Genome sequence of the reddish-pigmented Rubellimicrobium thermophilum type strain (DSM 16684T), a member of the Roseobacter clade
© The Author(s) 2013
Published: 30 July 2013
Rubellimicrobium thermophilum Denner et al. 2006 is the type species of the genus Rubellimicrobium, a representative of the Roseobacter clade within the Rhodobacteraceae. Members of this clade were shown to be abundant especially in coastal and polar waters, but were also found in microbial mats and sediments. They are metabolically versatile and form a physiologically heterogeneous group within the Alphaproteobacteria. Strain C-Ivk-R2A-2T was isolated from colored deposits in a pulp dryer; however, its natural habitat is so far unknown. Here we describe the features of this organism, together with the draft genome sequence and annotation and novel aspects of its phenotype. The 3,161,245 bp long genome contains 3,243 protein-coding and 45 RNA genes.
Strain C-Ivk-R2A-2T (= DSM 16684 = CCUG 51817 = HAMBI 2421) is the type strain of the species Rubellimicrobium thermophilum . The genus name Rubellimicrobium was derived from the Neo-Latin adjective ‘rubellus’, red or reddish, and the Neo-Latin noun ‘microbium’, microbe, referring to its reddish pigmentation. The species epithet was derived from the Greek noun ‘thermê’, heat, as well as from the Neo-Latin adjective ‘philus –a –um’, friend/loving, referring to its growth temperature . C-Ivk-R2A-2T was isolated from colored deposits in a pulp dryer in Finland, so the natural habitat is so far unknown . At the time of writing, PubMed records did not indicate any follow-up research with strain C-Ivk-R2A-2T after the initial description and valid publication of the new name Rubellimicrobium thermophilum . Here we present a summary classification and a set of features for R. thermophilum C-Ivk-R2A-2T, together with the description of the genomic sequencing and annotation. We also describe novel aspects of its phenotype.
Features of the organism
16S rRNA gene analysis
Morphology and physiology
The cells of strain C-Ivk-R2A-2T assimilate the following compounds: L-arabinose, p-arbutin, D-cellobiose, D-fructose, D-galactose, gluconate, D-glucose, D-mannose, D-maltose, α-D-melibiose, D-rhamnose, D-ribose, sucrose, salicin, D-trehalose, D-xylose, adonitol, myo-inositol, maltitol, D-mannitol, D-sorbitol, acetate, 4-aminobutyrate, glutarate, DL-3-hydroxybutyrate, DL-lactate, L-malate, oxoglutarate, pyruvate, L-alanine, L-ornithine and L-proline. Cells do not produce acid from D-glucose, lactose, sucrose, L-arabinose, L-rhamnose, maltose, D-xylose, cellobiose, D-mannitol, dulcitol, salicin, adonitol, myo-inositol, sorbitol, raffinose, trehalose, methyl α-D-glucoside, erythritol, melibiose, D-arabitol or D-mannose . The strain does not assimilate the following compounds: N-acetyl-D-glucosamine, putrescine, propionate, cis- and trans-aconitate, adipate, azelate, citrate, fumarate, itaconate, mesaconate, suberate, β-alanine, L-aspartate, L-histidine, L-leucine, L-phenylalanine, L-serine, L-tryptophan, 3- and 4-hydroxybenzoate and phenylacetate . The following compounds are hydrolyzed by strain C-Ivk-R2A-2T: p-nitrophenyl (pNP) α-d-glucopyranoside, pNP β-D-glucopyranoside, bis-pNP phosphate, pNP phenylphosphonate and L-alanine p-nitroanilide (pNA), whereas aesculin, pNP β-D-galactopyranoside, pNP β-D-glucuronide, pNP phosphorylcholine, 2-deoxythymidine-5′-pNP phosphate, L-glutamate-γ-3-carboxy pNA, L-proline pNA, Tween 80, starch and casein are not hydrolyzed .
Strain C-Ivk-R2A-2T was also found to be susceptible to ampicillin, chloramphenicol, colistin sulfate, gentamicin, kanamycin, lincomycin, neomycin, nitrofurantoin, penicillin G, polymyxin B, streptomycin, tetracycline and vancomycin .
The physiology of R. thermophilum DSM 16684T was investigated in this study using Generation-III microplates in an OmniLog phenotyping device (BIOLOG Inc., Hayward, CA, USA). The microplates were inoculated at 28°C and 37°C, respectively, with a cell suspension at a cell density of 95–96% turbidity and dye IF-A. Further additives were vitamin, micronutrient and sea-salt solutions. The plates were sealed with parafilm to avoid a loss of fluid. The exported measurement data were further analyzed with the opm package for R [23,24], using its functionality for statistically estimating parameters from the respiration curves such as the maximum height, and automatically translating these values into negative and positive reactions.
At 28°C, the strain was positive for D-turanose, pH 6, 1% NaCl, 4% NaCl, D-galactose, 3-O-methyl-D-glucose, D-fucose, L-fucose, L-rhamnose, 1% sodium lactate, myo-inositol, rifamycin SV, L-aspartic acid, L-glutamic acid, L-histidine, L-serine, D-glucuronic acid, quinic acid, L-lactic acid, citric acid, α-keto-glutaric acid, D-malic acid, L-malic acid, nalidixic acid, potassium tellurite, acetoacetic acid and sodium formate. The strain was negative for dextrin, D-maltose, D-trehalose, D-cellobiose, β-gentiobiose, sucrose, stachyose, pH 5, D-raffinose, α-D-lactose, D-melibiose, β-methyl-D-galactoside, D-salicin, N-acetyl-D-glucosamine, N-acetyl-β-D-mannosamine, N-acetyl-D-galactosamine, N-acetyl-neuraminic acid, 8% NaCl, D-glucose, D-mannose, D-fructose, inosine, fusidic acid, D-serine, D-sorbitol, D-mannitol, D-arabitol, glycerol, D-glucose-6-phosphate, D-fructose-6-phosphate, D-aspartic acid, D-serine, troleandomycin, minocycline, gelatin, glycyl-L-proline, L-alanine, L-arginine, L-pyroglutamic acid, lincomycin, guanidine hydrochloride, niaproof, pectin, D-galacturonic acid, L-galactonic acid-γ-lactone, D-gluconic acid, glucuronamide, mucic acid, D-saccharic acid, vancomycin, tetrazolium violet, tetrazolium blue, p-hydroxy-phenylacetic acid, methyl pyruvate, D-lactic acid methyl ester, bromo-succinic acid, lithium chloride, tween 40, γ-amino-n-butyric acid, α-hydroxy-butyric acid, β-hydroxy-butyric acid, α-keto-butyric acid, propionic acid, acetic acid, aztreonam, butyric acid and sodium bromate.
At 37°C, the strain was positive for D-maltose, D-trehalose, D-cellobiose, β-gentiobiose, sucrose, D-turanose, stachyose, pH 6, D-raffinose, D-melibiose, β-methyl-D-galactoside, D-salicin, 1% NaCl, 4% NaCl, D-glucose, D-mannose, D-fructose, D-galactose, 3-O-methyl-D-glucose, D-fucose, L-fucose, L-rhamnose, inosine, 1% sodium lactate, D-sorbitol, D-mannitol, D-arabitol, myo-inositol, glycerol, rifamycin SV, L-alanine, L-arginine, L-aspartic acid, L-glutamic acid, L-histidine, L-serine, pectin, D-gluconic acid, D-glucuronic acid, glucuronamide, quinic acid, methyl pyruvate, L-lactic acid, citric acid, α-keto-glutaric acid, D-malic acid, L-malic acid, nalidixic acid, potassium tellurite, tween 40, γ-amino-n-butyric acid, β-hydroxy-butyric acid, propionic acid, acetic acid and sodium formate. No reactions could be observed for dextrin, pH 5, α-D-lactose, N-acetyl-D-glucosamine, N-acetyl-β-D-mannosamine, N-acetyl-D-galactosamine, N-acetyl-neuraminic acid, 8% NaCl, fusidic acid, D-serine, D-glucose-6-phosphate, D-fructose-6-phosphate, D-aspartic acid, D-serine, troleandomycin, minocycline, gelatin, glycyl-L-proline, L-pyroglutamic acid, lincomycin, guanidine hydrochloride, niaproof, D-galacturonic acid, L-galactonic acid-γ-lactone, mucic acid, D-saccharic acid, vancomycin, tetrazolium violet, tetrazolium blue, p-hydroxy-phenylacetic acid, D-lactic acid methyl ester, bromo-succinic acid, lithium chloride, α-hydroxy-butyric acid, α-keto-butyric acid, acetoacetic acid, aztreonam, butyric acid and sodium bromate.
According to , R. thermophilum is able to metabolize a wide range of carbon sources. This observation is not fully confirmed by the OmniLog measurements at 28°C. For instance, more than eleven sugars were not metabolized under the given cultivation conditions in the Generation-III microplates. This is apparently caused by distinct cultivation conditions, because the behavior is in high agreement with  if a temperature of 37°C is chosen, which is closer to the reported optimum temperature . Particularly the optimal growth temperature of 45°C highly differs from the one that had to be used in the OmniLog assays (28°C). Conversely, in contrast to  the OmniLog measurements yielded positive reactions for citrate, L-histidine and L-serine at 28°C and additionally for propionate at 37°C. This may be due to the higher sensitivity of respiratory measurements compared to growth measurements [24,25].
The principal cellular fatty acids of strain C-Ivk-R2A-2T are C19:0 cycloω7c (43.9 %), C16:0 (22.3 %), C18:0 (22.0 %), C18:1ω7c (4.5 %), C10:0 3-OH (1.2 %), C18:1ω7c 11-methyl (0.9 %), C20:2ω6,9c (0.7 %), C17:0 cyclo (0.5 %)C17:0 (0.4 %) and summed feature 2 containing C16:1 iso I and/or C14:0 3-OH (1.2 %). Two unknown fatty acids are identified by their equivalent chain length (ECL): ECL 11.799 (2.3 %) as well as ECL 17.322 (0.7 %) .
Additionally, ubiquinone Q-10 is the predominant respiratory lipoquinone, but ubiquinone Q-9 was also detected in minor amounts .
Classification and general features of R. thermophilum C-Ivk-R2A-2T according to the MIGS recommendations .
Species Rubellimicrobium thermophilum
Type strain C-Ivk-R2A-2T
Relationship to oxygen
mono- and polysaccharides
colored deposits in a pulp dryer
Genome sequencing and annotation
Genome project history
Genome sequencing project information
Two genomic libraries: one Illumina PE library (456 bp insert size), one 454 PE library (3kb insert size)
Illumina GAIIx, 454 GS-FLX + Titanium (Roche)
Velvet version 1.1.36, Newbler version 2.3, consed 20.0
Gene calling method
GenBank Date of Release
July 31, 2013
NCBI project ID
Source material identifier
Tree of Life, biodiversity
Growth conditions and DNA isolation
A culture of DSM 16684T was grown aerobically in DSMZ medium 830 (R2A medium)  at 45°C. Genomic DNA was isolated using Jetflex Genomic DNA Purification Kit (GENOMED 600100) following the standard protocol provided by the manufacturer but modified by an incubation time of 60 min, the incubation on ice over night on a shaker, the use of additional 50 µl proteinase K, and the addition of 100 µl protein precipitation buffer. DNA is available from DSMZ through the DNA Bank Network .
Genome sequencing and assembly
The genome was sequenced using a combination of Illumina and 454 libraries (Table 2). Illumina sequencing was performed on a GA IIx platform with 150 cycles. The paired-end library contained inserts of 456 nt length in average. To correct sequencing errors and improve quality of the reads, clipping was performed using fastq-mcf  and quake . The remaining 4,190,250 reads with an average length of 106 nt were assembled using Velvet . To gain information on the contig arrangement an additional 454 run was performed. The paired-end jumping library of 3 kb insert size was sequenced on a 1/8 lane. Pyrosequencing resulted in 115,925 reads, with an average read length of 451 nt, assembled with Newbler (Roche Diagnostics) into a draft assembly comprising 36 scaffolds. Both draft assemblies (Illumina and 454 sequences) were fractionated into artificial Sanger reads of 1000 nt in length plus 75 nt overlap on each site. These artificial reads served as an input for the phred/phrap/consed package . By manual editing the number of contigs was reduced to 43 organized in ten scaffolds. The combined sequences provided a 203 × coverage of the genome.
Genes were identified using Prodigal  as part of the JGI genome annotation pipeline . 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. Identification of RNA genes were carried out by using HMMER 3.0rc1  (rRNAs) and tRNAscan-SE 1.23  (tRNAs). Other non-coding genes were predicted using INFERNAL 1.0.2  Additional gene prediction analysis and functional annotation was performed within the Integrated Microbial Genomes - Expert Review (IMG-ER) platform . CRISPR elements were detected using CRT  and PILER-CR .
% of Total
Genome size (bp)
DNA coding region (bp)
DNA G+C content (bp)
Number of scaffolds
Genes with function prediction (proteins)
Genes in paralog clusters
Genes assigned to COGs
Genes assigned Pfam domains
Genes with signal peptides
Genes with transmembrane helices
Number of genes associated with the 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/envelope biogenesis
Intracellular trafficking and secretion, and vesicular transport
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 into the genome
The ten scaffolds of the draft genome sequence of strain C-Ivk-R2A-2T were screened with BLAST for the presence of the four abundant plasmid replicases from the Rhodobacterales, representing DnaA-like, RepABC-, RepA- and RepB-type replicons . None of these typical extrachromosomal elements was detected.
Prophage-like structures have been found in many bacteria and they are known to drive the diversity of bacteria by facilitating lateral gene transfer . Genome analysis of strain DSM 16684T revealed the presence of several genes encoding proteins associated with prophages (ruthe_00218 to 00220, ruthe_00605, ruthe_00607 to 00610, ruthe_00612, ruthe_00614, ruthe_00617, ruthe_00618, ruthe_00620, ruthe_2061, ruthe_2066, ruthe_02072, ruthe_02185, ruthe_02480, ruthe_02482 to 02484, ruthe_02495, ruthe_02499, ruthe_02502, ruthe_02972, ruthe_02974, ruthe_02976, ruthe_02977, ruthe_02984, ruthe_02988, and ruthe_02991 to 03295).
The soxB gene (ruthe_01788) encodes a component of the thiosulfate-oxidizing Sox enzyme complex, which is known to be part of the genomes of various groups of bacteria . Several other genes involved in this process were also detected (e.g. ruthe_01784, ruthe_01785 and ruthe_01786).
Genome analysis of strain R. thermophilum DSM 16684T further revealed the presence of several genes encoding proteins associated with the utilization of urease (ruthe_02149 to 02151, ruthe_02153 to 02156). Several genes encoding proteins involved in the transport of Fe3+-siderophores and Fe3+-hydroxamate via ABC-transporters were also detected (e.g. ruthe_03167 to 03172).
Additionally, several gene sequences associated with CRISPRs (ruthe_02227 to 02230, ruthe_02232 to 02234, ruthe_02250, ruthe_02251, ruthe_02253 and ruthe_02255), cytochrome c oxidase activity (ruthe_00413 to 00417), cytochrome cbb3 oxidase activity (ruthe_01647 to 01654) as well as cytochrome bd-I ubiquinol oxidase activity (ruthe_01776, ruthe_01777) were found.
Additional gene sequences of interest encode a predicted ring-cleavage extradiol dioxygenase (ruthe_00477), which indicates a possible degradation of aromatic compounds. A sensor of blue light using FAD (BLUF, ruthe_01818) was also found, indicating possible blue-light dependent signal transduction.
The authors gratefully acknowledge the assistance of Iljana Schröder for growing R. thermophilum DSM 16684T cultures and Meike Döppner for DNA extraction and quality control (both at the DSMZ). This work was performed under the auspices of the German Research Foundation (DFG) Transregio-SFB 51 Roseobacter grant.
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