Open Access

Complete genome sequence of Granulicella tundricola type strain MP5ACTX9T, an Acidobacteria from tundra soil

  • Suman R. Rawat
  • , Minna K. Männistö
  • , Valentin Starovoytov
  • , Lynne Goodwin
  • , Matt Nolan
  • , Loren Hauser
  • , Miriam Land
  • , Karen Walston Davenport
  • , Tanja Woyke
  • and Max M. Häggblom
Corresponding author

DOI: 10.4056/sigs.4648353

Received: 05 December 2013

Accepted: 05 December 2013

Published: 15 June 2014


Granulicella tundricola strain MP5ACTX9T is a novel species of the genus Granulicella in subdivision 1 Acidobacteria. G. tundricola is a predominant member of soil bacterial communities, active at low temperatures and nutrient limiting conditions in Arctic alpine tundra. The organism is a cold-adapted acidophile and a versatile heterotroph that hydrolyzes a suite of sugars and complex polysaccharides. Genome analysis revealed metabolic versatility with genes involved in metabolism and transport of carbohydrates, including gene modules encoding for the carbohydrate-active enzyme (CAZy) families for the breakdown, utilization and biosynthesis of diverse structural and storage polysaccharides such as plant based carbon polymers. The genome of G. tundricola strain MP5ACTX9T consists of 4,309,151 bp of a circular chromosome and five mega plasmids with a total genome content of 5,503,984 bp. The genome comprises 4,705 protein-coding genes and 52 RNA genes.


cold adaptedacidophiletundra soilAcidobacteria


The strain MP5ACTX9T (=ATCC BAA-1859T =DSM 23138T) is the type strain of Granulicella tundricola [’la. N.L. n. tundra, tundra, a cold treeless region; L. masc. suffix -cola (from L. n. incola) dweller; N.L. n. tundricola tundra dweller] that was isolated from soil at the Malla Nature Reserve, Kilpisjärvi, Finland; 69°01’N, 20°50’E) and described along with other species of the genus Granulicella isolated from tundra soil [1].

Acidobacteria is a phylogenetically and physiologically diverse phylum [2,3], the members of which are ubiquitously found in diverse habitats and are abundant in most soil environments [4,5] including Arctic tundra soils [6,7]. Acidobacteria are relatively difficult to cultivate, as they have slow growth rates. To date only subdivisions 1, 3, 4, 8, 10 and 23 Acidobacteria are defined by taxonomically characterized representatives [8-23] as well as three ‘Candidatus’ taxa [24,25]. The phylogenetic diversity, ubiquity and abundance of this group suggest that they play important ecological roles in soils. The abundance of Acidobacteria correlates with soil pH [26,27] and carbon [28,29], with subdivision 1 Acidobacteria being most abundant in slightly acidic soils. Acidobacteria, including members of the genera Granulicella and Terriglobus, dominate the acidic tundra heaths of northern Finland [26,30-32]. Using selective isolation techniques we have been able to isolate several slow growing and fastidious strains of Acidobacteria [1,11]. On the basis of phylogenetic, phenotypic and chemotaxonomic data, including 16S rRNA, rpoB gene sequence similarity and DNA–DNA hybridization, strain MP5ACTX9T was classified as a novel species of the genus Granulicella [1]. Here, we summarize the physiological features together with the complete genome sequence, annotation and data analysis of Granulicella tundricola strain MP5ACTX9T.

Classification and features

Within the genus Granulicella, eight species are described with validly published names: G. mallensis MP5ACTX8T, G. tundricola MP5ACTX9T, G. arctica MP5ACTX2T,G. sapmiensis S6CTX5AT isolated from Arctic tundra soil [1] and G. paludicola OB1010T, G. paludicola LCBR1, G. pectinivorans TPB6011T ,G. rosea TPO1014T ,G. aggregans TPB6028T isolated from sphagnum peat bogs [2].

Strain MP5ACTX9T shares 95.5 - 97.2% 16S rRNA gene identity with tundra soil strains G. mallensis MP5ACTX8T (95.5%), G. arctica MP5ACTX2T (96.9%), G. sapmiensis S6CTX5AT (97.2%) and 95.2 – 97.7% identity with the sphagnum bog strains, G. pectinivorans TPB6011T (97.7%), G. rosea TPO1014T (97.2%), %), G. aggregans TPB6028T (96.8%), G. paludicola LCBR1 (95.9%), and G. paludicola strain OB1010T (95.3%), which were isolated from sphagnum peat. Phylogenetic analysis based on the 16S rRNA gene of taxonomically classified strains of family Acidobacteriaceae placed G. rosea type strain T4T (AM887759) as the closest taxonomically classified relative of G. tundricola strain MP5ACTX9T (Table 1, Figure 1).

Table 1

Classification and general features of G. tundricola strain MP5ACTX9T




   Evidence codea


     Domain Bacteria

   TAS [33]

     Phylum Acidobacteria

   TAS [34,35]

     Class Acidobacteria

   TAS [36,37]

     Order Acidobacteriales

   TAS [37,38]

     Family Acidobacteriaceae

   TAS [35,39]

     Genus Granulicella

   TAS [1,40]

     Species Granulicella tundricola

   TAS [1]

     Type strain: MP5ACTX9T (ATCC BAA-1859T = DSM 23138T)

     Gram stain


   TAS [1]

     Cell shape


   TAS [1]



   TAS [1]


     not reported


     Temperature range


   TAS [1]

     Optimum temperature

     21–24 °C

   TAS [1]

     pH range; Optimum

     3.5–6.5; 5

   TAS [1]

     Carbon source

     D-glucose, maltose, cellobiose, D-fructose, D-galactose, lactose, lactulose, D-mannose, sucrose, trehalose, D-xylose, raffinose, N-acetyl-D-glucosamine, glutamate

   TAS [1]



     terrestrial, tundra soil

   TAS [1]



     No growth with >1.0% NaCl (w/v)

   TAS [1]


     Oxygen requirement


   TAS [1]


     Biotic relationship


   TAS [1]






     Geographic location

     Malla Nature Reserve, Arctic-alpine tundra, Finland

   TAS [1]


     Sample collection


   TAS [1]




   TAS [1]




   TAS [1]



     700 m

   TAS [1]

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 [41].

Figure 1

Phylogenetic tree highlighting the position of G. tundricola MP5ACTX9T (shown in bold) relative to the other type strains within subdivision1 Acidobacteria. The maximum likelihood tree was inferred from 1,361 aligned positions of the 16S rRNA gene sequences and derived based on the Tamura-Nei model using MEGA 5 [42]. Bootstrap values >50 (expressed as percentages of 1,000 replicates) are shown at branch points. Bar: 0.01 substitutions per nucleotide position. The corresponding GenBank accession numbers are displayed in parentheses. Strains whose genomes have been sequenced, are marked with an asterisk; G. mallensis MP5ACTX8T (CP003130), G. tundricola MP5ACTX9T (CP002480), T. saanensis SP1PR4T (CP002467), T. roseus KBS63T (CP003379), and A. capsulatum ATCC 51196T (CP001472). Bryobacter aggregatus MPL3 (AM162405) in SD3 Acidobacteria was used as an outgroup.

Morphology and physiology

G. tundricola cells are Gram-negative, non-motile, aerobic rods, approximately 0.5 μm wide and 0.5 – 1.8 μm long. Colonies on R2A agar are pink, circular, convex and smooth. Growth occurs at +4 to 28°C and at pH 3.5-6.5 with an optimum at 21-24°C and pH 5 (Fig. 2). Genotypic analyses, including low rpoB gene sequence similarity and phenotypic characteristics clearly distinguished strain MP5ACTX9T from other Granulicella species/strains, leading us to conclude that MP5ACTX9T represents a novel species of the genus Granulicella, for which the name Granulicella tundricola sp. nov. was proposed [1].

Figure 2

Electron micrograph of G. tundricola MP5ACTX9T

Strain MP5ACTX9T hydrolyzed complex to simple carbon substrates [1] which include complex polysaccharides like aesculin, pectin, laminarin, starch and pullulan, but not gelatin, cellulose, lichenan, sodium alginate, xylan, chitosan or chitin. Strain MP5ACTX9T also utilized the following sugars as growth substrates: D-glucose, maltose, cellobiose, D-fructose, D-galactose, lactose, lactulose, D-mannose, sucrose, trehalose, D-xylose, raffinose, N-acetyl-D-glucosamine, glutamate and gluconic acid. Enzyme activities reported for the strain MP5ACTX9T include acid phosphatase, esterase (C4 and C8), leucine arylamidase, valine arylamidase, α-chymotrypsin, trypsin, naphthol-AS-BI-phosphohydrolase, α- and β-galactosidases, α- and β-glucosidases, N-acetyl- β-glucosaminidase, β-glucuronidase, α-fucosidase and α-mannosidase but negative for alkaline phosphatase and lipase (C14). Strain MP5ACTX9T is resistant to ampicillin, erythromycin, chloramphenicol, neomycin, streptomycin, tetracycline, gentamicin, bacitracin, polymyxin B and penicillin, but susceptible to rifampicin, kanamycin, lincomycin and novobiocin.


The major cellular fatty acids in G. tundricola are iso-C15:0 (46.4%), C16:1ω7c (35.0%) and C16:0 (6.6%). The cellular fatty acid composition of strain MP5ACTX9T was similar to that of other Granulicella strains with fatty acids iso-C15:0 and C16:1ω7c being most abundant in all strains. Strain MP5ACTX9T contains MK-8 as the major quinone and also contains 4% of MK-7.

Genome sequencing and annotation

Genome project history

G. tundricola strain MP5ACTX9T was selected for sequencing in 2009 by the DOE Joint Genome Institute (JGI) community sequencing program. The Quality Draft (QD) assembly and annotation were completed on May 24, 2010. The GenBank Date of Release was February 2, 2011. The genome project is deposited in the Genomes On-Line Database (GOLD) [43] and the complete genome sequence of strain MP5ACTX9T is deposited in GenBank (CP002480.1). Table 2 presents the project information and its association with MIGS version 2.0 [44].

Table 2

Project information.





    Finishing quality



    Libraries used

    Three libraries, an Illumina GAii shotgun library (GUIX),    a 454 Titanium standard library (GTWG, GWTA) and a paired end 454 (GSUN) library


    Sequencing platforms

    454 Titanium standard, 454 Paired End, Illumina

MIGS 31.2

    Fold coverage

    20×(454), 274X (Illumina)



    Newbler, VELVET, PHRAP


    Gene calling method

    ProdigaL, GenePRIMP

    Locus Tag


    Genbank ID


    GenBank Date of Release

    February 2, 2011




    PRJNA50551, PRJNA47621

    Project relevance

    Environmental, Biogeochemical cycling of Carbon, Biotechnological, GEBA

Growth conditions and genomic DNA extraction

G. tundricola MP5ACTX9T was cultivated on R2 medium as previously described [1]. Genomic DNA (gDNA) of high sequencing quality was isolated using a modified CTAB method and evaluated according to the Quality Control (QC) guidelines provided by the DOE Joint Genome Institute [45].

Genome sequencing and assembly

The finished genome of G. tundricola MP5ACTX9T (JGI ID 4088693) was generated at the DOE Joint genome Institute (JGI) using a combination of Illumina [46] and 454 technologies [47]. For this genome we constructed and sequenced an Illumina GAii shotgun library which generated 42,620,699 reads totaling 3239 Mb, a 454 Titanium standard library which generated 146,119 reads and three paired end 454 libraries with an average insert size of 9.3 kb which generated 178,757 reads totaling 154.3 Mb of 454 data. All general aspects of library construction and sequencing performed at the JGI can be found at the JGI website [45]. The 454 Titanium standard data and the 454 paired end data were assembled with Newbler, version 2.3. Illumina sequencing data was assembled with Velvet, version 0.7.63 [48]. The 454 Newbler consensus shreds, the Illumina Velvet consensus shreds and the read pairs in the 454 paired end library were integrated using parallel phrap, version SPS - 4.24 (High Performance Software, LLC) [49]. The software Consed [50] was used in the finishing process. The Phred/Phrap/Consed software package [51] was used for sequence assembly and quality assessment in the subsequent finishing process. Illumina data was used to correct potential base errors and increase consensus quality using the software Polisher developed at JGI (Alla Lapidus, unpublished). Possible misassemblies were corrected using gapResolution (Cliff Han, un-published), Dupfinisher [52] or sequencing cloned bridging PCR fragments with sub-cloning. Gaps between contigs were closed by editing in Consed, by PCR and by Bubble PCR (J-F Cheng, unpublished) primer walks. The final assembly is based on 29.1 Mb of 454 draft data which provides an average 20× coverage of the genome and 975 Mb of Illumina draft data which provides an average 274× coverage of the genome.

Genome annotation

Genes were identified using Prodigal [53] as part of the Oak Ridge National Laboratory genome annotation pipeline, followed by a round of manual curation using the JGI GenePRIMP pipeline [54]. The predicted CDSs were translated and used to search the National Center for Biotechnology Information (NCBI) non-redundant database, UniProt, TIGRFam, Pfam, PRIAM, KEGG, (COGs) [55,56], and InterPro. These data sources were combined to assert a product description for each predicted protein. Non-coding genes and miscellaneous features were predicted using tRNAscan-SE [57], RNAMMer [58], Rfam [59], TMHMM [60], and signalP [61]. Additional gene prediction analysis and functional annotation were performed within the Integrated Microbial Genomes Expert Review (IMG-ER) platform [62].

Genome properties

The genome is 5,503,984 bp in size, which includes the 4,309,151 bp chromosome and five plasmids pACIX901 (0.48 Mbp); pACIX902 (0.3 Mbp); pACIX903 (0.19 Mbp), pACIX904 (0.12 Mbp) and pACIX905 (0.12 Mbp), with a GC content of 59.9 mol%. There are 52 RNA genes (Figures 3 and 4, and Table 3). Of the 4,758 predicted genes, 4,706 are protein-coding genes (CDSs) and 163 are pseudogenes. Of the total CDSs, 68.8% represent COG functional categories and 27.5% consist of signal peptides. The distribution of genes into COG functional categories is presented in Figure 3 and Table 4, and Table 5.

Figure 3

Circular representation of the chromosome of G. tundricola MP5ACTX9T displaying relevant genome features. From outside to center; Genes on forward strand (colored by COG categories), genes on reverse strand (colored by COG categories), RNA genes (tRNAs green, rRNAs red, other RNAs black), GC content and GC skew.

Figure 4

Circular representation of the plasmids of G. tundricola MP5ACTX9T displaying relevant genome features. From outside to 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 and GC skew. Order and size from left to right: pACIX901, 0.48 Mbp; pACIX902, 0.3 Mbp; pACIX903, 0.19 Mbp; pACIX904, 0.12 Mbp; pACIX905, 0.12 Mbp.

Table 3

Summary of genome: one chromosome and five plasmids


    Size (Mb)


    INSDC identifier

   RefSeq ID






Plasmid pACIX901





Plasmid pACIX902





Plasmid pACIX903





Plasmid pACIX904





Plasmid pACIX905





Table 4

Genome statistics.



   % of Total

Genome size (bp)



DNA coding (bp)



DNA G+C (bp)



DNA scaffolds



Total genes



Protein coding genes



RNA genes



Pseudo genes



Genes in internal clusters



Genes with function prediction



Genes assigned to COGs



Genes with Pfam domains



Genes with signal peptides



Genes with transmembrane helices



CRISPR repeats



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

Table 5

Number of genes associated with general COG functional categories.








    Translation, ribosomal structure and biogenesis




    RNA processing and modification








    Replication, recombination and repair




    Chromatin structure and dynamics




    Cell cycle control, Cell division, chromosome partitioning




    Defense mechanisms




    Signal transduction mechanisms




    Cell wall/membrane biogenesis




    Cell motility




    Intracellular trafficking and secretion




    Posttranslational modification, protein turnover, chaperones




    Energy production and conversion




    Carbohydrate transport and metabolism




    Amino acid transport and metabolism




    Nucleotide transport and metabolism




    Coenzyme transport and metabolism




    Lipid transport and metabolism




    Inorganic ion transport and metabolism




    Secondary metabolites biosynthesis, transport and catabolism




    General function prediction only




    Function unknown




    Not in COGs

The total is based on the total number of protein coding genes in the genome.


Granulicella tundricola MP5ACTX9T is a tundra soil strain with a genome consisting of a circular chromosome and five mega plasmids ranging in size from 1.1 x 105 to 4.7 x 105 bp for a total genome size of 5.5 Mbp. The G. tundricola genome also contains close to twice as many pseudogenes and a large number of mobile genetic elements as compared to Granulicella mallensis and Terrigobus saanensis, two other Acidobacteria isolated from the same habitat [29]. A large number of genes assigned to COG functional categories for transport and metabolism of carbohydrates (6.9%) and amino acids (6.5%) and involved in cell envelope biogenesis (8%) and transcription (6.9%) were identified. Further genome analysis revealed an abundance of gene modules encoding for functional activities within the carbohydrate-active enzymes (CAZy) families [63,64] involved in breakdown, utilization and biosynthesis of carbohydrates. G. tundricola hydrolyzed complex carbon polymers, including CMC, pectin, lichenin, laminarin and starch, and utilized sugars such as cellobiose, D-mannose, D-xylose and D-trehalose. Genome predictions for CDSs encoding for enzymes such as cellulases, pectinases, alginate lyases, trehalase and amylases are in agreement with biochemical activities in strain MP5ACTX9T. However, the genome of G. tundricola did contain many CDSs encoding for GH18 chitinases although no chitinase activity was detected after 10 day-incubation with chitinazure [29]. In addition, the G. tundricola genome contained a cluster of genes in close proximity to the cellulose synthase gene (bcsAB), which included cellulase (bscZ) (endoglucanase Y) of family GH8, cellulose synthase operon protein (bcsC) and a cellulose synthase operon protein (yhjQ) involved in cellulose biosynthesis. We previously reported on a detailed comparative genome analysis of G. tundricola MP5ACTX9T with other Acidobacteria strains for which finished genomes are available [29]. The data suggests that G. tundricola is involved in hydrolysis and utilization of stored carbohydrates and biosynthesis of exopolysaccharides from organic matter and plant based polymers in the soil. Therefore, G. tundricola may be central to carbon cycling processes in Arctic and boreal soil ecosystems.



The work conducted by the US Department of Energy Joint Genome Institute is supported by the Office of Science of the US Department of Energy Under Contract No. DE-AC02-05CH11231. This work was funded in part by the Academy of Finland and the New Jersey Agricultural Experiment Station.

This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.


  1. Männistö MK, Rawat S, Starovoytov V and Häggblom MM. Granulicella arctica sp. nov., Granulicella mallensis sp. nov., Granulicella sapmiensis sp. nov. and Granulicella tundricola sp. nov., novel Acidobacteria from tundra soil of Northern Finland. Int J Syst Evol Microbiol. 2012; 62:2097-2106 View ArticlePubMed
  2. Jones RT, Robeson MS, Lauber CL, Hamady M, Knight R and Fierer N. A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J. 2009; 3:442-453 View ArticlePubMed
  3. Barns SM, Cain EC, Sommerville L and Kuske CR. Acidobacteria phylum sequences in uranium-contaminated subsurface sediments greatly expand the known diversity within the phylum. Appl Environ Microbiol. 2007; 73:3113-3116 View ArticlePubMed
  4. Janssen PH. Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol. 2006; 72:1719-1728 View ArticlePubMed
  5. Fierer N, Bradford MA and Jackson RB. Toward an ecological classification of soil bacteria. Ecology. 2007; 88:1354-1364 View ArticlePubMed
  6. Campbell BJ, Polson SW, Hanson TE, Mack MC and Schuur EA. The effect of nutrient deposition on bacterial communities in Arctic tundra soil. Environ Microbiol. 2010; 12:1842-1854 View ArticlePubMed
  7. Chu H, Fierer N, Lauber CL, Caporaso JG, Knight R and Grogan P. Soil bacterial diversity in the Arctic is not fundamentally different from that found in other biomes. Environ Microbiol. 2010; 12:2998-3006 View ArticlePubMed
  8. Pankratov TA and Dedysh SN. Granulicella paludicola gen. nov., sp. nov., Granulicella pectinivorans sp. nov., Granulicella aggregans sp. nov. and Granulicella rosea sp. nov., acidophilic, polymer degrading acidobacteria from Sphagnum peat bogs. Int J Syst Evol Microbiol. 2010; 60:2951-2959 View ArticlePubMed
  9. Kishimoto N, Kosako Y and Tano T. Acidobacterium capsulatum gen. nov., sp. nov.: an acidophilic chemoorganotrophic bacterium containing menaquinone from acidic mineral environment. Curr Microbiol. 1991; 22:1-7 View Article
  10. Eichorst SA, Breznak JA and Schmidt TM. Isolation and characterization of soil bacteria that define Terriglobus gen. nov., in the phylum Acidobacteria. Appl Environ Microbiol. 2007; 73:2708-2717 View ArticlePubMed
  11. Männistö MK, Rawat SR, Starovoytov V and Häggblom MM. Terriglobus saanensis sp. nov., an acidobacterium isolated from tundra soil. Int J Syst Evol Microbiol. 2011; 61:1823-1828 View ArticlePubMed
  12. Koch IH, Gich F, Dunfield PF and Overmann J. Edaphobacter modestus gen. nov., sp. nov., and Edaphobacter aggregans sp. nov., acidobacteria isolated from alpine and forest soils. Int J Syst Evol Microbiol. 2008; 58:1114-1122 View ArticlePubMed
  13. Okamura K, Kawai A, Yamada T and Hiraishi A. Acidipila rosea gen. nov.,sp nov., an acidophilic chemoorganotrophic bacterium belonging to the phylum Acidobacteria. FEMS Microbiol Lett. 2011; 317:138-142 View ArticlePubMed
  14. Pankratov TA, Kirsanova LA, Kaparullina EN, Kevbrin VV and Dedysh SN. Telmatobacter bradus gen. nov., sp. nov., a cellulolytic facultative anaerobe from subdivision 1 of the Acidobacteria and emended description of Acidobacterium capsulatum Kishimoto et al. Int J Syst Evol Microbiol. 2012; 62:430-437 View ArticlePubMed
  15. Kulichevskaya IS, Kostina LA, Valásková V, Rijpstra IC, Sinninghe Damsté JS, de Boer W and Dedysh SN. Acidicapsa borealis gen. nov., sp. nov. and A. ligni sp. nov., two novel subdivision 1 Acidobacteria from sphagnum peat and decaying wood. Int J Syst Evol Microbiol. 2012; 62:1512-1520 View ArticlePubMed
  16. Dedysh SN, Kulichevskaya IS, Serkebaeva YM, Mityaeva MA, Sorokin VV, Suzina NE, Rijpstra WI and Damste JS. Bryocella elongata gen. nov., sp. nov., a novel member of Subdivision 1 of the Acidobacteria isolated from a methanotrophic enrichment culture, and emended description of Edaphobacter aggregans Koch et al. 2008. Int J Syst Evol Microbiol. 2012; 62:654-664 View ArticlePubMed
  17. Kulichevskaya IS, Suzina NE, Liesack W and Dedysh SN. Bryobacter aggregatus gen. nov., sp. nov., a peat-inhabiting, aerobic chemoorganotroph from subdivision 3 of the Acidobacteria. Int J Syst Evol Microbiol. 2010; 60:301-306 View ArticlePubMed
  18. Foesel BU, Rohde M and Overmann J. Blastocatella fastidiosa gen. nov., sp. nov., isolated from semiarid savanna soil – The first described species of Acidobacteria subdivision 4. Syst Appl Microbiol. 2013; 36:82-89 View ArticlePubMed
  19. Izumi H, Nunoura T, Miyazaki M, Mino S, Toki T, Takai K, Sako Y, Sawabe T and Nakagawa S. Thermotomaculum hydrothermale gen. nov., sp. nov., a novel heterotrophic thermophile within the phylum Acidobacteria from a deep-sea hydrothermal vent chimney in the Southern Okinawa Trough. Extremophiles. 2012; 16:245-253 View ArticlePubMed
  20. Liesack W, Bak F, Kreft JU and Stackebrandt E. Holophaga foetida gen.nov., sp. nov., a new homoacetogenic bacterium degrading methoxylated aromatic compounds. Arch Microbiol. 1994; 162:85-90 View ArticlePubMed
  21. Coates JD, Ellis DJ, Gaw CV and Lovley DR. Geothrix fermentans gen. nov., sp. nov., a novel Fe(III)-reducing bacterium from a hydrocarbon contaminated aquifer. Int J Syst Bacteriol. 1999; 49:1615-1622 View ArticlePubMed
  22. Fukunaga Y, Kurahashi M, Yanagi K, Yokota A and Harayama S. Acanthopleuribacter pedis gen. nov., sp. nov., a marine bacterium isolated from a chiton, and description of Acanthopleuribacteraceae fam. nov., Acanthopleuribacterales ord. nov., Holophagales ord. nov. and Holophagae classis nov. in the phylum ‘Acidobacteria’. Int J Syst Evol Microbiol. 2008; 58:2597-2601 View ArticlePubMed
  23. Losey NA, Stevenson BS, Busse HJ, Damste JSS, Rijpstra WIC, Rudd S, Lawson PA. Thermoanaerobaculum aquaticum gen. nov., sp. nov., the first cultivated member of Acidobacteria subdivision 23, isolated from a hot spring. [PMID: 23771620]. [DOI Int J Syst Evol Microbiol 2013; 63:4149-4157. View Article
  24. Ward NL, Challacombe JF, Janssen PH, Henrissat B, Coutinho PM, Wu M, Xie G, Haft DH, Sait M and Badger J. Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Appl Environ Microbiol. 2009; 75:2046-2056 View ArticlePubMed
  25. Bryant DA and Amaya M. Garcia Costas AMG, Maresca JA, Chew AGM, Klatt CG, Bateson MM, Tallon LJ, Hostetler J, Nelson WC, Heidelberg JF, Ward DM. Candidatus Chloracidobacterium thermophilum: an aerobic phototrophic acidobacterium. Science. 2007; 317:523-526 View ArticlePubMed
  26. Männistö MK, Tiirola M and Häggblom MM. Microbial communities in Arctic fjelds of Finnish Lapland are stable but highly pH dependent. FEMS Microbiol Ecol. 2007; 59:452-465 View ArticlePubMed
  27. Sait M, Davis KE and Janssen PH. Effect of pH on isolation and distribution of members of subdivision 1 of the phylum Acidobacteria occurring in soil. Appl Environ Microbiol. 2006; 72:1852-1857 View ArticlePubMed
  28. Eichorst SA, Kuske CR and Schmidt TM. Influence of plant polymers on the distribution and cultivation of bacteria in the phylum Acidobacteria. Appl Environ Microbiol. 2011; 77:586-596 View ArticlePubMed
  29. Rawat SR, Männistö MK, Bromberg Y and Häggblom MM. Comparative genomic and physiological analysis provides insights into the role of Acidobacteria in organic carbon utilization in Arctic tundra soils. FEMS Microbiol Ecol. 2012; 82:341-355 View ArticlePubMed
  30. Rawat SR, Männistö MK, Starovoytov V, Goodwin L, Nolan M, Hauser L, Land M, Davenport KW, Woyke T and Häggblom MM. Complete genome sequence of Terriglobus saanensis strain SP1PR4T, an Acidobacteria from tundra soil. Stand Genomic Sci. 2012; 7:59-69 View ArticlePubMed
  31. Männistö MK, Tiirola M and Häggblom MM. Effect of freeze-thaw cycles on bacterial communities of Arctic tundra soil. Microb Ecol. 2009; 58:621-631 View ArticlePubMed
  32. Männistö MK, Kurhela E, Tiirola M and Häggblom MM. Acidobacteria dominate the active bacterial communities of sub-Arctic tundra with widely divergent winter-time snow accumulation and soil temperatures. FEMS Microbiol Ecol. 2013; 84:47-59 View ArticlePubMed
  33. Woese CR, Kandler O and Wheelis ML. Towards a natural system of organisms: proposal for the do-mains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA. 1990; 87:4576-4579 View ArticlePubMed
  34. Thrash JC, Coates JD. Phylum XVII. Acidobacteria phyl. nov. In: Krieg NR, Staley JT, Brown DR, Hedlund BP, Paster BJ, Ward NL, Ludwig W, Whitman WB (eds), Bergey's Manual of Systematic Bacteriology, Second Edition, Volume 4, Springer, New York, 2011, p. 725.
  35. . 143. Int J Syst Evol Microbiol. 2012; 62:1-4 View Article
  36. Cavalier-Smith T. The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial megaclassification. Int J Syst Evol Microbiol. 2002; 52:7-76PubMed
  37. . The nomenclatural types of the orders Acholeplasmatales, Halanaerobiales, Halobacteriales, Methanobacteriales, Methanococcales, Methanomicrobiales, Planctomycetales, Prochlorales, Sulfolobales, Thermococcales, Thermoproteales and Verrucomicrobiales are the genera Acholeplasma, Halanaerobium, Halobacterium, Methanobacterium, Methanococcus, Methanomicrobium, Planctomyces, Prochloron, Sulfolobus, Thermococcus, Thermoproteus and Verrucomicrobium, respectively. Opinion 79. Int J Syst Evol Microbiol. 2005; 55:517-518 View ArticlePubMed
  38. Ludwig W, Euzeby J, Whitman WG. Draft taxonomic outline of the Bacteroidetes, Planctomycetes, Chlamydiae, Spirochaetes, Fibrobacteres, Fusobacteria, Acidobacteria, Verrucomicrobia, Dictyoglomi, and Gemmatimonadetes Taxonomic Outline 2008.Web Site
  39. Thrash JC, Coates JD. Family I. Acidobacteriaceae fam. nov. In: Krieg NR, Staley JT, Brown DR, Hedlund BP, Paster BJ, Ward NL, Ludwig W, Whitman WB (eds), Bergey's Manual of Systematic Bacteriology, Second Edition, Volume 4, Springer, New York, 2011, p. 728.
  40. Pankratov TA and Dedysh SN. Granulicella paludicola gen. nov., sp. nov., Granulicella pectinivorans sp. nov., Granulicella aggregans sp. nov. and Granulicella rosea sp. nov., acidophilic, polymer-degrading acidobacteria from Sphagnum peat bogs. Int J Syst Evol Microbiol. 2010; 60:2951-2959 View ArticlePubMed
  41. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS and Eppig JT. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000; 25:25-29 View ArticlePubMed
  42. Tamura K, Peterson D, Peterson N, Stecher G, Nei M and Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011; 28:2731-2739 View ArticlePubMed
  43. Liolios K, Mavromatis K, Tavernarakis N and Kyrpides NC. The Genomes On Line Database (GOLD) in 2007: status of genomic and metagenomic projects and their associated metadata. Nucleic Acids Res. 2007; 36:D475-D479 View ArticlePubMed
  44. Field D, Garrity G, Gray T, Morrison N, Selengut J, Sterk P, Tatusova T, Thomson N, Allen MJ and Angiuoli SV. The minimum information about a genome sequence (MIGS) specification. Nat Biotechnol. 2008; 26:541-547 View ArticlePubMed
  45. . Web Site
  46. Bennett S. Solexa Ltd. Pharmacogenomics. 2004; 5:433-438 View ArticlePubMed
  47. Margulies M, Egholm M and Altman WE. Genome sequencing in microfabricated high-density picolitre reactors. Nature. 2005; 437:376-380PubMed
  48. Zerbino DR and Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 2008; 18:821-829 View ArticlePubMed
  49. Ewing B, Hillier L, Wendl MC and Green P. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 1998; 8:175-185 View ArticlePubMed
  50. Gordon D, Abajian C and Green P. Consed: a graphical tool for sequence finishing. Genome Res. 1998; 8:195-202 View ArticlePubMed
  51. The Phred/Phrap/Consed software package. Web Site
  52. Han CS, Chain P. Finishing repeat regions automatically with Dupfinisher CSREA Press. In: Arabnia AR, Valafar H, editors. Proceedings of the 2006 international conference on bioinformatics & computational biology; 2006; June 26-29. CSREA Press. p 141-146.
  53. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW and Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics. 2010; 11:119 View ArticlePubMed
  54. Pati A, Ivanova NN, Mikhailova N, Ovchinnikova G, Hooper SD, Lykidis A and Kyrpides NC. GenePRIMP: a gene prediction improvement pipeline for prokaryotic genomes. Nat Methods. 2010; 7:455-457 View ArticlePubMed
  55. Tatusov RL, Koonin EV and Lipman DJ. A genomic perspective on protein families. Science. 1997; 278:631-637 View ArticlePubMed
  56. . Web Site
  57. Lowe TM and Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 1997; 25:955-964PubMed
  58. Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T and Ussery DW. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 2007; 35:3100-3108 View ArticlePubMed
  59. Griffiths-Jones S, Bateman A, Marshall M, Khanna A and Eddy SR. Rfam: an RNA family database. Nucleic Acids Res. 2003; 31:439-441 View ArticlePubMed
  60. Krogh A, Larsson B, von Heijne G and Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 2001; 305:567-580 View ArticlePubMed
  61. Bendtsen JD, Nielsen H, von Heijne G and Brunak S. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol. 2004; 340:783-795 View ArticlePubMed
  62. Markowitz VM, Mavromatis K, Ivanova N, Chen IM, Chu K and Kyrpides N. Expert Review of Functional Annotations for Microbial Genomes. Bioinformatics. 2009; 25:2271-2278 View ArticlePubMed
  63. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V and Henrissat B. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res. 2009; 37:D233-D238 View ArticlePubMed
  64. Lombard V, Ramulu HG, Drula E, Coutinho PM and Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Research 1–6.