paralogs are hits of a protein against another protein within the same genome with an e-value of 10−2 or lower. The tRNAScanSE tool [21] was used to find tRNA genes. Additional gene prediction analysis and manual functional annotation was performed within the Integrated Microbial Genomes Expert Review (IMG-ER) [22] and HaloWeb [23] platform.

Genome properties

The genome of H. lacusprofundi consists of two chromosomes of length 2,735,295 bp (Chromosome 1) and 525,943 bp (Chromosome 2 or pHL500) and one plasmid of length 431,338 bp (pHL400) (Table 3). The map of the genome is available on HaloWeb [24]. Partial sequence was obtained from a second smaller plasmid, but it appeared to be present in a minority of the cells and its complete sequence could not be determined. The GC content of the large chromosome (67 %) is larger than those of the small chromosome (57 %) and the plasmid (55 %). There are 2801 genes on the large chromosome, 522 genes on the smaller chromosome, and 402 genes on the plasmid. Two of the ribosomal RNA operons are on the large chromosome and one is found on the smaller chromosome. The properties and statistics of the genome are summarized in Table 4, and genes belonging to COG functional categories are listed in Table 5.
Table 3

Summary of genome: two chromosomes and one plasmid

Label

Size (Mb)

Topology

INSDC identifier

RefSeq ID

Chromosome 1

2.74

circular

CP001365.1

NC012029.1

Chromosome 2 (pHL500)

0.53

circular

CP001366.1

NC012028.1

Plasmid (pHL400)

0.43

circular

CP001367.1

NC012030.1

Table 4

Genome statistics

Attribute

Value

% of Total

Genome size (bp)

3,692,576

100.00 %

DNA coding (bp)

3,199,417

86.64 %

DNA G + C (bp)

2,362,214

63.97 %

DNA scaffolds

3

 

Number of replicons

3

 

Extrachromosomal elements

1

 

Total genes

3725

100.00 %

Protein coding genes

3665

98.39 %

RNA genes

60

1.61 %

Pseudo genes

105

2.82 %

Genes in internal clusters

2009

53.93 %

Genes with function prediction

2143

57.53 %

Genes assigned to COGs

2226

59.76 %

Genes with Pfam domains

2162

58.04 %

Genes with signal peptides

396

10.63 %

Genes with transmembrane helices

779

20.91 %

CRISPR repeats

3

 
Table 5

Numbers of genes associated with the 25 general COG functional categories

Code

Value

% agea

Description

J

159

4.34

Translation, ribosomal structure and biogenesis

A

0

0.00

RNA processing and modification

K

136

3.71

Transcription

L

226

6.17

Replication, recombination and repair

B

4

0.11

Chromatin structure and dynamics

D

27

0.74

Cell cycle control, Cell division, chromosome partitioning

V

27

0.74

Defense mechanisms

T

104

2.84

Signal transduction mechanisms

M

68

1.86

Cell wall/membrane biogenesis

N

28

0.76

Cell motility

U

30

0.82

Intracellular trafficking and secretion

O

111

3.03

Posttranslational modification, protein turnover, chaperones

C

156

4.26

Energy production and conversion

G

113

3.08

Carbohydrate transport and metabolism

E

227

6.19

Amino acid transport and metabolism

F

73

1.99

Nucleotide transport and metabolism

H

122

3.33

Coenzyme transport and metabolism

I

62

1.69

Lipid transport and metabolism

P

146

3.98

Inorganic ion transport and metabolism

Q

33

0.90

Secondary metabolites biosynthesis, transport and catabolism

Z

0

0.00

Cytoskeleton

W

0

0.00

Extracellular structures

Y

0

0.00

Nuclear structure

R

362

9.88

General function prediction only

S

214

5.84

Function unknown

-

1439

39.26

Not in COGs

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

Conclusions

The Halorubrum lacusprofundi genome sequence is the first established from a cold-adapted haloarchaeon. The genome has features typical of halophilic Archaea, including high G + C-content, large extrachromosomal replicons, and eukaryotic-like DNA replication and transcription genes. Encoded proteins are highly acidic with properties that suggest looser packing and greater flexibility important for function at cold temperatures [2528]. H. lacusprofundi co-exists in a community of three major haloarchaea in Deep Lake, Antarctica [29, 30].

Abbreviations

TE: 

Tris-EDTA buffer

CRITICA: 

Coding region identification tool invoking comparative analysis

PRIAM: 

PRofils pour l’Identification Automatique du Métabolisme

KEGG: 

Kyoto Encyclopedia of Genes and Genomes

COG: 

Clusters of Orthologous Groups

TMHMM: 

Transmembrane hidden Markov model

CRISPR: 

Clustered regularly interspaced short palindromic repeats

Declarations

Acknowlegements

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. L. H. and M. L. were supported by the Department of Energy under contract DE-AC05-000R22725. P. D. and S. D. were supported by NASA grants NNX10AP47G and NNX15AM07G.

Authors’ contributions

All authors contributed to the generation, analysis and interpretation of the data and manuscript preparation. PD cultured the microbe and prepared the genomic DNA. CW conceived the project. IA led the genomics efforts and IA, PD and SD prepared the manuscript. All authors read and approved the final manuscript.

Competing interests

The authors declare that they have no competing interests.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
DOE Joint Genome Institute
(2)
Institute of Marine and Environmental Technology, Columbus Center, University of Maryland School of Medicine, University System of Maryland
(3)
DOE Joint Genome Institute, Los Alamos National Laboratory
(4)
Oak Ridge National Laboratory
(5)
School of Biotechnology and Biomolecular Sciences, The University of New South Wales
(6)
B103 Chemical and Life Sciences Laboratory, University of Illinois at Urbana-Champaign

References

  1. Franzmann PD, Stackebrandt E, Sanderson K, Volkman JK, Cameron DE, Stevenson PL, McMeekin TA, Burton HR. Halobacterium lacusprofundi sp. nov., a halophilic bacterium isolated from Deep Lake, Antarctica. Syst Appl Microbiol. 1988;11:20–7.View ArticleGoogle Scholar
  2. McGenity TJ, Grant WD. Transfer of Halobacterium saccharovorum, Halobacterium sodomense, Halobacterium trapanicum NRC 34021 and Halobacterium lacusprofundi to the genus Halorubrum gen. nov., as Halorubrum saccharovorum comb. nov., Halorubrum sodomense comb. nov., Halorubrum trapanicum comb. nov., and Halorubrum lacusprofundi comb. nov. Syst Appl Microbiol. 1995;18:237–43.View ArticleGoogle Scholar
  3. Kharroub K, Quesada T, Ferrer R, Fuentes S, Aguilera M, Boulahrouf A, Ramos-Cormenzana A, Monteoliva-Sánchez M. Halorubrum ezzemoulense sp. nov., a halophilic archaeon isolated from Ezzemoul sabkha, Algeria. Int J Syst Evol Microbiol. 2006;56:1583–8.View ArticlePubMedGoogle Scholar
  4. Cui H-L, Tohty D, Zhou P-J, Liu S-J. Halorubrum lipolyticum sp. nov. and Halorubrum aidingense sp. nov., isolated from two salt lakes in Xin-Jiang, China. Int J Syst Evol Microbiol. 2006;56:1631–4.View ArticlePubMedGoogle Scholar
  5. Pesenti PT, Sikaroodi M, Gillevet PM, Sánchez-Porro C, Ventosa A, Litchfield CD. Halorubrum californiense sp. nov., an extreme archaeal halophile isolated from a crystallizer pond at a solar salt plant in California, USA. Int J Syst Evol Microbiol. 2008;58:2710–5.View ArticlePubMedGoogle Scholar
  6. Mwatha WE, Grant WD. Natronobacterium vacuolata sp. nov., a haloalkaliphilic archaeon isolated from Lake Magadi, Kenya. Int J Syst Bacteriol. 1993;43:401–4.View ArticleGoogle Scholar
  7. Fan H, Xue Y, Ma Y, Ventosa A, Grant WD. Halorubrum tibetense sp. nov., a novel haloalkaliphilic archaeon from Lake Zabuye in Tibet, China. Int J Syst Evol Microbiol. 2004;54:1213–6.View ArticlePubMedGoogle Scholar
  8. Reid IN, Sparks WB, Lubow S, McGrath M, Livio M, Valenti J, Sowers KR, Shukla HD, MacAuley S, Miller T, Suvanasuthi R, Belas R, Colman A, Robb FT, DasSarma P, Müller JA, Coker JA, Cavicchioli R, Chen F, DasSarma S. Terrestrial models for extraterrestrial life: methanogens and halophiles at Martian temperatures. Int J Astrobiol. 2006;5:89–97.View ArticleGoogle Scholar
  9. DasSarma S, Fleischmann EM, Robb FT, Place AR, Sowers KR, Schreier HJ, editors. Archaea–A Laboratory Manual–Halophiles, Cold Spring Harbor. New York: Cold Spring Harbor Press; 1995.Google Scholar
  10. Joint Genome Institute, Our Projects. http://www.jgi.doe.gov/sequencing/protocols/prots_production.html. Accessed 27 Jun 2016.
  11. Ewing B, Green P. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res. 1998;8:186–94.View ArticlePubMedGoogle Scholar
  12. Ewing B, Hillier L, Wendl MC, Green P. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 1998;8:175–85.View ArticlePubMedGoogle Scholar
  13. Gordon D, Abajian C, Green P. Consed: a graphical tool for sequence finishing. Genome Res. 1998;8:195–202.View ArticlePubMedGoogle Scholar
  14. Han CS, Chain P. Finishing repeat regions automatically with Dupfinisher. In: Arabnia HR, Valafar H, editors. Proceedings of the 2006 international conference on bioinformatics & computational biology. Las Vegas: CSREA Press; 2006. p. 141–6.Google Scholar
  15. Badger JH, Olsen GJ. CRITICA: coding region identification tool invoking comparative analysis. Mol Biol Evol. 1999;16:512–24.View ArticlePubMedGoogle Scholar
  16. Delcher AL, Harmon D, Kasif S, White O, Salzberg SL. Improved microbial gene identification with GLIMMER. Nucleic Acids Res. 1999;27:4636–41.View ArticlePubMedPubMed CentralGoogle Scholar
  17. Pati A, Ivanova NN, Mikhailova N, Ovchinnikova G, Hooper SD, Lykidis A, Kyrpides NC. GenePRIMP: a gene prediction improvement pipeline for prokaryotic genomes. Nat Methods. 2010;7:455–7.View ArticlePubMedGoogle Scholar
  18. Emanuelsson O, Brunak S, von Heijne G, Nielsen H. Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc. 2007;2:953–71.View ArticlePubMedGoogle Scholar
  19. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 2001;305:567–80.View ArticlePubMedGoogle Scholar
  20. Bland C, Ramsey TL, Sabree F, Lowe M, Brown K, Kyrpides NC, Hugenholtz P. CRISPR recognition tool (CRT): a tool for automatic detection of clustered regularly interspaced palindromic repeats. BMC Bioinform. 2007;8:209.View ArticleGoogle Scholar
  21. Lowe TM, Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 1997;25:955–64.View ArticlePubMedPubMed CentralGoogle Scholar
  22. Markowitz VM, Mavromatis K, Ivanova NN, Chen IMA, Chu K, Kyrpides NC. IMG ER: a system for microbial genome annotation expert review and curation. Bioinform. 2009;25:2271–8.View ArticleGoogle Scholar
  23. DasSarma SL, Capes MD, DasSarma P, DasSarma S. HaloWeb: the haloarchaeal genomes database. Saline Sys. 2010;6:12.View ArticleGoogle Scholar
  24. Halorubrum lacusprofundi Genome. http://halo.umbc.edu/cgi-bin/haloweb/hla.pl?operation=map_query1. Accessed 27 Jun 2016.
  25. DasSarma S, DasSarma P. Halophiles and their enzymes: negativity put to good use. Curr Opin Microbiol. 2015;25:120–6.View ArticlePubMedPubMed CentralGoogle Scholar
  26. Karan R, Capes MD, DasSarma S. Function and biotechnology of extremophilic enzymes in low water activity. Aquat Biosyst. 2012;8:4. doi:10.1186/2046-9063-8-4.View ArticlePubMedPubMed CentralGoogle Scholar
  27. Karan R, Capes MD, DasSarma P, DasSarma S. Cloning, overexpression, purification, and characterization of a polyextremophilic β-galactosidase from the Antarctic haloarchaeon Halorubrum lacusprofundi. BMC Biotechnol. 2013;13:3.View ArticlePubMedPubMed CentralGoogle Scholar
  28. DasSarma S, Capes MD, Karan R, DasSarma P. Amino acid substitutions in cold-adapted proteins from Halorubrum lacusprofundi, an extremely halophilic microbe from antarctica. PLoS One. 2013;8:e58587.View ArticlePubMedPubMed CentralGoogle Scholar
  29. Williams TJ, Allen MA, DeMaere MZ, Kyrpides NC, Tringe SG, Woyke T, Cavicchioli R. Microbial ecology of an Antarctic hypersaline lake: genomic assessment of ecophysiology among dominant haloarchaea. ISME J. 2014;8:1645–58. Erratum in: ISME J. 2014;8:1752.View ArticlePubMedPubMed CentralGoogle Scholar
  30. Tschitschko B, Williams TJ, Allen MA, Zhong L, Raftery MJ, Cavicchioli R. Ecophysiological Distinctions of Haloarchaea from a Hypersaline Antarctic Lake as Determined by Metaproteomics. Appl Environ Microbiol. 2016;82:3165–73.View ArticlePubMedGoogle Scholar
  31. 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;26:541–7.View ArticlePubMedPubMed CentralGoogle Scholar
  32. Woese CR, Kandler O, Wheelis ML. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A. 1990;87:4576–9.View ArticlePubMedPubMed CentralGoogle Scholar
  33. Garrity GM, Holt JG. Phylum AII. Euryarchaeota phy. nov. In: Boone DR, Castenholz RW, Garrity GM, editors. Bergey’s Manual of Systematic Bacteriology, vol. 1. 2nd ed. New York: Springer; 2001. p. 211–355.View ArticleGoogle Scholar
  34. 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;52:685–90.Google Scholar
  35. Grant WD, Kamekura M, McGenity TJ, Ventosa A. Class III. Halobacteria class. nov. In: Boone DR, Castenholz RW, Garrity GM, editors. Bergey’s Manual of Systematic Bacteriology, vol. 1. 2nd ed. New York: Springer; 2001. p. 294–334.Google Scholar
  36. Grant WD, Larsen H. Group III. Extremely halophilic archaeobacteria. Order Halobacteriales ord. nov. In: Staley JT, Bryant MP, Pfennig N, Holt JG, editors. Bergey’s Manual of Systematic Bacteriology, vol. 3. 1st ed. Baltimore: The Williams & Watkins Co; 1989. p. 2216–28.Google Scholar
  37. Gibbons NE. Family V. Halobacteriaceae fam. nov. In: Bergey’s Manual of Determinative Bacteriology. 8th ed. Baltimore: The Williams & Watkins Co; 1974. p. 279.Google Scholar
  38. 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;25:25–9.View ArticlePubMedPubMed CentralGoogle Scholar
  39. 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;22:4673–80.View ArticlePubMedPubMed CentralGoogle Scholar
  40. Perrière G, Gouy M. WWW-Query: an on-line retrieval system for biological sequence banks. Biochim. 1996;78:364–9.View ArticleGoogle Scholar

Copyright

© The Author(s). 2016