High quality draft genome sequence of Janthinobacterium psychrotolerans sp. nov., isolated from a frozen freshwater pond
© The Author(s). 2016
Received: 22 July 2016
Accepted: 27 November 2016
Published: 19 January 2017
Strain S3-2T, isolated from sediment of a frozen freshwater pond, shares 99% 16S rRNA gene sequence identity with strains of the genus Janthinobacterium. Strain S3-2T is a facultative anaerobe that lacks the ability to produce violacein but shows antibiotic resistance, psychrotolerance, incomplete denitrification, and fermentation. The draft genome of strain S3-2T has a size of ~5.8 Mbp and contains 5,297 genes, including 115 RNA genes. Based on the phenotypic properties of the strain, the low in silico DNA-DNA hybridization (DDH) values with related genomes (<35%), and the low whole genome-based average nucleotide identity (ANI) (<86%) with other strains within the genus Janthinobacterium, we propose that strain S3-2T is the type strain (= DSM 102223 = LMG 29653) of a new species within this genus. We propose the name Janthinobacterium psychrotolerans sp. nov. to emphasize the capability of the strain to grow at low temperatures.
KeywordsJanthinobacterium psychrotolerans Freshwater sediment Low temperature Denitrification Fermentation
The genus Janthinobacterium includes Gram-negative, motile, aerobic rod-shaped bacteria, which were isolated from soil and aquatic environments. Production of violacein, a purple, water-insoluble, secondary metabolite, is a feature commonly found in this genus [1, 2]. Violacein has anti-bacterial, anti-viral, and anti-fungal properties , and has even been reported to protect frogs against fungal infection, when produced by the frog skin microbiota .
Strain S3-2T, which is affiliated with the genus Janthinobacterium was isolated from freshwater sediment while screening for denitrifying bacteria. However, strain S3-2T has traits that unambiguously distinguish it from the other strains of the genus [2, 5, 6]. Among these traits is the ability of strain S3-2T to grow at −3 °C, and to ferment different sugars. In contrast to the other strains, strain S3-2T does not produce the violet pigment violacein, not even when grown on glycerol medium (20 g L−1) that induces violacein synthesis in other members of the genus Janthinobacterium . Here we present the genome of strain S3-2T as well as its classification and phenotypic features. Taken together, these characteristics support the circumscription of S3-2T as novel species, Janthinobacterium psychrotolerans sp. nov.
Classification and features
Sediment was obtained from a small fresh water pond near Aarhus, Denmark (coordinates 56.182804 N, 10.176294 E); the pond was covered with a thick layer of ice at the time of sampling. Strain S3-2T was isolated at room temperature under oxic conditions from a diluted sediment sample (3 g in 10 mL sterile water) by direct plating on TSB agar, containing 3 g tryptic soy broth (Scharlau Chemie S.A., Spain) L−1, 15 g agar L−1.
Different growth temperatures (−3 °C, 0 °C, 4 °C, 10 °C, 21 °C, 25 °C, 30 °C, 35 °C, and 40 °C) were tested on TSB plates. Growth occurred between −3 °C and 30 °C, with the optimal growth temperature being 25 °C. The range of pH tolerance was tested in TSB (10 g L−1) adjusted to pH values 4–9 and buffered with citric acid, phosphate, or Tris . Growth occurred between pH 6 and 8, with optimal growth at pH 7. Salt tolerance was tested on TSB (10 g L−1) agar with NaCl concentrations ranging from 0.17% to 3.17%. Strain S3-2T tolerated up to 2.17% of NaCl. Strain S3-2T produced N2O (determined by an N2O sensor ) as the end product of denitrification in anoxic incubations with TSB containing 5 mM nitrate; nitrite or N2 gas were never detected.
Strain S3-2T showed mucoid pale yellow colonies on TSB agar, while colonies were non-mucoid, circular with undulate margins, and orange on modified Lysogeny broth (LB) agar (10 g L−1 tryptone, 5 g L−1 yeast extract, 10 g L−1 NaCl, 1% glycerol, 15 g L−1 agar), and brownish on glycerol medium (20 g L−1 glycerol, 0.5 g L−1 NaCl, 2.4 g L−1 MgSO4, 1 ml L−1 trace metal solution , 15 g L−1 agar). None of the media induced the production of violacein . None of the observed pigments were fluorescent under UV light (365 nm; Vilber Lourmat, Germany).
Strain S3-2T was resistant to penicillin (5 μg disc), and ampicillin (10 μg disc), but susceptible to streptomycin (10 μg disc) and tetracycline (30 μg disc) on TSB (3 g L−1) agar. In GEN III microplate assays (Biolog), strain S3-2T was resistant to rifamycin SV, lincomycin, and vancomycin; susceptible to niaproof 4. Strain S3-2T did not inhibit growth of Escherichia coli K12 (DSM498; a strain resistant to penicillin, ampicillin, streptomycin, and tetracycline) on TSB (10 g L−1) agar.
Strain S3-2T was tested positive for alkaline phosphatase using the API ZYM test (BioMérieux, France), catalase using hydrogen peroxide, and oxidase (Bactident Oxidase, Merck, Germany). Using API 20E (BioMérieux, France), positive reactions were observed for enzymatic activity of arginine dihydrolase, for indole production, and the fermentation of D-glucose, D-mannitol, D-sucrose, and L-arabinose. Negative reactions were observed for enzymatic activities of β-galactosidase, lysine decarboxylase, ornithine decarboxylase, urease, and gelatinase. Inositol, D-sorbitol, L-rhamnose, D-melibiose, and amygdalin were not fermented, and H2S and acetoin were not produced. Janthinobacterium has previously been considered as non-fermentative [1, 11]. The capability of linking fermentation to growth has only been reported for J. lividum strain UTB1302 with glucose . Using API 20NE (BioMérieux, France), positive reactions were observed for hydrolysis of esculin ferric citrate, and the assimilation of arabinose. Negative reactions were observed for the assimilation of D-maltose, phenylacetic acid, N-acetyl-glucosamine, capric acid, and adipic acid. According to GEN III microplate assays (Biolog) at 25 °C, strain S3-2T could metabolize dextrin, D-cellobiose, D-raffinose, α-D-lactose, D-salicin, D-mannose, D-galactose, L-fucose, L-rhamnose, inosine, D-mannitol, D-arabitol, myo-inositol, glycyl-L-proline, L-alanine, L-aspartic acid, L-glutamic acid, L-histidine, L-pyroglutamic acid, D-galacturonic acid, L-galacturonic acid lactone, L-lactic acid, citric acid, α-keto-glutaric acid, D-malic acid, L-malic acid, bromo-succinic acid, Tween 40, and α-hydroxy-butyric acid. D-maltose, D-trehalose, N-acetyl-D-galactosamine, and formic acid were not metabolized.
Classification and general features of Janthinobacterium psychrotolerans S3-2T 
Species Janthinobacterium psychrotolerans
Strain S3-2T (LMG 29653 = DSM 102223)
−3 °C – 30 °C
pH range; Optimum
Sugars, amino acids, fatty acids etc.
0.17–2.17% NaCl (w/v)
Genome sequencing information
Genome project history
High quality draft
NexteraXT DNA sample preparation
Gene calling method
GenBank Date of Release
Source Material Identifier
LMG 29653, DSM 102223
Growth conditions and genomic DNA preparation
Strain S3-2T was grown at 25 °C in TSB (10 g L−1) supplemented with 5 mM nitrate. The cells were harvested by centrifugation and DNA was extracted from the pellet using the PowerLyser® PowerSoil® DNA extraction kit (MoBio, Carlsbad, CA, USA) according to the manufacturer’s protocol.
Genome sequencing and assembly
The genome of strain S3-2T was sequenced with the Illumina MiSeq Reagent Kit V3 (Illumina Inc. San Diego, CA, USA). Sequencing libraries were prepared using the Nextera XT Library Preparation Kit (Illumina). The sequencing library produced 3,761,645 paired end reads totalling ~2.11 Gbp. In total, 2,868,634 reads remained after quality trimming and adapter removal with Trimmomatic-0.33  and the following trimming parameters: CROP:235 HEADCROP:25 SLIDINGWINDOW:4:20. Read quality before and after trimming was assessed by FastQC version 0.11.4 . The trimmed reads (~1.04 Gbp) represented an average genome coverage of ~178-fold based on the size of the assembled draft genome of strain S3-2T. Reads were assembled using SPAdes 3.6.1 . Contigs shorter than 1,000 bp were removed after the assembly.
The draft genome was annotated using the standard operation procedure of the DOE-JGI Microbial Genome Annotation Pipeline (MGAP v.4) supported by the JGI (Walnut Creek, CA; USA) . Briefly, CRISPR elements were determined by the programs CRT  and PILER-CR v1.06 . Non-coding RNAs, and tRNAs, were predicted by tRNAscan-SE 1.3.1 . rRNA genes were identified by HMMER 3.1b2 . Protein-coding genes were determined by Prodigal v2.6.2 . Functional annotation was based on assigning the genes to different databases: the COG & KOG database (November, 2014) , the KEGG database (release 71.0, July 2014) , the MetaCyc database (release 18.1, June 2014) , the Pfam database (version 28.0, May, 2015) , the TIGRfam database (release 14.0, January, 2014) , and the InterPro Scan database (release 48) . In silico DNA-DNA hybridization (GGDC 2.0) was carried out with the online genome-to-genome calculator provided by the DSMZ .
% of Totala
Genome size (bp)
DNA coding (bp)
DNA G + C (bp)
Protein coding 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
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
Signal transduction mechanisms
Cell wall/membrane biogenesis
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
Not in COGs
Insights from the genome sequence
Sequence similarity of J. psychrotolerans strain S3-2T with described species of the genus Janthinobacterium
16S rRNA identity (%)a
DDH (Model-based Confidence Interval) (%)
ANI ± SDb (%)
81.66 ± 5.07
Janthinobacterium lividum MTR
84.69 ± 4.73
Janthinobacterium lividum NFR18
84.73 ± 4.87
Janthinobacterium lividum PMC 25724
83.84 ± 4.58
Janthinobacterium lividum RIT308
84.75 ± 4.84
Violacein production, a common feature in Janthinobacterium , was never observed in growth studies with strain S3-2T. This observation is consistent with the absence of the vioABCDE operon, which encodes the genes required for the synthesis of this pigment; neither the automated annotation nor manual BLAST searches of the S3-2T genome for known components of the vioABCDE operon (Additional file 1: Table S3) [2, 6] identified any genes encoding violacein synthesis.
The genome of strain S3-2T features all necessary genes for nitrate reduction to N2O but lacks genes encoding the nitrous oxide reductase (Additional file 1: Table S4), which is consistent with N2O as end-product of denitrification. Genes affiliated with aerobic respiration were identified, including terminal oxidases with both high- and low-affinity for oxygen (Additional file 1: Table S5). Another characteristic of strain S3-2T is its capability to ferment different sugars, a trait which has not been reported for other strains in the genus Janthinobacterium [1, 5, 11]. The genes that encode these properties were summarized (Additional file 1: Table S6, and Figure S1).
Based on the phenotypic properties, phylogenetic position, and whole genome comparison, we formally propose strain S3-2T as novel species of the genus Janthinobacterium , for which we propose the name Janthinobacterium psychrotolerans sp. nov. with strain S3-2T (=DSM 102223 = LMG 29653) as the type strain.
Description of Janthinobacterium psychrotolerans sp. nov.
Janthinobacterium psychrotolerans (psy.chro.to'le.rans. Gr. adj. psychros cold; L. part. adj. tolerans tolerating; N.L. neut. part. adj. psychrotolerans tolerating cold temperatures).
Janthinobacterium psychrotolerans is a facultative anaerobic, Gram-negative bacterium. Cells are rod-shaped, motile, and have a size of 1.9 ± 0.3 × 0.7 ± 0.1 μm. Colonies are pale yellow and mucoid on TSB agar. Growth occurs between −3 and 30 °C, with optimal growth observed at 25 °C. Strain S3-2T tolerates salinity between 0.17% and 2.17% NaCl, and grows within the pH range of 6 to 8 with optimal growth observed at pH 7.
Positive for catalase, oxidase, alkaline phosphatase, arginine dihydrolase. Negative for β-galactosidase, lysine decarboxylase, ornithine decarboxylase, urease, gelatinase.
Positive for metabolizing dextrin, D-cellobiose, D-raffinose, α-D-lactose, D-salicin, D-mannose, D-galactose, L-fucose, L-rhamnose, inosine, D-mannitol, D-arabitol, myo-inositol, glycyl-L-proline, L-alanine, L-aspartic acid, L-glutamic acid, L-histidine, L-pyroglutamic acid, D-galacturonic acid, L-galacturonic acid lactone, L-lactic acid, citric acid, α-keto-glutaric acid, D-malic acid, L-malic acid, bromo-succinic acid, Tween 40, and α-hydroxy-butyric acid. Negative for metabolizing D-maltose, D-trehalose, N-acetyl-D-galactosamine, and formic acid.
Positive for hydrolysis of esculin ferric citrate, assimilation of arabinose, and indole production. Negative for assimilation of D-maltose, phenylacetic acid, N-acetyl-glucosamine, capric acid, and adipic acid, acetoin production, and H2S production.
Strain S3-2T is able to ferment D-glucose, D-mannitol, D-sucrose, and L-arabinose; unable to ferment inositol, D-sorbitol, L-rhamnose, D-meliblose, and amygdalin.
Resistant to penicillin, vancomycin, rifamycin SV, lincomycin, and ampicillin; susceptible to streptomycin, niaproof 4, and tetracycline.
The G + C content of the genome is 63.04 mol%. The genome project is deposited in the Genomes OnLine Database (GOLD) as project Gp0124039. This Whole Genome Shotgun project is deposited at GenBank under the accession LOCQ00000000. The type strain S3-2T (= LMG 29653 = DSM 102223) was isolated from sediment of a small, frozen pond in Hasle, Aarhus, Denmark (coordinates 56.182804 N, 10.176294 E) in January, 2015.
Average nucleotide identities
Genomes OnLine database
General time reversible
Microbial genome annotation pipeline
Ribosomal database project
Tryptic soy broth.
We thank Anne B. Stentebjerg, Britta Poulsen, Trine B. Søgaard, Lars B. Pedersen, Preben G. Sørensen, and Lars R. Damgaard for excellent technical assistance. This study was supported by the Danish National Research Foundation (grants no. DNRF104), the European Research Council (grants no. 267233 and 294200), the Graduate School of Science and Technology, Aarhus University, Denmark, and the Department of Bioscience, Aarhus University.
KF and AS designed research; SS and BSK isolated and characterized strain S3-2T; XG carried out the genome sequencing and additional strain characterization; XG, LS, and IM performed bioinformatics analyses; all authors analysed data; XG, AS, and KF wrote the manuscript; all authors read and approved the final manuscript.
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.
- Shivaji S, Ray MK, Kumar GS, Reddy GSN, Saisree L, Wynn-Williams DD. Identification of Janthinobacterium lividum from the soils of the islands of Scotia Ridge and from Antarctic peninsula. Polar Biol. 1991;11.
- Hornung C, Poehlein A, Haack FS, Schmidt M, Dierking K, et al. The Janthinobacterium sp. HH01 genome encodes a homologue of the V. cholerae CqsA and L. pneumophila LqsA autoinducer synthases. PLoS One. 2013;8(2):e55045.View ArticlePubMedPubMed CentralGoogle Scholar
- Durán N, Justo GZ, Ferreira CV, Melo PS, Cordi L, Martins D. Violacein: properties and biological activities. Biotechnol. Appl. Biochem. 2007;48:127–33.Google Scholar
- Harris RN, Brucker RM, Walke JB, Becker MH, Schwantes CR, et al. Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus. ISME J. 2009;3:818–24.View ArticlePubMedGoogle Scholar
- Kawakami R, Sakuraba H, Ohshima T. Gene cloning and characterization of the very large NAD-dependent l-glutamate dehydrogenase from the psychrophile Janthinobacterium lividum, isolated from cold soil. J Bacteriol. 2007;189:5626–33.View ArticlePubMedPubMed CentralGoogle Scholar
- Schloss PD, Allen HK, Klimowicz AK, Mlot C, Gross JA, et al. Psychrotrophic strain of Janthinobacterium lividum from a cold Alaskan soil produces prodigiosin. DNA Cell Biol. 2010;29:533–41.View ArticlePubMedGoogle Scholar
- Breznak JA, Costilow RN. Physicochemical factors in growth. In: Gerhard P, Murray RGE, Wood WA, Krieg NR, editors. Methods for General and Molecular Bacteriology. Washington: American Society of Microbiology; 2007. p. 137–54.Google Scholar
- Andersen K, Kjær T, Revsbech NP. An oxygen insensitive microsensor for nitrous oxide. Sensors Actuators B Chem. 2001;81:42–8.View ArticleGoogle Scholar
- Widdel F, Bak F. Gram-negative mesophilic sulfate-reducing bacteria. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer K-H, editors. The Prokaryotes. New York: Springer; 1992. p. 3352–78.View ArticleGoogle Scholar
- Pantanella F, Berlutti F, Passariello C, Sarli S, Morea C, Schippa S. Violacein and biofilm production in Janthinobacterium lividum. J Appl Microbiol. 2007;102:992–9.PubMedGoogle Scholar
- Lincoln SP, Fermor TR, Tindall BJ. Janthinobacterium agaricidamnosum sp. nov., a soft rot pathogen of Agaricus bisporus. Int. J Syst Bacteriol. 1999;49:1577–89.View ArticleGoogle Scholar
- Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114–20.View ArticlePubMedPubMed CentralGoogle Scholar
- Babraham Bioinformatics - FastQC. Available at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc/. Accessed October 20, 2015.
- Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19:455–77.View ArticlePubMedPubMed CentralGoogle Scholar
- Huntemann M, Ivanova NN, Mavromatis K, Tripp HJ, Paez-Espino D, et al. The standard operating procedure of the DOE-JGI Microbial Genome Annotation Pipeline (MGAP v.4). Stand. Genomic Sci. 2015;10:86.View ArticleGoogle Scholar
- Bland C, Ramsey TL, Sabree F, Lowe M, Brown K, et al. CRISPR Recognition Tool (CRT): a tool for automatic detection of clustered regularly interspaced palindromic repeats. BMC Bioinformatics. 2007;8:209.View ArticlePubMedPubMed CentralGoogle Scholar
- Edgar RC. PILER-CR: fast and accurate identification of CRISPR repeats. BMC Bioinformatics. 2007;8:18.View ArticlePubMedPubMed CentralGoogle Scholar
- 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
- Eddy SR. Accelerated profile HMM searches. PLoS Comput Biol. 2011;7(10):e1002195.View ArticlePubMedPubMed CentralGoogle Scholar
- Hyatt D, Chen G-L, Locascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics. 2010;11:119.View ArticlePubMedPubMed CentralGoogle Scholar
- Marchler-Bauer A, Anderson JB, Derbyshire MK, DeWeese-Scott C, Gonzales NR, et al. CDD: a conserved domain database for interactive domain family analysis. Nucleic Acids Res. 2007;35:D237–40.View ArticlePubMedGoogle Scholar
- Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M. Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res. 2014;42:D199–205.View ArticlePubMedGoogle Scholar
- Caspi R, Altman T, Billington R, Dreher K, Foerster H, et al. The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of Pathway/Genome Databases. Nucleic Acids Res. 2014;42:D459–71.View ArticlePubMedGoogle Scholar
- Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, et al. The Pfam protein families database. Nucleic Acids Res. 2012;40:D290–301.View ArticlePubMedGoogle Scholar
- Haft DH, Selengut JD, Richter RA, Harkins D, Basu MK, Beck E. TIGRFAMs and genome properties in 2013. Nucleic Acids Res. 2013;41:D387–95.View ArticlePubMedGoogle Scholar
- Jones P, Binns D, Chang H-Y, Fraser M, Li W, et al. InterProScan 5: genome-scale protein function classification. Bioinformatics. 2014;30:1236–40.View ArticlePubMedPubMed CentralGoogle Scholar
- Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics. 2013;14:60.View ArticlePubMedPubMed CentralGoogle Scholar
- Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015: doi:10.1101/gr.186072.114.
- Meier-Kolthoff JP, Göker M, Spröer C, Klenk H-P. When should a DDH experiment be mandatory in microbial taxonomy? Arch Microbiol. 2013;195:413–8.View ArticlePubMedGoogle Scholar
- Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol. 2007;57:81–91.View ArticlePubMedGoogle Scholar
- Rodriguez-R LM, Konstantinidis KT. Bypassing cultivation to identify bacterial species. Microbe Mag. 2014;9:111–8.View ArticleGoogle Scholar
- Cole JR, Wang Q, Cardenas E, Fish J, Chai B, et al. The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 2009;37:D141–5.View ArticlePubMedGoogle Scholar
- Ludwig W, Strunk O, Westram R, Richter L, Meier H, et al. ARB: a software environment for sequence data. Nucleic Acids Res. 2004;32:1363–71.View ArticlePubMedPubMed CentralGoogle Scholar
- Stamatakis A, Hoover P, Rougemont J. A rapid bootstrap algorithm for the RAxML web servers. Syst Biol. 2008;57:758–71.View ArticlePubMedGoogle Scholar
- Field D, Garrity G, Gray T, Morrison N, Selengut J, et al. The minimum information about a genome sequence (MIGS) specification. Nat Biotechnol. 2008;26:541–7.View ArticlePubMedPubMed CentralGoogle Scholar
- Woese CR, Kandler O, Wheelis ML. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci. 1990;87:4576–9.View ArticlePubMedPubMed CentralGoogle Scholar
- Garrity GM, Bell JA, Lilburn TE. Phylum XIV. Proteobacteria phyl. In: Garrity GM, Brenner DJ, Krieg NR, Staley JT, editors. Bergey’s Manual of Systematic Bacteriology, vol. 1. 2nd ed. New York: Springer; 2005. p. 1.View ArticleGoogle Scholar
- Garrity GM, Bell JA, Lilburn TE. Class II. Betaproteobacteria. In: Garrity GM, Brenner DJ, Krieg NR, Staley JT, editors. Bergey’s Manual of Systematic Bacteriology, vol. 1. 2nd ed. New York: Springer; 2005. p. 575.View ArticleGoogle Scholar
- Garrity GM, Bell JA, Lilburn TE. Order 1. Burkholderiales. In: Garrity GM, Brenner DJ, Krieg NR, Staley JT, editors. Bergey’s Manual of Systematic Bacteriology, vol. 1. 2nd ed. New York: Springer; 2005. p. 575.View ArticleGoogle Scholar
- Garrity GM, Bell JA, Lilburn T. Family II. Oxalobacteraceae fam. In: Garrity GM, Brenner DJ, Krieg NR, Staley JT, editors. Bergey’s Manual of Systematic Bacteriology, vol. 1. 2nd ed. New York: Springer; 2005. p. 623.Google Scholar
- Ashburner M, Ball CA, Blake JA, et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000;25:25–9.View ArticlePubMedPubMed CentralGoogle Scholar