Open Access

Complete genome sequence of the moderate thermophile Anaerobaculum mobile type strain (NGAT)

  • Konstantinos Mavromatis1,
  • Erko Stackebrandt2,
  • Brittany Held1, 3,
  • Alla Lapidus1,
  • Matt Nolan1,
  • Susan Lucas1,
  • Nancy Hammon1, 3,
  • Shweta Deshpande1, 3,
  • Jan-Fang Cheng1,
  • Roxanne Tapia1, 3,
  • Lynne A. Goodwin1, 3,
  • Sam Pitluck1,
  • Konstantinos Liolios1,
  • Ioanna Pagani1,
  • Natalia Ivanova1,
  • Natalia Mikhailova1,
  • Marcel Huntemann1,
  • Amrita Pati1,
  • Amy Chen4,
  • Krishna Palaniappan4,
  • Miriam Land1, 5,
  • Manfred Rohde6,
  • Stefan Spring2,
  • Markus Göker2,
  • Tanja Woyke1,
  • John C. Detter3,
  • James Bristow1,
  • Jonathan A. Eisen1, 7,
  • Victor Markowitz4,
  • Philip Hugenholtz1, 8,
  • Hans-Peter Klenk2 and
  • Nikos C. Kyrpides1
Standards in Genomic Sciences20138:8010047

https://doi.org/10.4056/sigs.3547050

Published: 15 April 2013

Abstract

Anaerobaculum mobile Menes and Muxí 2002 is one of three described species of the genus Anaerobaculum, family Synergistaceae, phylum Synergistetes. This anaerobic and motile bacterium ferments a range of carbohydrates and mono- and dicarboxylic acids with acetate, hydrogen and CO2 as end products. A. mobile NGAT is the first member of the genus Anaerobaculum and the sixth member of the phylum Synergistetes with a completely sequenced genome. Here we describe the features of this bacterium, together with the complete genome sequence, and annotation. The 2,160,700 bp long single replicon genome with its 2,053 protein-coding and 56 RNA genes is part of the Genomic Encyclopedia of Bacteria and Archaea project.

Keywords

Gram-negativerod-shapedmotileflagellumnon-spore forminganaerobicchemoorganotrophiccrotonate-reducer Synergistetes Synergistaceae GEBA

Introduction

Strain NGAT (= DSM 13181 = ATCC BAA-54 = JCM 12221) is the type strain of Anaerobaculum mobile [1]. The genus, described for a thermophilic, citrate-fermenting anaerobe with A. thermoterrenum as the type species [2], was emended twice [1,3]. The third species is the recently described A. hydrogeniformans, forming H2 and acetate from glucose [3] while the other two species form CO2. A. mobile was isolated from a 10−7 dilution of an oleic acid-degrading consortium, originating from the sludge of a wool-scouring wastewater. Enrichment was performed in BCYT medium (basal BC medium [4] with tryptone and yeast extract), supplemented with crotonate [1]. Here we present a summary classification and a set of features for A. mobile NGAT together with the description of the complete genomic sequencing and annotation.

Classification and features

16S rRNA gene sequence analysis

A representative genomic 16S rRNA gene sequence of A. mobile NGAT was compared using NCBI BLAST [5,6] under default settings (e.g., considering only the high-scoring segment pairs (HSPs) from the best 250 hits) with the most recent release of the Greengenes database [7] and the relative frequencies of taxa and keywords (reduced to their stem [8]) were determined, weighted by BLAST scores. The most frequently occurring genera were Anaerobaculum (81.9%), Acetomicrobium (9.9%), Thermovirga (4.5%) and Dethiosulfovibrio (3.6%) (12 hits in total). Regarding the two hits to sequences from members of the species, the average identity within HSPs was 99.9%, whereas the average coverage by HSPs was 100.0%. Regarding the seven hits to sequences from other members of the genus, the average identity within HSPs was 97.1%, whereas the average coverage by HSPs was 99.1%. Among all other species, the one yielding the highest score was Acetomicrobium flavidum (FR733692), which corresponded to an identity of 99.8% and an HSP coverage of 100.0%. (Note that the Greengenes database uses the INSDC (= EMBL/NCBI/DDBJ) annotation, which is not an authoritative source for nomenclature or classification.) The highest-scoring environmental sequence was FN436106 (Greengenes name ‘Molekularbiologische Charakterisierung der bakteriellen Populationsdynamik eines thermophil betriebenen Biogasfermenters zur Vergaerung nachwachsender Rohstoffe thermophilic biogas reactor fed renewable biomass clone HAW-R60-B-745d-BC’), which showed an identity of 99.9% and an HSP coverage of 99.9%. The most frequently occurring keywords within the labels of all environmental samples which yielded hits were ‘digest’ (7.0%), ‘anaerob’ (4.6%), ‘thermophil’ (4.3%), ‘microbi’ (3.4%) and ‘mesophil’ (3.3%) (238 hits in total). The most frequently occurring keywords within the labels of those environmental samples which yielded hits of a higher score than the highest scoring species were ‘thermophil’ (12.3%), ‘reactor’ (8.8%), ‘bioga, fed’ (7.0%), ‘bakteriellen, betriebenen, biogasferment, biomass, charakterisierung, molekularbiologisch, nachwachsend, populationsdynamik, renew, rohstoff, vergaerung’ (5.3%) and ‘corn, microbi, silag, structur’ (1.8%) (4 hits in total).

A. flavidum is a species that was originally described without 16S rRNA gene sequencing [9]. The sequence FR733692 was only recently been generated by DSMZ staff in the course of the Living-Tree Project [10], yielding an unexpected placement of the species within the Synergistetes. An assessment of whether a contamination or confusion of strains has occurred, or whether the currently available culture deposits are biologically identical to the original description but the classification of A. flavidum needs to be revised. This work is currently in progress. (R. Pukall (DSMZ), personal communication).

Figure 1 shows the phylogenetic neighborhood of A. mobile in a 16S rRNA gene based tree. The sequences of the two identical 16S rRNA gene copies in the genome differ by one nucleotide from the previously published 16S rRNA gene sequence (AJ243189).
Figure 1.

Phylogenetic tree highlighting the position of A. mobile relative to the type strains of the other species within the phylum ‘Synergistetes’. The tree was inferred from 1,360 aligned characters [11,12] of the 16S rRNA gene sequence under the maximum likelihood (ML) criterion [13]. Rooting was done initially using the midpoint method [14] and then checked for its agreement with the current classification (Table 1). The branches are scaled in terms of the expected number of substitutions per site. Numbers adjacent to the branches are support values from 1,000 ML bootstrap replicates [15] (left) and from 1,000 maximum-parsimony bootstrap replicates [16] (right) if larger than 60%. Lineages with type strain genome sequencing projects registered in GOLD [17] are labeled with one asterisk, those also listed as ‘Complete and Published’ with two asterisks [1820]; the non-contiguous finished draft genomes of Aminomonas paucivorans [21] and Dethiosulfovibrio peptidovorans [22] lack the second asterisk.

Morphology and physiology

The Gram-negative rod-shaped cells of A. mobile are straight (0.5–1.0 × 2.0–4.0 µm; Figure 2), occurring singly or, predominantly in the exponential growth phase, in pairs. Longer cells (4.0-8.0 µm) are observed in older cultures. Spores or sheath formation were never observed. Cells are moderately thermophilic; motile by means of a single flagellum inserted in the lateral region of the cell. On BCTC agar, colonies (1.0–1.5 mm in diameter) are white, lens shaped and with entire margins. Temperature and pH range for growth is between 35–65°C (optimum between 55 and 60°C) and between 5.4 and 8.7 (optimum between 6.6 and 7.3), respectively. Growth occurs at NaCl concentrations of up to 1.5%, with an optimum of 0.8%.
Figure 2.

Scanning electron micrograph of A. mobile NGAT

Cells are strictly anaerobic, fermenting glucose, organic acids (pyruvate, tartrate and malate) and glycerol to acetate, H2 and, presumably, CO2 (the authors of [1] assumed that 2 mol CO2 was produced per mol glucose, tartrate and malate degraded, and 1 mol CO2 was produced per mol pyruvate and glycerol degraded). Gluconate, L-malate, glycerol, tryptone, L-arginine, L-leucin, L-phenylalanine and starch are utilized [3]. No growth occurs on citrate, 2-oxoglutarate, glutamate, mannose, pectin, lactose, xylose, galactose, maltose, sucrose, rhamnose, raffinose, malonate, lactate, succinate, xylan, dextrin, inulin, melibiose, adonitol, cellobiose, arabinose, polygalacturonate, cellulose, gelatin, butyrate or oleate [1], nor lactate, maltose, malonate, mannose, inositol and inulin [3].

In co-culture with Methanothermobacter thermautotrophicus glucose and malate degradation were enhanced. Crotonate is not fermented but used as an electron acceptor, reducing it to butyrate in the presence of yeast extract and tryptone, glucose, Casamino acids and leucine. Fumarate, acetate, sulfate, sulfite and nitrate are not used as electron acceptors in PY broth. The addition of crotonate, sulfur, cystine and thiosulfate enhances growth from tryptone and yeast extract, Casamino acids and glucose, as indicated by an increase in OD and by the production of reduction compounds (butyrate and sulfide, respectively) [1].

Chemotaxonomy

The cell wall is of the Gram-negative type as judged by transmission electron micrography [1]. Polar lipid composition includes diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine, three unknown phospholipids and four unknown aminophospholipids [3]. Major fatty acids (>20%) are iso-C15:0 and iso-C11:0; iso-C13:0 3-OH is found in smaller amounts (<10%) [3]. The DNA G+C content was previously reported with 51.5 mol% [1].

Genome sequencing and annotation

Genome project history

This organism was selected for sequencing on the basis of its phylogenetic position [29], and is part of the Genomic Encyclopedia of Bacteria and Archaea project [30]. The genome project is deposited in the Genomes On Line Database [17] and the complete genome sequence is deposited in GenBank. Sequencing, finishing and annotation were performed by the DOE Joint Genome Institute (JGI) using state of the art sequencing technology [31]. A summary of the project information is shown in Table 2.
Table 1.

Classification and general features of A. mobile NGAT according to the MIGS recommendations [23].

MIGS ID

Property

Term

Evidence code

 

Current classification

Domain Bacteria

TAS [24]

 

Phylum Synergistetes

TAS [25]

 

Class Synergistia

TAS [25]

 

Order Synergistales

TAS [25]

 

Family Synergistaceae

TAS [25]

 

Genus Anaerobaculum

TAS [1,3,26]

 

SpeciesAnaerobaculum mobile

TAS [1]

MIGS-7

Subspecific genetic lineage (strain)

NGAT

TAS [1]

MIGS-12

Reference for biomaterial

Menes and Muxí 2002

TAS [1]

 

Gram stain

Gram-negative

TAS [1]

 

Cell shape

rod-shaped

TAS [1]

 

Motility

motile

TAS [1]

 

Sporulation

non-sporulating

TAS [1]

 

Temperature range

35–65°C

TAS [1]

 

Optimum temperature

55–60°C

TAS [1]

 

Salinity

optimum growth at 0.8%

TAS [1]

MIGS-22

Relationship to oxygen

obligate anaerobe

TAS [1]

 

Carbon source

organic acids and carbohydrates

NAS

 

Energy metabolism

chemoorganotroph

TAS [1]

MIGS-6

Habitat

wastewater

TAS [1]

MIGS-6.2

pH

optimum 6.6 – 7.3

TAS 19]

MIGS-15

Biotic relationship

free living

TAS [1]

MIGS-14

Known pathogenicity

none

TAS [1]

MIGS-16

Specific host

not reported

 

MIGS-14

Biosafety level

1

TAS [27]

MIGS-19

Trophic level

not reported

 

MIGS-23.1

Isolation

wool-scouring wastewater treatment lagoon

TAS [1]

MIGS-4

Geographic location

Trinidad, Uruguay

TAS [1]

MIGS-5

Time of sample collection

November 1998 or earlier

NAS

MIGS-4.1

Latitude

−33.506

TAS [1]

MIGS-4.2

Longitude

−56.889

TAS [1]

MIGS-4.3

Depth

not reported

 

MIGS-4.4

Altitude

not reported

 

Evidence codes - 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). Evidence codes are from of the Gene Ontology project [28].

Table 2.

Genome sequencing project information

MIGS ID

Property

Term

MIGS-31

Finishing quality

Finished

MIGS-28

Libraries used

Three genomic libraries: one 454 pyrosequence standard library, one 454 PE libraries (11.0 kb insert size), one Illumina library

MIGS-29

Sequencing platforms

Illumina GAii, 454 GS FLX Titanium

MIGS-31.2

Sequencing coverage

1,109.0 × Illumina; 38.3 × pyrosequence

MIGS-30

Assemblers

Newbler version 2.3-PreRelease-6/30/2009, Velvet version 1.0.13, phrap version SPS - 4.24

MIGS-32

Gene calling method

Prodigal 1.4, GenePRIMP

 

INSDC ID

CP003198

 

GenBank Date of Release

June 14, 2012

 

GOLD ID

Gc02248

 

NCBI project ID

53351

 

Database: IMG

2509601011

MIGS-13

Source material identifier

DSM 13181

 

Project relevance

Tree of Life, GEBA

Growth conditions and DNA isolation

A mobile strain NGAT, DSM 13181, was grown anaerobically in DSMZ medium 104b (PYX, medium) at 55°C. DNA was isolated from 1–1.5 g of cell paste using a Jetflex Genomic DNA Purification Kit (GENOMED 600100) and following the standard protocol as recommended by the manufacturer with modification (an additional 10 µl proteinase K digestion for cell lysis was added; 40 min incubation at 58°C). DNA is available through the DNA Bank Network [32].

Genome sequencing and assembly

The genome was sequenced using a combination of Illumina and 454 sequencing platforms. All general aspects of library construction and sequencing can be found at the JGI website [33]. Pyrosequencing reads were assembled using the Newbler assembler (Roche). The initial Newbler assembly, consisting of 31 contigs in one scaffold, was converted into a phrap [34] assembly by making fake reads from the consensus, to collect the read pairs in the 454 paired end library. Illumina GAii sequencing data (2,649.5 Mb) was assembled with Velvet [35] and the consensus sequences were shredded into 1.5 kb overlapped fake reads and assembled together with the 454 data. The 454 draft assembly was based on 113.8 Mb 454 draft data and all of the 454 paired end data. Newbler parameters are -consed -a 50 -l 350 -g -m -ml 20. The Phred/Phrap/Consed software package [34] was used for sequence assembly and quality assessment in the subsequent finishing process. After the shotgun stage, reads were assembled with parallel phrap (High Performance Software, LLC). Possible mis-assemblies were corrected with gapResolution [33], Dupfinisher [36], or sequencing cloned bridging PCR fragments with subcloning. Gaps between contigs were closed by editing in Consed, by PCR and by Bubble PCR primer walks (J.-F. Chang, unpublished). A total of 68 additional reactions and 3 shatter libraries were necessary to close gaps and to raise the quality of the finished sequence. Illumina reads were also used to correct potential base errors and increase consensus quality using a software Polisher developed at JGI [37]. The error rate of the completed genome sequence is less than 1 in 100,000. Together, the combination of the Illumina and 454 sequencing platforms provided 1147.3 × coverage of the genome. The final assembly contained 237,629 pyrosequence and 32,103,764 Illumina reads.

Genome annotation

Genes were identified using Prodigal [38] as part of the DOE-JGI genome annotation pipeline [39], followed by a round of manual curation using the JGI GenePRIMP pipeline [40]. The predicted CDSs were translated and used to search the National Center for Biotechnology Information (NCBI) non-redundant 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 (IMG-ER) platform [41].

Genome properties

The genome statistics are provided in Table 3 and Figure 3. The genome consists of one chromosome with a total length of 2,160,700 bp and a G+C content of 48.0%. Of the 2,109 genes predicted, 2,053 were protein-coding genes, and 56 RNAs; 34 pseudogenes were also identified. The majority of the protein-coding genes (85.7%) were assigned a putative function while the remaining ones were annotated as hypothetical proteins. The distribution of genes into COGs functional categories is presented in Table 4.
Figure 3.

Graphical 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 (purple/olive).

Table 3.

Genome Statistics

Attribute

Number

% of Total

Genome size (bp)

2,160,700

100.00

DNA coding region (bp)

1,982,774

91.77

DNA G+C content (bp)

1,036,446

47.97

Number of replicons

1

 

Extrachromosomal elements

0

 

Total genes

2,109

100.00

RNA genes

56

2.66

rRNA operons

2

 

tRNA genes

48

2.28

Protein-coding genes

2,053

97.34

Pseudo genes

34

1.61

Genes with function prediction

1,808

85.73

Genes in paralog clusters

881

41.77

Genes assigned to COGs

1,796

85.16

Genes assigned Pfam domains

1,809

85.78

Genes with signal peptides

276

13.09

Genes with transmembrane helices

487

23.09

CRISPR repeats

3

 
Table 4.

Number of genes associated with the general COG functional categories

Code

Value

%age

Description

J

149

7.51

Translation, ribosomal structure and biogenesis

A

0

0.00

RNA processing and modification

K

86

4.34

Transcription

L

102

5.14

Replication, recombination and repair

B

0

0.00

Chromatin structure and dynamics

D

31

1.56

Cell cycle control, cell division, chromosome partitioning

Y

0

0.00

Nuclear structure

V

16

0.81

Defense mechanisms

T

56

2.82

Signal transduction mechanisms

M

117

5.90

Cell wall/membrane/envelope biogenesis

N

63

3.18

Cell motility

Z

0

0.00

Cytoskeleton

W

0

0.00

Extracellular structures

U

41

2.07

Intracellular trafficking, secretion, and vesicular transport

O

61

3.08

Posttranslational modification, protein turnover, chaperones

C

176

8.88

Energy production and conversion

G

131

6.61

Carbohydrate transport and metabolism

E

263

13.26

Amino acid transport and metabolism

F

69

3.48

Nucleotide transport and metabolism

H

85

4.29

Coenzyme transport and metabolism

I

34

1.71

Lipid transport and metabolism

P

92

4.64

Inorganic ion transport and metabolism

Q

36

1.82

Secondary metabolites biosynthesis, transport and catabolism

R

218

10.99

General function prediction only

S

157

7.92

Function unknown

-

313

14.84

Not in COGs

Declarations

Acknowledgements

We would like to gratefully acknowledge the help of Maren Schröder for growing A. mobile cultures, Evelyne-Marie Brambilla for DNA extraction and quality control, and Cathrin Spröer and Rüdiger Pukall for helpful comments (all at DSMZ). This work was performed under the auspices of the US Department of Energy 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, UT-Battelle and Oak Ridge National Laboratory under contract DE-AC05-00OR22725.

Authors’ Affiliations

(1)
DOE Joint Genome Institute
(2)
Leibniz-Institute, DSMZ - German Collection of Microorganisms and Cell Cultures
(3)
Bioscience Division, Los Alamos National Laboratory
(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
(8)
Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland

References

  1. Menes RJ, Muxi L. Anaerobaculum mobile sp. nov., a novel anaerobic, moderately thermophilic, peptide-fermenting bacterium that uses crotonate as an electron acceptor, and emended description of the genus Anaerobaculum. Int J Syst Evol Microbiol 2002; 52:157–164. PubMedView ArticlePubMedGoogle Scholar
  2. Rees GN, Pater BKC, Grassia GS, Sheehy AJ. Anaerobaculum thermoterrenum gen. nov., sp. nov., a novel, thermophilic bacterium which ferments citrate. Int J Syst Bacteriol 1997; 47:150–154. PubMed http://dx.doi.org/10.1099/00207713-47-1-150View ArticlePubMedGoogle Scholar
  3. Maune, MW, Tanner, RS 2012Description of Anaerobaculum hydrogeniformans sp. nov., an anaerobe that produces hydrogen from glucose, and emended description of the genus AnaerobaculumInt J Syst Evol Microbiol62832838PubMedView ArticlePubMedGoogle Scholar
  4. Touzel JP, Albagnac G. Isolation and characterization of Methanococcus mazeii strain MC3. FEMS Microbiol Lett 1983; 16:241–245. http://dx.doi.org/10.1111/j.15746968.1983.tb00295.xView ArticleGoogle Scholar
  5. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410. PubMedView ArticlePubMedGoogle Scholar
  6. Korf I, Yandell M, Bedell J. BLAST, O’Reilly, Sebastopol, 2003.Google Scholar
  7. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 2006; 72:5069–5072. PubMed http://dx.doi.org/10.1128/AEM.03006-05PubMed CentralView ArticlePubMedGoogle Scholar
  8. Porter MF. An algorithm for suffix stripping. Program: electronic library and information systems 1980; 14:130–137.View ArticleGoogle Scholar
  9. Soutschek E, Winter J, Schindler F, Kandler O. Acetomicrobium flavidum, gen. nov., sp. nov., a thermophilic, anaerobic bacterium from sewage sludge, forming acetate, CO2 and H2 from glucose. Syst Appl Microbiol 1984; 5:377–390. http://dx.doi.org/10.1016/S0723-2020(84)80039-9View ArticleGoogle Scholar
  10. Munoz R, Yarza P, Ludwig W. Euzéby, Amann R, Schleifer K-H, Glöckner FO, Rossellö-Möra R. Release LTPs104 of the All-Species Living Tree. Syst Appl Microbiol 2011; 34:169–170. PubMed http://dx.doi.org/10.1016/j.syapm.2011.03.001View ArticlePubMedGoogle Scholar
  11. Lee C, Grasso C, Sharlow MF. Multiple sequence alignment using partial order graphs. Bioinformatics 2002; 18:452–464. PubMed http://dx.doi.org/10.1093/bioinformatics/18.3.452View ArticlePubMedGoogle Scholar
  12. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000; 17:540–552. PubMed http://dx.doi.org/10.1093/oxfordjournals.molbev.a 026334View ArticlePubMedGoogle Scholar
  13. Stamatakis A, Hoover P, Rougemont J. A rapid bootstrap algorithm for the RAxML web-servers. Syst Biol 2008; 57:758–771. PubMed http://dx.doi.org/10.1080/10635150802429642View ArticlePubMedGoogle Scholar
  14. Hess PN, De Moraes Russo CA. An empirical test of the midpoint rooting method. Biol J Linn Soc Lond 2007; 92:669–674. http://dx.doi.org/10.1111/j.10958312.2007.00864.xView ArticleGoogle Scholar
  15. 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. http://dx.doi.org/10.1007/978-3-642-02008-7_13View ArticleGoogle Scholar
  16. Swofford DL. PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4.0 b10. Sinauer Associates, Sunderland, 2002.Google Scholar
  17. Pagani I, Liolios K, Jansson J, Chen IM, 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:D571–D579. PubMed http://dx.doi.org/10.1093/nar/gkr1100PubMed CentralView ArticlePubMedGoogle Scholar
  18. Chovatia M, Sikorski J, Schröder M, Lapidus A, Nolan M, Tice H, Del Rio TG, Copeland A, Cheng JF, Lucas S, et al. Complete genome sequence of Thermanaerovibrio acidaminovorans type strain (Su883T). Stand Genomic Sci 2009; 1:254–261. PubMed http://dx.doi.org/10.4056/sigs.40645PubMed CentralView ArticlePubMedGoogle Scholar
  19. Göker M, Saunders E, Lapidus A, Nolan M, Lucas S, Hammon N, Deshpande S, Cheng JF, Han C, Tapia R, et al. Genome sequence of the moderately thermophilic, amino-acid-degrading and sulfur-reducing bacterium Thermovirga lienii type strain (Cas60314T). Stand Genomic Sci 2012; 6:230–239. PubMed http://dx.doi.org/10.4056/sigs.2726028PubMed CentralView ArticlePubMedGoogle Scholar
  20. Chertkov O, Sikorski J, Brambilla E, Lapidus A, Copeland A, Del Rio TG, Nolan M, Lucas S, Chen F, Tice H, et al. Complete genome sequence of Aminobacterium colombiense type strain (ALA-1T). Stand Genomic Sci 2010; 2:280–289. PubMed http://dx.doi.org/10.4056/sigs.902116PubMed CentralView ArticlePubMedGoogle Scholar
  21. Pitluck S, Yasawong M, Held B, Lapidus A, Nolan M, Copeland A, Lucas S, Del Rio TG, Tice H, Cheng JF, et al. Non-contiguous finished genome sequence of Aminomonas paucivorans type strain (GLU-3T). Stand Genomic Sci 2009; 3:285–293. http://dx.doi.org/10.4056/sigs.1253298View ArticleGoogle Scholar
  22. LaButti K, Mayilraj S, Clum A, Lucas S, Del Rio TG, Nolan M, Tice H, Cheng JF, Pitluck S, Liolios K, et al. Permanent draft genome sequence of Dethiosulfovibrio peptidovorans type strain (SEBR 4207T). Stand Genomic Sci 2010; 3:85–92. PubMed http://dx.doi.org/10.4056/sigs.1092865PubMed CentralView ArticlePubMedGoogle Scholar
  23. 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 http://dx.doi.org/10.1038/nbt1360PubMed CentralView ArticlePubMedGoogle Scholar
  24. 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
  25. Jumas-Bilak E, Roudière L, Marchandin H. Description of ‘Synergistetes’ phyl. nov. and emended description of the phylum ‘Deferribacteres’ and of the family Syntrophomonadaceae, phylum ‘Firmicutes’. Int J Syst Evol Microbiol 2009; 59:1028–1035. PubMed http://dx.doi.org/10.1099/ijs.0.006718-0View ArticlePubMedGoogle Scholar
  26. Rees GN, Patel BKC, Grassia GS, Sheehy AJ. Anaerobaculum thermoterrenum gen. nov., sp. nov., a novel, thermophilic bacterium which ferments citrate. Int J Syst Bacteriol 1997; 47:150–154. PubMed http://dx.doi.org/10.1099/00207713-47-1-150View ArticlePubMedGoogle Scholar
  27. BAuA. 2010, Classification of bacteria and archaea in risk groups. http://www.baua.de TRBA 466, p. 24.
  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 http://dx.doi.org/10.1038/75556PubMed CentralView ArticlePubMedGoogle Scholar
  29. Klenk HP, Göker M. En route to a genome-based classification of Archaea and Bacteria? Syst Appl Microbiol 2010; 33:175–182. PubMed http://dx.doi.org/10.1016/j.syapm.2010.03.003View ArticlePubMedGoogle Scholar
  30. Wu D, Hugenholtz P, Mavromatis K, Pukall R, Dalin E, Ivanova NN, Kunin V, Goodwin L, Wu M, Tindall BJ, et al. A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature 2009; 462:1056–1060. PubMed http://dx.doi.org/10.1038/nature08656PubMed CentralView ArticlePubMedGoogle Scholar
  31. Mavromatis K, Land ML, Brettin TS, Quest DJ, Copeland A, Clum A, Goodwin L, Woyke T, Lapidus A, Klenk HP, et al. The fast changing landscape of sequencing technologies and their impact on microbial genome assemblies and annotation. PLoS ONE 2012; 7:e48837;. PubMed http://dx.doi.org/10.1371/journal.pone.0048837PubMed CentralView ArticlePubMedGoogle Scholar
  32. Gemeinholzer B, Dröge G, Zetzsche H, Haszprunar G, Klenk HP, Güntsch A, Berendsohn WG, Wägele JW. The DNA Bank Network: the start from a German initiative. Biopreserv Biobank 2011; 9:51–55. http://dx.doi.org/10.1089/bio.2010.0029View ArticlePubMedGoogle Scholar
  33. JGI website. http://www.jgi.doe.gov
  34. The Phred/Phrap/Consed software package. http://www.phrap.com
  35. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 2008; 18:821–829. PubMed http://dx.doi.org/10.1101/gr.074492.107PubMed CentralView ArticlePubMedGoogle Scholar
  36. Han C, Chain P. Finishing repeat regions automatically with Dupfinisher. In: Proceeding of the 2006 international conference on bioinformatics & computational biology. Arabnia HR, Valafar H (eds), CSREA Press. June 26–29, 2006: 141–146.Google Scholar
  37. Lapidus A, LaButti K, Foster B, Lowry S, Trong S, Goltsman E. POLISHER: An effective tool for using ultra short reads in microbial genome assembly and finishing. AGBT, Marco Island, FL, 2008.Google Scholar
  38. Hyatt D, Chen GL, LoCascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 2010; 11:119. PubMed http://dx.doi.org/10.1186/1471-2105-11-119PubMed CentralView ArticlePubMedGoogle Scholar
  39. Mavromatis K, Ivanova NN, Chen IM, Szeto E, Markowitz VM, Kyrpides NC. The DOE-JGI Standard operating procedure for the annotations of microbial genomes. Stand Genomic Sci 2009; 1:63–67. PubMed http://dx.doi.org/10.4056/sigs.632PubMed CentralView ArticlePubMedGoogle Scholar
  40. 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; 7:455–457. PubMed http://dx.doi.org/10.1038/nmeth.1457View ArticlePubMedGoogle Scholar
  41. 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 http://dx.doi.org/10.1093/bioinformatics/btp393View ArticlePubMedGoogle Scholar

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