Non-contiguous finished genome sequence and contextual data of the filamentous soil bacterium Ktedonobacter racemifer type strain (SOSP1-21T)
- Yun-juan Chang1, 2,
- Miriam Land1, 2,
- Loren Hauser1, 2,
- Olga Chertkov2, 3,
- Tijana Glavina Del Rio2,
- Matt Nolan2,
- Alex Copeland2,
- Hope Tice2,
- Jan-Fang Cheng2,
- Susan Lucas2,
- Cliff Han2, 3,
- Lynne Goodwin2, 3,
- Sam Pitluck2,
- Natalia Ivanova2,
- Galina Ovchinikova2,
- Amrita Pati2,
- Amy Chen4,
- Krishna Palaniappan4,
- Konstantinos Mavromatis2,
- Konstantinos Liolios2,
- Thomas Brettin2, 3,
- Anne Fiebig5,
- Manfred Rohde6,
- Birte Abt5,
- Markus Göker5,
- John C. Detter2, 3,
- Tanja Woyke2,
- James Bristow2,
- Jonathan A. Eisen2, 7,
- Victor Markowitz4,
- Philip Hugenholtz2, 8,
- Nikos C. Kyrpides2,
- Hans-Peter Klenk5 and
- Alla Lapidus2
© The Author(s) 2011
Published: 15 October 2011
Ktedonobacter racemifer corrig. Cavaletti et al. 2007 is the type species of the genus Ktedonobacter, which in turn is the type genus of the family Ktedonobacteraceae, the type family of the order Ktedonobacterales within the class Ktedonobacteria in the phylum ‘Chloroflexi’. Although K. racemifer shares some morphological features with the actinobacteria, it is of special interest because it was the first cultivated representative of a deep branching unclassified lineage of otherwise uncultivated environmental phylotypes tentatively located within the phylum ‘Chloroflexi’. The aerobic, filamentous, non-motile, spore-forming Gram-positive heterotroph was isolated from soil in Italy. The 13,661,586 bp long non-contiguous finished genome consists of ten contigs and is the first reported genome sequence from a member of the class Ktedonobacteria. With its 11,453 protein-coding and 87 RNA genes, it is the largest prokaryotic genome reported so far. It comprises a large number of over-represented COGs, particularly genes associated with transposons, causing the genetic redundancy within the genome being considerably larger than expected by chance. This work is a part of the Genomic Encyclopedia of Bacteria and Archaea project.
Keywordsaerobic heterotrophic filamentous non-motile Gram-positive moderately acidophilic sporulating transposon broken-stick distribution entropy Ktedonobacteraceae Chloroflexi GEBA
Strain SOSP1-21T (= DSM 44963 = NRRL B-41538) is the type strain of the species Ktedonobacter racemifer, which is the type species of the monotypic genus Ktedonobacter, the type genus of the family Ktedonobacteraceae . K. racemifer was first described in 2006 [1,2] as an aerobic, non-motile, filamentous, mesophilic, Gram-positive heterotroph also capable of growing under microaerophilic conditions . The genus name was derived from the Greek word ktedon-onos, fiber, and the Neo-Latin bacter, a rod, meaning a filamentous rod . The species epithet is derived from the Latin adjective racemifer, carrying clusters of grapes .
The original spelling, Ktedobacter racemifer was corrected in 2007 on validation according to Rule 61 and Recommendation 6(7) . Strain SOSP1-21T was originally isolated from a soil sample of a black locust wood in Gerenzano, Northern Italy. Ten phylogenetically (class level) related strains were also isolated from soil samples collected at different locations in Northern Italy . Only recently, a nearest cultivated neighbor, Thermosporothrix hazakensis, was isolated from hot compost in Japan . Here we present a summary classification and a set of features for K. racemifer strain SOSP1-21T, together with the description of the complete genomic sequencing and annotation.
Classification and features
Using NCBI BLAST , a representative genomic 16S rRNA sequence of K. racemifer SOSP1-21T was compared 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  and the relative frequencies of taxa and keywords (reduced to their stem ) were determined, weighted by BLAST scores. The most frequently occurring genus was ‘Ktedobacter’ (100.0%) (1 hit in total; this represents the original, incorrect spelling of Ktedonobacter). No hits to sequences with (other) species names were found. (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 AM180157 (‘New lineage filamentous spore-forming soil isolate SOSP1-30SOSP1-30 str. SOSP1-30’), which showed an identity of 99.0% and an HSP coverage of 95.2%. The most frequently occurring keywords within the labels of environmental samples which yielded hits were ‘soil’ (11.2%), ‘prari, tallgrass’ (4.9%), ‘miner, weather’ (1.9%), ‘new’ (1.8%) and ‘filament, lineag, spore-form’ (1.6%) (249 hits in total). These keywords reflect some of the ecological properties reported for strain SOSP1-21T in the original description . Environmental samples which yielded hits of a higher score than the highest scoring species were not found.
Strain SOSP1-21T was capable of hydrolyzing starch, casein, gelatin, and (to a lesser extent) keratin but not cellulose, xylan, or chitin . Strain SOSP1-21T was catalase positive and produced H2S but could not reduce nitrates . It is sensitive to 5 ug/ml novobiocin or ramoplanin and to 20 mg/ml apramycin and the glycopeptide A40926.
Species Ktedonobacter racemifer
Type strain SOSP1-21
NaCl up to 10 g/l growth w/o problem, inhibited at 30 g/l
aerobic and microaerophilic
sugars and peptides
soil from a black locust wood
Gerenzano, Northern Italy
Sample collection time
about 210 m
Genome sequencing and annotation
Genome project history
Genome sequencing project information
Two Sanger 8 kb pMCL200 and fosmid libraries; one 454 pyrosequence standard library
ABI3730, 454 GS FLX
10.1 × Sanger; 24.6 × pyrosequence
Newbler version 1.1.02.15, phrap
Gene calling method
Prodigal 1.4, Genemark 4.6b, tRNAScan-SE-1.23, infernal 0.81
Genbank Date of Release
June 14, 2010
NCBI project ID
Source material identifier
Tree of Life, GEBA
Growth conditions and DNA isolation
K. racemifer SOSP1-21T, DSM 44963, was grown in DSMZ medium 65 (GYM Streptomyces medium)  adjusted to pH 6.0, at 28°C. DNA was isolated from 0.5–1 g of cell paste using Qiagen Genomic 500 DNA Kit (Qiagen 10262) following the manufacturer’s protocol, with cell lysis protocol st/LALMP as described in Wu et al. . DNA is available through the DNA Bank Network .
Genome sequencing and assembly
The genome was sequenced using a combination of Sanger and 454 sequencing platforms. All general aspects of library construction and sequencing can be found at the JGI website . Pyrosequencing reads were assembled using the Newbler assembler (Roche). The initial Newbler contigs were broken into 14,080 overlapping fragments of 1,000 bp and entered as pseudo-reads into the subsequence assembly. The sequences were assigned quality scores based on Newbler consensus q-scores with modifications to account for overlap redundancy and to adjust inflated q-scores. A hybrid 454/Sanger assembly was produced using parallel phrap (High Performance Software, LLC). Possible mis-assemblies were corrected with Dupfinisher , or transposon bombing of bridging clones (Epicentre Biotechnologies, Madison, WI) . Some gaps between contigs were closed by editing in Consed , custom primer walking or PCR amplification. A total of 3,354 Sanger finishing reads and five shatter libraries were produced to close gaps, to resolve some repetitive regions, 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 . The error rate of the completed genome sequence is less than 1 in 100,000. Together, the combination of the Sanger and 454 sequencing platforms provided 34.7 × coverage of the genome. The final assembly contained 165,050 pyrosequence and 2,305,667 Illumina reads.
Genes were identified using Prodigal  as part of the Oak Ridge National Laboratory genome annotation pipeline, followed by a round of manual curation using the JGI GenePRIMP 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. Additional gene prediction analysis and functional annotation were performed within the Integrated Microbial Genomes - Expert Review (IMG-ER) platform .
% of Total
Genome size (bp)
DNA coding region (bp)
DNA G+C content (bp)
Number of contigs
Genes with function prediction
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, 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 from the genome sequence
Lacking an available genome sequence of the closest relative of K. racemifer, Thermosporothrix hazakensis  (Figure 1), the following comparative analyses were done with Sphaerobacter thermophilus  and Thermomicrobium roseum , the closest organisms phylogenetically for which there are publically available genome sequences [15,16].
K. racemifer stands out because of its enormous genome size of more than 13 Mbp. The genomes of S. thermophilus and T. roseum are significantly smaller, 3.9 Mbp and 2.9 Mbp, respectively. Whereas S. thermophilus and T. roseum have similar G+C-contents of 68% and 64%, respectively, the G+C-content of the K. racemifer genome is significantly lower (54%).
A total of 1,393 genes are shared by the three genomes, referring to the whole genome sizes 39% and 48% of the genes in S. thermophilus and T. roseum have homologs in the three genomes, in the case of K. racemifer only 12% of the genes are shared by the other two genomes. The pairwise comparison of S. thermophilus and T. roseum revealed 2,249 genes which are shared by these two organisms, referring to the whole genomes 64% of the S. thermophilus genes and 79% of the T. roseum have homologous genes in the respective other genome.
The genome of K. racemifer encodes an enormously high number of transposon-associated genes; its annotation revealed 601 genes encoding transposases, 151 genes encoding integrases and 107 genes encoding resolvases. The genes coding these enzymes are spread over the whole genome with some regions having a higher density than others. The extremely high number of transposases is due to several gene copies that are to a greater or lesser extent similar in their sequences. The presence of that many mobile elements may explain the unusually high number of identical sequence fragments across the genome and the resulting difficulties occurring during the genome assembly.
Within the 9,539 unique genes of K. racemifer that have no detectable homologs in the genomes of S. thermophilus and T. roseum (under the sequence similarity thresholds used for the comparison) the 29 genes encoding xylose isomerases appear to be especially noteworthy; for 27 of these isomerase genes no homologous genes were detected in the other two genomes; only one gene was identified in T. roseum, and two in S. thermophilus. The high number of xylose isomerase genes suggests a strong utilization of pentoses by K. racemifer. To date K. racemifer was not tested regarding xylose utilization, but the close relative T. hazakensis is able to use xylose as the only carbon source . Furthermore, a high number of genes encoding proteins responsible for resistance against several antibiotics were predicted: 61 bleomycin resistance proteins and 41 aminoglycoside phosphotransferases.
Pairwise comparison of K. racemifer, S. thermophilus and T. roseum using the GGDC-Calculator.
HSP length / total length [%]
identities / HSP length [%]
identities / total length [%]
The pairwise comparison (Table 5) of the genomes of K. racemifer with S. thermophilus and T. roseum revealed that only 0.57% and 0.48% of the average of the genome lengths are covered with HSPs. The identity within these HSPs was 86.4% and 87.2%, whereas the identity over the whole genome was only 0.50% and 0.42%, respectively. The comparison of T. roseum with S. thermophilus revealed that 9.41% of the average of both genome lengths are covered with HSPs, with an identity within these HSPs of 83.1%. The identity over the whole genome is 7.82%. These results show how distant the relationship between K. racemifer and S. thermophilus and T. roseum, respectively, is, if genome sizes are taken into consideration.
In order to quantify the differences in gene redundancy between the three genomes, as well as to determine over-represented genes, we used approaches based on entropy and the broken-stick distribution, respectively, applied to the set of genes from either genome assigned to COGs. Shannon’s entropy (see, e.g., pp. 214, 243 in ) H can be used as a measure of disorder for discrete distributions; it is maximum (H max ) if all categories (COGs in our case) are represented by exactly one item (gene) and then equal to the logarithm of the number of items (genes).
Thus, one can measure the evenness (non-redundancy) within such a distribution as H/H max and the corresponding redundancy as 1.0 − H/H max . The broken-stick distribution reflects the relative abundance of a given number of categories within a random population of items (see, e.g., p. 244 and 410 in ). Over-represented items (here: COGs) are those whose real relative frequencies (here: number of genes assigned to this COG relative to the total number of genes assigned to COGs) are larger than the broken-stick value of the corresponding rank within the list of frequencies sorted in decreasing order. Moreover, the entropy H exp of the broken-stick distribution can be used as an estimate for the expected entropy, yielding 1.0 − H/H exp as an alternative measure of redundancy (which becomes negative when the evenness is larger than expected by chance).
The 2,022 genes assigned to 1,300 distinct COGs in the genome of T. roseum corresponded to an entropy of 6.912, an expected entropy of 6.748 and, hence, a redundancy of 9.20% if measured using H max and of −2.42% using H exp , whereas S. thermophilus (2,619 genes assigned to 1,383 COGs) yielded an entropy of 6.837 (expected: 6.810) and a redundancy of 13.14% with H max and −0.39% with H exp . In contrast, the 6,654 genes assigned to 1,731 distinct COGs in the genome of K. racemifer yielded an entropy of only 6.455 (expected: 7.034) and a redundancy of 26.67% (using H max ) and 8.24% (using H exp ). That is, in contrast to the other two genomes the genes within the genome of K. racemifer are distributed less even than expected by chance.
Our analyses also showed that genes belonging to the category COG3344 are over-represented in the genome of K. racemifer. COG3344 represents retron type reverse transcriptases, which are found in group II introns. Group II introns are large catalytic RNA molecules that act as mobile genetic elements . They were first identified in mitochondria and chloroplast genomes, but with the increasing number of bacterial genome sequencing projects, the number of group II intron sequences in the databases also increased. Dai and Zimmerly reported in 2003 that a quarter of the sequenced bacterial genomes contain group II introns [48,49]. By using the IMG-ER platform  we calculated that approximately one third of the 2,727 sequenced bacterial genomes contain group II introns. In the genome of K. racemifer, 34 genes coding reverse transcriptases could be identified, all of them having the same domain structure with the reverse transcriptase domain followed by a maturase-specific domain and the C-terminal HNH-endonuclease domain.
We would like to gratefully acknowledge the help of Marlen Jando for growing K. racemifer cultures and Susanne Schneider for DNA extraction and quality control (both at DSMZ). This work was performed under the auspices of the US Department of Energy’s Office of Science, Biological and Environmental Research Program, and by the University of California, Lawrence Berkeley National Laboratory under contract No. DE-AC02-05CH11231, Lawrence Livermore National Laboratory under Contract No. DE-AC52-07NA27344, and Los Alamos National Laboratory under contract No. DE-AC02-06NA25396, UT-Battelle and Oak Ridge National Laboratory under contract DE-AC05-00OR22725, as well as German Research Foundation (DFG) INST 599/1-1.
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