Genome sequence of the Litoreibacter arenae type strain (DSM 19593T), a member of the Roseobacter clade isolated from sea sand
© The Author(s) 2013
Published: 16 October 2013
Litoreibacter arenae Kim et al. 2012 is a member of the genomically well-characterized Rhodobacteraceae clade within the Roseobacter clade. Representatives of this clade are known to be metabolically versatile and involved in marine carbon-producing and biogeochemical processes. They form a physiologically heterogeneous group of Alphaproteobacteria and were mostly found in coastal or polar waters, especially in symbiosis with algae, in microbial mats, in sediments or together with invertebrates and vertebrates. Here we describe the features of L. arenae DSM 19593T, including novel aspects of its phenotype, together with the draft genome sequence and annotation. The 3,690,113 bp long genome consists of 17 scaffolds with 3,601 protein-coding and 56 RNA genes. This genome was sequenced as part of the activities of the Transregional Collaborative Research Centre 51 funded by the German Research Foundation (DFG).
Keywordsmarine rod-shaped sea sand sediment motile strictly aerobic mesophile chemoorganotrophic halophilic virus-like structures carbon monoxide utilization sulfur oxidation Rhodobacteraceae Alphaproteobacteria Thalassobacter arenae
Strain GA2-M15T (= DSM 19593 = KACC 12675) is the type strain of the species Litoreibacter arenae [1,2]. The genus Litoreibacter is a member of the highly abundant marine Roseobacter lineage, which plays an important role in the global carbon and sulfur cycles and thus for the climate on Earth. Phylogenetically, this alphaproteobacterial genus is related to the genera Jannaschia, Octadecabacter and Thalassobius . Strain GA2-M15T was isolated from a sea-sand sample from the coast of Homi Cape, Pohang City, South Korea as Thalassobacter arenae , which was later on reclassified into Litoreibacter arenae . The name for the genus Litoreibacter was constructed from litoreus (‘belonging to the seashore’) and bacter (‘a rod’) . The species epithet arenae refers to the Neolatin adjective arenae, ‘of sand’. Current PubMed records do not indicate any follow-up research with strain GA2-M15T after the initial description of T. arenae  and its reclassification into L. arenae . Here we present a summary classification and a set of features for L. arenae DSM 19593T, including novel aspects of its phenotype, together with the description of the genomic sequencing and annotation.
Classification and features of the organism
16S rRNA gene analysis
A representative genomic 16S rRNA gene sequence of L. arenae DSM 19593T was compared using NCBI BLAST [4,5] 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 genera were Jannaschia (38.1%), Thalassobacter (15.4%), Octadecabacter (11.7%), Roseovarius (10.7%) and Roseobacter (10.2%) (28 hits in total). Regarding the three hits to sequences from other members of the genus, the average identity within HSPs was 96.0%, whereas the average coverage by HSPs was 98.7%. Among all other species, the one yielding the highest score was ‘Octadecabacter orientus’ (DQ167247), which corresponded to an identity of 99.2% and an HSP coverage of 99.6%. (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 FJ664800 (Greengenes short name ‘Quantitative dynamics cells plankton-fed microbial fuel cell clone plankton D11’), which showed an identity of 97.0% and an HSP coverage of 99.6%. The most frequently occurring keywords within the labels of all environmental samples which yielded hits were ‘lake’ (9.9%), ‘tin’ (9.8%), ‘xiaochaidan’ (9.4%), ‘microbi’ (2.6%) and ‘sea’ (2.5%) (222 hits in total). Environmental samples which yielded hits of a higher score than the highest scoring species were not found.
Morphology and physiology
Cells hydrolyze aesculin and tyrosine weakly, but do not show any hydrolysis of alginic acid, casein, chitin, CM-cellulose, DNA, gelatin, pectin, starch or urea . They assimilate citrate, D-fructose, D-galactose, D-glucose, L-glutamate, glycerol, β-hydroxybutyrate, D-mannitol, D-mannose, melibiose, propionate, pyruvate, L-serine, L-tyrosine and D-xylose, but not L-alanine, L-arabinose, L-aspartate, cellobiose, glycine, L-histidine, lactose, L-leucine, maltose, L-rhamnose, D-ribose, sucrose, L-threonine or trehalose. Cells are positive for β-galactosidase, esterase (C4), esterase lipase (C8), leucine arylamidase, naphthol-AS-BI-phosphohydrolase, α-glucosidase and β-glucosidase, but negative for indole production, arginine dihydrolase, alkaline phosphatase, lipase (C14), valine arylamidase, cystine arylamidase, trypsin, α-chymotrypsin, acid phosphatase, α-galactosidase, β-glucuronidase, N-acetyl-β-glucosaminidase, α-mannosidase and α-fucosidase .
The substrate utilization and resistance patterns of L. arenae DSM 19593T were also determined for this study using Generation-III microplates in an OmniLog phenotyping device (BIOLOG Inc., Hayward, CA, USA). The microplates were inoculated at 28°C 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 exported measurement data were further analyzed with the opm package for R [26,27], using its functionality for statistically estimating parameters from the respiration curves such as the maximum height, and automatically translating these values into negative, ambiguous, and positive reactions. The strain was studied in two independent biological replicates, and reactions with a different behavior between the two repetitions, if any, were regarded as ambiguous.
L. arenae DSM 19593T showed positive reactions for 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, glucuronamide, quinic acid, L-lactic acid, citric acid, α-keto-glutaric acid, D-malic acid, L-malic acid, nalidixic acid, lithium chloride, acetic acid and sodium formate.
No reaction was found for dextrin, D-maltose, D-trehalose, D-cellobiose, β-gentiobiose, sucrose, D-turanose, 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, mucic acid, D-saccharic acid, vancomycin, tetrazolium violet, tetrazolium blue, p-hydroxy-phenylacetic acid, methyl pyruvate, D-lactic acid methyl ester, bromo-succinic acid, potassium tellurite, tween 40, γ-amino-n-butyric acid, α-hydroxy-butyric acid, β-hydroxy-butyric acid, α-keto-butyric acid, acetoacetic acid, propionic acid, aztreonam, butyric acid and sodium bromate.
The measured utilization of carbon sources differs in some aspects from the one recorded in . L-histidine and L-rhamnose were reported in  not to support bacterial growth, whereas in the Omnilog measurements both substrates yielded a positive reaction. This may be due to the higher sensitivity of respiratory measurements . The utilization of propionate, D-fructose, D-glucose, D-mannose, D-mannitol, melibiose and glycerol reported by  could not be confirmed by the Omnilog measurements. Changes in the substrate-utilization pattern may arise from distinct cultivation conditions such as growth medium and temperature.
The principal cellular fatty acids of strain GA2-M15T are C18:1 ω7c (74.3%), C16:0 (10.4%), C18:1 ω7c 11-methyl (5.9%), C10:0 3-OH (3.7%) as well as an unknown fatty acid 11.799 (3.0%) . In comparison to Thalassobacter stenotrophicus DSM 16310T [29,30], strain GA2-M15T reflected a higher content of C16:0 (1.1% vs 10.4%) . The predominant polar lipids are diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine and phosphatidyl-choline .
Genome sequencing and annotation
Genome project history
Species Litoreibacter arenae
Subspecific genetic lineage (strain)
Reference for biomaterial
Kim et al. 2009
halophilic, 0.85–8% NaCl (w/v)
Relationship to oxygen
yeast extract, peptone
sea sand, sediment, seawater
Coast of Homi Cape, Pohang City, South Korea
Genome sequencing project information
One Illumina PE library (520 bp insert size)
Illumina GA IIx, Illumina MiSeq
195 × Illumina
velvet version 1.1.36, consed version 20.0
Gene calling method
NCBI project ID
Genbank Date of Release
March 13, 2013
IMG Taxon OID
Source material identifier
Tree of Life, biodiversity
Growth conditions and DNA isolation
A culture of DSM 19593T was grown aerobically in DSMZ medium 514  at 28°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, 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 one Illumina PE library (Table 2). Illumina sequencing  was performed on a GA IIx platform with 150 cycles. The paired-end library contained 520 bp insert size. To correct sequencing errors and improve quality of the reads, clipping was performed using fastq-mcf  and quake . After this step 4,717,610 reads with a median length of 124 bp were assembled using velvet . The resulting draft genome consisted of 71 contigs organized in 45 scaffolds. The initial draft sequences were separated into artificial Sanger reads of 1,000 nt size plus 75 nt overlap. The number of gaps was reduced by manual editing in phred/phrap/consed version 20.0 . The final assembly was composed of 17 contigs organized in 15 scaffolds. (The version deposited at Genbank contains two scaffolds less, which did not meet the requirements for the minimal contig length.) The additional fragments ‘thalar_Contig12.1’ and ‘thalar_Contig18_1.4’ can be found in the IMG database). The combined sequences provided a 195× 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) nonredundant 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 genome comprises a single extrachromosomal element (with not yet validated circularity), ‘thalar_Contig204.17’, 139.9 kbp in size containing 130 protein-coding genes including a large RTX-toxin gene and a F0F1-type ATPase operon. It contains the typical replication modules. Its replication system is of the ABC-9 type with the compatibility group RepC-9 . This type of repABC operon was found in two representatives of the genera Octadecabacter and Roseobacter, respectively, as well as in Dinoroseobacter shibae . The presence of the replication-initiation gene DnaA (Thalar_03034) reveals the chromosomal origin of largest, 1.091 Mbp long scaffold ‘thalar_Contig148.14’, but it harbors neither a plasmid stability module nor a type IV secretion system.
Genome analysis of strain DSM 19593T revealed the presence of genes encoding proteins associated to carbon monoxide utilization (thalar_00241, thalar_00242, thalar_02265, thalar_03324, thalar_03325, thalar_03395, thalar_03397) as well as genes forming a putative operon, which are involved in the oxidation of sulfur (thalar_01786 to_01792) indicating the oxidation of sulfur to produce energy. Additional gene sequences of interest encode a homogentisate 1,2-dioxygenase (thalar_03573), several haloacid dehalogenase superfamily proteins (thalar_00489, thalar_00580, thalar_01120, thalar_01943, thalar_02401) and a 2-haloalkanoic acid dehalogenase type II (thalar_00287). The presence of such genes could indicate a respiratory degradation of recalcitrant compounds by strain DSM 19593T in its ecological niche.
Further genes encoding a N-acyl-L-homoserine lactone synthetase (thalar_00160) and a response regulator (thalar_00161) associated to quorum sensing were observed [50–53]. Genome analysis of strain DSM 19593T also revealed the presence of genes encoding a bacteriophage associated genes (e.g., thalar_00003 to 00007). A gene encoding a sensor of blue light using FAD (BLUF, thalar_02670) was also detected, indicating possible blue-light dependent signal transduction.
The authors gratefully acknowledge the assistance of Iljana Schröder for technical assistance and Evelyne-Marie Brambilla for DNA extraction and quality control (both at the DSMZ). This study was supported by the German Research Foundation (DFG) Transregio-SFB 51.
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