Genome sequence of the marine bacterium Corynebacterium maris type strain Coryn-1T (= DSM 45190T)
© The Author(s) 2013
Published: 30 July 2013
Corynebacterium maris Coryn-1T Ben-Dov et al. 2009 is a member of the genus Corynebacterium which contains Gram-positive, non-spore forming bacteria with a high G+C content. C. maris was isolated from the mucus of the Scleractinian coral Fungia granulosa and belongs to the aerobic and non-haemolytic corynebacteria. It displays tolerance to salts (up to 10%) and is related to the soil bacterium Corynebacterium halotolerans. As this is a type strain in a subgroup of Corynebacterium without complete genome sequences, this project, describing the 2.78 Mbp long chromosome and the 45.97 kbp plasmid pCmaris1, with their 2,584 protein-coding and 67 RNA genes, will aid the Genomic Encyclopedia of Bacteria and Archaea project.
Keywordsaerobic non-motile Gram-positive non-spore forming non-hemolytic heterotrophic mesophilic halotolerant
Strain Coryn-1T (= DSM 45190T) is the type strain of the species Corynebacterium maris originally isolated from the mucus of the coral Fungia granulosa from the Gulf of Eilat (Red Sea, Israel) . The genus Corynebacterium is comprised of Gram-positive bacteria with a high G+C content. It currently contains over 80 members  isolated from diverse backgrounds like human clinical samples  and animals , but also from soil  and ripening cheese .
Within this diverse genus, C. maris has been proposed to form a distinct lineage with C. halotolerans YIM 70093T demonstrating 94% similarity related to the 16S rRNA gene sequences . Similar to the closest phylogenetic relative C. halotolerans, which displays the highest resistance to salt described for the genus Corynebacterium to date, C. maris Coryn-1T is able to live under conditions with high salinity. This species grows on LB agar plates with salinity ranging between 0 and 10%. Optimal growth was detected between 0.5 and 4.0% . Aside from this Coryn-1T is an alkaline-tolerant bacterium, which grows well at pH 7.2–9.0 (optimum pH 7.2) .
Here we present a summary classification and a set of features for C. maris DSM 45190T, together with the description of the genomic sequencing and annotation.
Classification and features
A representative genomic 16S rRNA sequence of C. maris DSM 45190T was compared to the Ribosomal Database Project database  confirming the initial taxonomic classification. C. maris shows highest similarity to C. halotolerans (94%). Because sequence similarity greater than 97% was not obtained with any member of the genus Corynebacteria, it was suggested that C. maris forms an new novel species, a hypothesis that is backed by other taxonomic classifiers .
Classification and general features of C. maris Coryn-1T according to the MIGS recommendations .
Species Corynebacterium maris
Type-strain Coryne-1T (=DSM 45190T)
0–10% (w/v) NaCl or sea-salt mixture (instant ocean)
maltose, lactulose, β-hydroxybutyric acid, α-ketovaleric acid, Tween 40, phenylethylamine, N-acetyl-d-galactosamine, malonic acid, l-threonine, l-glutamic acid, l-fucose, l-alanyl glycine, inosine, raffinose, d-arabitol, l-asparigine and citric acid
Terminal electron acceptor
mucus of the Scleractinian coral Fungia granulosa
agarsphere culturing technique
Gulf of Eilat, Red Sea, Israel
Sample collection time
E 34° 94′
It is described as non-motile , which coincides with a complete lack of genes associated with ‘cell motility’ (functional category N in COGs table).
Optimal growth of Coryn-1T was shown between 0.5 and 4.0% (w/v) salinity (NaCl or sea-salt mixture); however, ranges between 0 and 10% salinity are accepted . C. maris grows at temperatures between 26–37 °C (optimum at 35 °C). Carbon sources utilized by strain Coryn-1T include maltose, lactulose, β-hydroxybutyric acid, α-ketovaleric acid, Tween 40, phenylethylamine, N-acetyl-d-galactosamine, malonic acid, l-threonine, l-glutamic acid, l-fucose, l-alanyl glycine, inosine, raffinose, d-arabitol, l-asparigine and citric acid were used weakly .
Coryn-1T is susceptible to sulfamethoxazole/trimethoprim, tetracycline, chloramphenicol, erythromycin, ampicillin and meticillin. The strain is resistant to nalidixic acid .
In C. maris cellular fatty acids are composed of 58% oleic acid (C18:1ω9c), 30% palmitic acid (C16:0) and 12% tuberculostearic acid 10-methyl (C18:0). The mycolic acids of C. maris are short-chained, like many but not all corynemycol acids (6% C30, 27% C32, 47% C34 and 20% C36).
The biochemical characterization by Ben-Dov et al.  revealed positive signals for the following enzymes/reactions: alkaline phosphatase, esterase (C4), esterase lipase (C8), lipase (C14), leucine arylamidase, α-glucosidase, pyrazinamidase, pyrrolidonyl arylamidase, and gelatin hydrolysis activities.
Genome sequencing and annotation
Genome project history
Genome sequencing project information
Nextera DNA Sample Prep Kit
Newbler version 2.6
Gene calling method
GenBank Date of Release
July 30, 2013
NCBI project ID
Source material identifier
Growth conditions and DNA isolation
C. maris strain Coryn-1T, DSM 45190, was grown aerobically in LB broth (Carl Roth GmbH, Karlsruhe, Germany) at 37 °C. DNA was isolated from ∼ 108 cells using the protocol described by Tauch et al. 1995 .
Genome sequencing and assembly
A WGS library was prepared using the Illumina-Compatible Nextera DNA Sample Prep Kit (Epicentre, WI, U.S.A) according to the manufacturer’s protocol. The library was sequenced in a 2 × 150 bp paired read run on the MiSeq platform, yielding 1,238,702 total reads, providing 56.45× coverage of the genome. Reads were assembled using the Newbler assembler v2.6 (Roche). The initial Newbler assembly consisted of 26 contigs in seven scaffolds. Analysis of the seven scaffolds revealed one to be an extrachromosomal element (plasmid pCmaris1), five to make up the chromosome with the remaining one containing the four copies of the RRN operon which caused the scaffold breaks. The scaffolds were ordered based on alignments to the complete genome of C. halotolerans  and subsequent verification by restriction digestion, Southern blotting and hybridization with a 16S rDNA specific probe.
The Phred/Phrap/Consed software package [27–30] was used for sequence assembly and quality assessment in the subsequent finishing process. After the shotgun stage, gaps between contigs were closed by editing in Consed (for repetitive elements) and by PCR with subsequent Sanger sequencing (IIT Biotech GmbH, Bielefeld, Germany). A total of 67 additional reactions were necessary to close gaps not caused by repetitive elements.
Gene prediction and annotation were done using the PGAAP pipeline . Genes were identified using GeneMark , GLIMMER , and Prodigal . For annotation, BLAST searches against the NCBI Protein Clusters Database  are performed and the annotation is enriched by searches against the Conserved Domain Database  and subsequent assignment of coding sequences to COGs. Non-coding genes and miscellaneous features were predicted using tRNAscan-SE , Infernal , RNAMMer , Rfam , TMHMM , and SignalP .
% of totala
Genome size (bp)
DNA Coding region (bp)
DNA G+C content (bp)
Genes with function prediction (protein)
Genes assigned to COGs
Genes in paralog clusters
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 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
Christian Rückert acknowledges funding through a grant by the Federal Ministry for Eduction and Research (0316017A) within the BioIndustry2021 initiative.
- Ben-Dov E, Ben Yosef DZ, Pavlov V, Kushmaro A. Corynebacterium maris sp. nov., a marine bacterium isolated from the mucus of the coral Fungia granulosa. Int J Syst Evol Microbiol 2009; 59:2458–2463. PubMed http://dx.doi.org/10.1099/ijs.0.007468-0View ArticlePubMedGoogle Scholar
- Euzéby JP. List of Bacterial Names with Standing in Nomenclature: a folder available on the Internet. Int J Syst Bacteriol 1997; 47:590–592. PubMed http://dx.doi.org/10.1099/00207713-47-2-590View ArticlePubMedGoogle Scholar
- Renaud FNR, Aubel D, Riegel P, Meugnier H, Bollet C. Corynebacterium freneyi sp. nov., alpha-glucosidase-positive strains related to Corynebacterium xerosis. Int J Syst Evol Microbiol 2001; 51:1723–1728. PubMed http://dx.doi.org/10.1099/00207713-51-5-1723View ArticlePubMedGoogle Scholar
- Collins MD, Hoyles L, Foster G, Falsen E. Corynebacterium caspium sp. nov., from a Caspian seal (Phoca caspica). Int J Syst Evol Microbiol 2004; 54:925–928. PubMed http://dx.doi.org/10.1099/ijs.0.02950-0View ArticlePubMedGoogle Scholar
- Zhou Z, Yuan M, Tang R, Chen M, Lin M, Zhang W. Corynebacterium deserti sp. nov., isolated from desert sand. Int J Syst Evol Microbiol 2012; 62:791–794. PubMed http://dx.doi.org/10.1099/ijs.0.030429-0View ArticlePubMedGoogle Scholar
- Brennan NM, Brown R, Goodfellow M, Ward AC, Beresford TP, Simpson PJ, Fox PF, Cogan TM. Corynebacterium mooreparkense sp. nov. and Corynebacterium casei sp. nov., isolated from the surface of a smear-ripened cheese. Int J Syst Evol Microbiol 2001; 51:843–852. PubMed http://dx.doi.org/10.1099/00207713-51-3-843View ArticlePubMedGoogle Scholar
- Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, et al. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 2009; 37(Database issue):D141–D145. PubMed http://dx.doi.org/10.1093/nar/gkn879PubMed CentralView ArticlePubMedGoogle Scholar
- Bruno WJ, Socci ND, Halpern AL. Weighted neighbor joining: a likelihood-based approach to distance-based phylogeny reconstruction. Mol Biol Evol 2000; 17:189–197. PubMed http://dx.doi.org/10.1093/oxfordjournals.molbev.a 026231View ArticlePubMedGoogle Scholar
- Cole JR, Chai B, Farris RJ, Wang Q, Kulam-Syed-Mohideen AS, McGarrell DM, Bandela AM, Cardenas E, Garrity GM, Tiedje JM. The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Res 2007; 35(Database issue):D169–D172. PubMed http://dx.doi.org/10.1093/nar/gkl889PubMed CentralView ArticlePubMedGoogle Scholar
- Du ZJ, Jordan EM, Rooney AP, Chen GJ, Austin B. Corynebacterium marinum sp. nov. isolated from coastal sediment. Int J Syst Evol Microbiol 2010; 60:1944–1947. PubMed http://dx.doi.org/10.1099/ijs.0.018523-0View ArticlePubMedGoogle Scholar
- Wu CY, Zhuang L, Zhou SG, Li FB, He J. Corynebacterium humireducens sp. nov., an alkaliphilic, humic acid-reducing bacterium isolated from a microbial fuel cell. Int J Syst Evol Microbiol 2011; 61:882–887. PubMed http://dx.doi.org/10.1099/ijs.0.020909-0View ArticlePubMedGoogle Scholar
- 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
- 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
- Garrity GM, Holt JG. The Road Map to the Manual. In: Garrity GM, Boone DR, Castenholz RW (eds), Bergey’s Manual of Systematic Bacteriology, Second Edition, Volume 1, Springer, New York, 2001, p. 119–169.View ArticleGoogle Scholar
- Stackebrandt E, Rainey FA, Ward-Rainey NL. Proposal for a New Hierarchic Classification System, Actinobacteria classis nov. Int J Syst Bacteriol 1997; 47:479–491. http://dx.doi.org/10.1099/00207713-47-2-479View ArticleGoogle Scholar
- Zhi XY, Li WJ, Stackebrandt E. An update of the structure and 16S rRNA gene sequence-based definition of higher ranks of the class Actinobacteria, with the proposal of two new suborders and four new families and emended descriptions of the existing higher taxa. Int J Syst Evol Microbiol 2009; 59:589–608. PubMed http://dx.doi.org/10.1099/ijs.0.65780-0View ArticlePubMedGoogle Scholar
- Skerman VBD, McGowan V, Sneath PHA. Approved Lists of Bacterial Names. Int J Syst Bacteriol 1980; 30:225–420. http://dx.doi.org/10.1099/00207713-30-1-225View ArticleGoogle Scholar
- Buchanan RE. Studies in the nomenclature and classification of bacteria. II. The primary subdivisions of the Schizomycetes. J Bacteriol 1917; 2:155–164. PubMedPubMed CentralPubMedGoogle Scholar
- Lehmann KB, Neumann R. Lehmann’s Medizin, Handatlanten. X Atlas und Grundriss der Bakteriologie und Lehrbuch der speziellen bakteriologischen Diagnostik., Fourth Edition, Volume 2, J.F. Lehmann, München, 1907, p. 270.Google Scholar
- Bernard KA, Wiebe D, Burdz T, Reimer A, Ng B, Singh C, Schindle S, Pacheco AL. Assignment of Brevibacterium stationis (ZoBell and Upham 1944) Breed 1953 to the genus Corynebacterium, as Corynebacterium stationis comb. nov., and emended description of the genus Corynebacterium to include isolates that can alkalinize citrate. Int J Syst Evol Microbiol 2010; 60:874–879. PubMed http://dx.doi.org/10.1099/ijs.0.012641-0View ArticlePubMedGoogle Scholar
- Lehmann KB, Neumann R. Atlas und Grundriss der Bakteriologie und Lehrbuch der speziellen bakteriologischen Diagnostik, First Edition, J.F. Lehmann, München, 1896, p. 1–448.Google Scholar
- 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. The Gene Ontology Consortium. Nat Genet 2000; 25:25–29. PubMed http://dx.doi.org/10.1038/75556PubMed CentralView ArticlePubMedGoogle Scholar
- 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
- Liolios K, Chen IM, Mavromatis K, Tavernarakis N, Hugenholtz P, Markowitz VM, Kyrpides NC. The Genomes OnLine Database (GOLD) in 2009: status of genomic and metagenomic projects and their associated metadata. Nucleic Acids Res 2010; 38:D346–D354. PubMed http://dx.doi.org/10.1093/nar/gkp848PubMed CentralView ArticlePubMedGoogle Scholar
- Tauch A, Kassing F, Kalinowski J, Pühler A. The Corynebacterium xerosis composite transposon Tn5432 consists of two identical insertion sequences, designated IS1249, flanking the erythromycin resistance gene ermCX. Plasmid 1995; 34:119–131. PubMed http://dx.doi.org/10.1006/plas.1995.9995View ArticlePubMedGoogle Scholar
- Rückert C, Albersmeier A, Al-Dilaimi A, Niehaus K, Szczepanowski R, Kalinowski J. Genome sequence of the halotolerant bacterium Corynebacterium halotolerans type strain YIM 70093(T) (= DSM 44683(T)). Stand Genomic Sci 2012; 7:284–293. PubMed http://dx.doi.org/10.4056/sigs.3236691PubMed CentralView ArticlePubMedGoogle Scholar
- Ewing B, Green P. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 1998; 8:175–185. PubMed http://dx.doi.org/10.1101/gr.8.3.175View ArticlePubMedGoogle Scholar
- Gordon D, Abajian C, Green P. Consed: a graphical tool for sequence finishing. Genome Res 1998; 8:195–202. PubMed http://dx.doi.org/10.1101/gr.8.3.195View ArticlePubMedGoogle Scholar
- Gordon D. Viewing and editing assembled sequences using Consed. Curr Protoc Bioinformatics 2003;Chapter 11:Unit11 2.
- Ewing B, Hillier L, Wendl MC, Green P. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 1998; 8:175–185. PubMed http://dx.doi.org/10.1101/gr.8.3.175View ArticlePubMedGoogle Scholar
- NCBI. 2010 NCBI Prokaryotic Genomes Automatic Annotation Pipeline (PGAAP). http://www.ncbi.nlm.nih.gov/genomes/static/Pipeline.html.
- Borodovsky M, Mills R, Besemer J, Lomsadze A. Prokaryotic gene prediction using GeneMark and GeneMark.hmm. Curr Protoc Bioinformatics 2003;Chapter 4:Unit4 5.
- Delcher AL, Harmon D, Kasif S, White O, Salzberg SL. Improved microbial gene identification with GLIMMER. Nucleic Acids Res 1999; 27:4636–4641. PubMed http://dx.doi.org/10.1093/nar/27.23.4636PubMed CentralView ArticlePubMedGoogle Scholar
- 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
- Klimke W, Agarwala R, Badretdin A, Chetvernin S, Ciufo S, Fedorov B, Kiryutin B, O’Neill K, Resch W, Resenchuk S, et al. The National Center for Biotechnology Information’s Protein Clusters Database. Nucleic Acids Res 2009; 37(Database issue):D216–D223. PubMed http://dx.doi.org/10.1093/nar/gkn734PubMed CentralView ArticlePubMedGoogle Scholar
- Marchler-Bauer A, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, et al. CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res 2009; 37(Database issue):D205–D210. PubMed http://dx.doi.org/10.1093/nar/gkn845PubMed CentralView ArticlePubMedGoogle Scholar
- Lowe TM, Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997; 25:955–964. PubMedPubMed CentralView ArticlePubMedGoogle Scholar
- Eddy SR. A memory-efficient dynamic programming algorithm for optimal alignment of a sequence to an RNA secondary structure. BMC Bioinformatics 2002; 3:18. PubMed http://dx.doi.org/10.1186/1471-2105-3-18PubMed CentralView ArticlePubMedGoogle Scholar
- Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T, Ussery DW. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 2007; 35:3100–3108. PubMed http://dx.doi.org/10.1093/nar/gkm160PubMed CentralView ArticlePubMedGoogle Scholar
- Griffiths-Jones S, Moxon S, Marshall M, Khanna A, Eddy SR, Bateman A. Rfam: annotating non-coding RNAs in complete genomes. Nucleic Acids Res. 2005;33 Database Issue:D121–124.PubMed CentralView ArticlePubMedGoogle Scholar
- Krogh A, Larsson B, von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 2001; 305:567–580. PubMed http://dx.doi.org/10.1006/jmbi.2000.4315View ArticlePubMedGoogle Scholar
- Bendtsen JD, Nielsen H, von Heijne G, Brunak S. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 2004; 340:783–795. PubMed http://dx.doi.org/10.1016/j.jmb.2004.05.028View ArticlePubMedGoogle Scholar