Genome sequence of the Litoreibacter arenae type strain (DSM 19593T), a member of the Roseobacter clade isolated from sea sand
Standards in Genomic Sciences volume 9, pages 117–127 (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).
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.
Figure 1 shows the phylogenetic neighborhood of L. arenae in a 16S rRNA sequence based tree. The sequence of the single 16S rRNA gene in the genome does not differ from the previously published 16S rDNA sequence (EU342372).
Morphology and physiology
Cells of strain GA2-M15T are Gram-negative short rods (0.7-1.2 µm in width and 1.2–2.4 µm in length) and contain a polar flagellum for motility , [Figure 2]. Polyhydroxybutyrate is accumulated in the cells. Colonies are deep-brown, circular and contain clear margins. Cells are catalase and oxidase positive . Growth occurs at 5–35 °C with an optimum at 30 °C. Cells were successfully grown on marine agar (MA), nutrient agar (NA, weak growth), salt tolerance agar (STA, containing 1% (w/v) tryptone, 0.3% (w/v) yeast extract and 1.5% (w/v) agar supplemented with salts) as well as on basal medium agar (BMA, recipe after ). No growth was observed on Reasoner’s 2A agar (R2A), trypticase soy agar (TSA) or MacConkey agar. The salinity range for growth is 0.85–8% NaCl (w/v), but the strain does not grow below 0.34% or at above 10% NaCl (w/v). The pH range for growth is pH 6–9 with an optimum at pH 7 .
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
The strain was first chosen for genome sequencing in the Genomic Encyclopedia of Bacteria and Archaea (GEBA) phase I project according the GEBA criteria [31,32], but then sequenced as part of the “Ecology, Physiology and Molecular Biology of the Roseobacter clade project: Towards a Systems Biology Understanding of a Globally Important Clade of Marine Bacteria” funded by the German Research Council (DFG). Project information is stored in the Genomes OnLine Database . The Whole Genome Shotgun (WGS) sequence is deposited in Genbank and the Integrated Microbial Genomes database (IMG) . A summary of the project information is shown in Table 2.
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 .
The genome statistics are provided in Table 3 and Figure 3. The genome consists of a 3.56 Mbp chromosome and a G+C content of 60% and a 140 kbp plasmid with a G+C content of 59%. Of the 3,657 genes predicted, 3,601 were protein-coding genes, and 56 RNAs. The majority of the protein-coding genes (81.8%) were assigned a putative function while the remaining ones were annotated as hypothetical proteins. The distribution of genes into COGs functional categories is presented in Table 4.
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.
Kim BY, Weon HY, Son JY, Lee CM, Hong SB, Jeon YA, Koo BS, Kwon SW. Thalassobacter arenae sp. nov., isolated from sea sand in Korea. Int J Syst Evol Microbiol 2009; 59:487–490. PubMed http://dx.doi.org/10.1099/ijs.0.65841-0
Kim YO, Park S, Nam BH, Kang SJ, Hur YB, Kim DG, Oh TK, Yoon JH. Description of Litoreibacter meonggei sp. nov., isolated from the sea squirt Halocynthia roretzi, reclassification of Thalassobacter arenae as Litoreibacter arenae comb. nov. and emended description of the genus Litoreibacter Romanenko et al. 2011. Int J Syst Evol Microbiol 2012; 62:1825–1831. PubMed http://dx.doi.org/10.1099/ijs.0.035113-0
Romanenko LA, Tanaka N, Frolova GM, Svetashev VI, Mikailov VV. Litoreibacter albidus gen. nov., sp. nov. and Litoreibacter janthinus sp. nov., members of the Alphaproteobacteria isolated from the seashore. Int J Syst Evol Microbiol 2011; 61:148–154. PubMed http://dx.doi.org/10.1099/ijs.0.019513-0
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410. PubMed
Korf I, Yandell M, Bedell J. BLAST, O’Reilly, Sebastopol, 2003.
DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL. Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB. Appl Environ Microbiol 2006; 72:5069–5072. PubMed http://dx.doi.org/10.1128/AEM.03006-05
Porter MF. An algorithm for suffix stripping. Program: electronic library and information systems 1980; 14:130–137.
Lee C, Grasso C, Sharlow MF. Multiple sequence alignment using partial order graphs. Bioinformatics 2002; 18:452–464. PubMed http://dx.doi.org/10.1093/bioinformatics/18.3.452
Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000; 17:540–552. PubMed http://dx.doi.org/10.1093/oxfordjournals.molbev.a026334
Stamatakis A, Hoover P, Rougemont J. A rapid bootstrap algorithm for the RAxML web-servers. Syst Biol 2008; 57:758–771. PubMed http://dx.doi.org/10.1080/10635150802429642
Hess PN, De Moraes Russo CA. An empirical test of the midpoint rooting method. Biol J Linn Soc Lond 2007; 92:669–674. http://dx.doi.org/10.1111/j.1095-8312.2007.00864.x
Pattengale ND, Alipour M, Bininda-Emonds ORP, Moret BME, Stamatakis A. How Many Bootstrap Replicates Are Necessary? Lect Notes Comput Sci 2009; 5541:184–200. http://dx.doi.org/10.1007/978-3-642-02008-7_13
Swofford DL. PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4.0 b10. Sinauer Associates, Sunderland, 2002.
Pagani I, Liolios K, Jansson J, Chen IM, Smirnova T, Nosrat B, Markowitz VM, Kyrpides NC. The GenomesOnLine Database (GOLD) v.4: status of genomic and metagenomic projects and their associated metadata. Nucleic Acids Res 2012; 40:D571–D579. PubMed http://dx.doi.org/10.1093/nar/gkr1100
Wagner-Döbler I, Ballhausen B, Berger M, Brinkhoff T, Buchholz I, Bunk B, Cypionka H, Daniel R, Drepper T, Gerdts G, et al. The complete genome sequence of the algal symbiont Dinoroseobacter shibae — a hitchhiker’s guide to life in the sea. ISME J 2010; 4:61–77. PubMed http://dx.doi.org/10.1038/ismej.2009.94
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/nbt1360
Field D, Amaral-Zettler L, Cochrane G, Cole JR, Dawyndt P, Garrity GM, Gilbert J, Glöckner FO, Hirschman L, Karsch-Mzrachi I, et al. PLoS Biol 2011; 9:e1001088. PubMed http://dx.doi.org/10.1371/journal.pbio.1001088
Woese CR, Kandler O, Weelis ML. Towards a natural system of organisms. Proposal for the domains Archaea and Bacteria. Proc Natl Acad Sci USA 1990; 87:4576–4579. PubMed http://dx.doi.org/10.1073/pnas.87.12.4576
Garrity GM, Bell JA, Lilburn T. Phylum XIV. Proteobacteria phyl nov. In: Brenner DJ, Krieg NR, Stanley JT, Garrity GM (eds), Bergey’s Manual of Sytematic Bacteriology, second edition. Vol. 2 (The Proteobacteria), part B (The Gammaproteobacteria), Springer, New York, 2005, p. 1.
Garrity GM, Bell JA, Lilburn T. Class I. Alphaproteobacteria class. nov. In: Brenner DJ, Krieg NR, Stanley JT, Garrity GM (eds), Bergey’s Manual of Sytematic Bacteriology, second edition. Vol. 2 (The Proteobacteria), part C (The Alpha-, Beta-, Delta-, and Epsilonproteobacteria), Springer, New York, 2005, p. 1.
Validation List No. 107. List of new names and new combinations previously effectively, but not validly, published. Int J Syst Evol Microbiol 2006; 56:1–6. PubMed http://dx.doi.org/10.1099/ijs.0.64188-0
Garrity GM, Bell JA, Lilburn T. Order III. Rhodobacterales ord. nov. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM (eds), Bergey’s Manual of Systematic Bacteriology, second edition. vol. 2 (The Proteobacteria), part C (The Alpha-, Beta-, Delta-, and Epsilonproteobacteria), Springer, New York, 2005, p. 161.
Garrity GM, Bell JA, Lilburn T. Family I. Rhodobacteraceae fam. nov. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM (eds), Bergey’s Manual of Systematic Bacteriology, second edition. vol. 2 (The Proteobacteria), part C (The Alpha-, Beta-, Delta-, and Epsilonproteobacteria), Springer, New York, 2005, p. 161.
BAuA. Classification of Bacteria and Archaea in risk groups. TRBA 2010; 466:93.
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/10.1038/75556
Vaas LA, Sikorski J, Michael V, Göker M, Klenk HP. Visualization and curve-parameter estimation strategies for efficient exploration of phenotype microarray kinetics. PLoS ONE 2012; 7:e34846. PubMed http://dx.doi.org/10.1371/journal.pone.0034846
Vaas LA, Sikorski J, Hofner B, Fiebig A, Buddruhs N, Klenk HP, Göker M. opm: an R package for analyzing OmniLog® phaenotype microarray date. Bioinformatics 2013; 29:1823–1824. PubMed http://dx.doi.org/10.1093/bioinformatics/btt291
Bochner BR. Global phenotypic characterization of bacteria. FEMS Microbiol Rev 2009; 33:191–205. PubMed http://dx.doi.org/10.1111/j.1574-6976.2008.00149.x
Macián MC, Arahal DR, Garay E, Ludwig W, Schleifer KH, Pujalte MJ. Thalassobacter stenotrophicus gen. nov., sp. nov., a novel marine alphaproteobacterium isolated from Mediterranean sea water. Int J Syst Evol Microbiol 2005; 55:105–110. PubMed http://dx.doi.org/10.1099/ijs.0.63275-0
Pujalte MJ, Macián MC, Arahal DR, Garay E. Thalassobacter stenothrophicus Macian et al 2005 is a later synonym of Jannaschia cystaugens Adachi et al. 2004, with emended description of the genus Thalassobacter. Int J Syst Evol Microbiol 2005; 55:1959–1963. PubMed http://dx.doi.org/10.1099/ijs.0.63617-0
Göker M, Klenk HP. Phylogeny-driven target selection for genome-sequencing (and other) projects. Stand Genomic Sci 2013; 8:360–374. PubMed http://dx.doi.org/10.4056/sigs.3446951
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/nature08656
Pagani I, Liolios K, Jansson J, Chen IM, Smirnova T, Nosrat B, Markowitz VM, Kyrpides NC. The Genomes OnLine Database (GOLD) v.4: status of genomic and metagenomic projects and their associated metadata. Nucleic Acids Res 2012; 40:D571–D579. PubMed http://dx.doi.org/10.1093/nar/gkr1100
Markowitz VM, Ivanova NN, Chen IMA, Chu K, Kyrpides NC. IMG ER: a system for microbial genome annotation expert review and curation. Bioinformatics 2009; 25:2271–2278. PubMed http://dx.doi.org/10.1093/bioinformatics/btp393
List of growth media used at the DSMZ: http://www.dmsz.de/catalogues/cataloque-microorganisms/culture-technology/list-of-media-for-microorganisms.html.
Gemeinholzer B, Dröge G, Zetzsche H, Haszprunar G, Klenk HP, Güntsch A, Berendsohn WG, Wägele JW. The DNA Bank Network: the start from a German initiative. Biopreserv Biobank 2011; 9:51–55. http://dx.doi.org/10.1089/bio.2010.0029
Bennett S. Solexa Ltd. Pharmacogenomics 2004; 5:433–438. PubMed http://dx.doi.org/10.1517/14622418.104.22.1683
Aronesty E. ea-utils: Command-line tools for processing biological sequencing data; 2011 http://code.google.com/p/ea-utils.
Kelley DR, Schatz MC, Salzberg SL. Quake: quality-aware detection and correction of sequencing errors. Genome Biol 2010; 11:R116. PubMed http://dx.doi.org/10.1186/gb-2010-11-11-r116
Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 2008; 18:821–829. PubMed http://dx.doi.org/10.1101/gr.074492.107
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.8.3.195
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/10.1186/1471-2105-11-119
Mavromatis K, Ivanova NN, Chen IM, Szeto E, Markowitz VM, Kyrpides NC. The DOE-JGI Standard operating procedure for the annotations of microbial genomes. Stand Genomic Sci 2009; 1:63–67. PubMed http://dx.doi.org/10.4056/sigs.632
Finn DR, Clements J, Eddy SR. HMMER web server: interactive sequence similarity searching. Nucleic Acids Research 2011, Web Server Issue 39:W29–W37.
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. PubMed
Nawrocki EP, Kolbe DL, Eddy SR. Infernal 1.0: Inference of RNA alignments. Bioinformatics 2009; 25:1335–1337. PubMed http://dx.doi.org/10.1093/bioinformatics/btp157
Bland C, Ramsey TL, Sabree F, Lowe M, Brown K, Kyrpides NC, Hugenholtz P. CRISPR recognition tool (CRT): a tool for automatic detection of clustered regularly interspaced palindromic repeats. BMC Bioinformatics 2007; 8:209. PubMed http://dx.doi.org/10.1186/1471-2105-8-209
Edgar RC. PILER-CR: Fast and accurate identification of CRISPR repeats. BMC Bioinformatics 2007; 8:18. PubMed http://dx.doi.org/10.1186/1471-2105-8-18
Petersen J, Brinkmann H, Pradella S. Diversity and evolution of repABC type plasmids in Rhodobacterales. Environ Microbiol 2009; 11:2627–2638. PubMed http://dx.doi.org/10.1111/j.1462-2920.2009.01987.x
Wagner-Döbler I, Thiel V, Eberl L, Allgaier M, Bodor A, Meyer S, Ebner S, Hennig A, Pukall R, Schulz S. Discovery of complex mixtures of novel long-chain quorum sensing signals in free-living and host-associated marine alphaproteobacteria. ChemBioChem 2005; 6:2195–2206. PubMed http://dx.doi.org/10.1002/cbic.200500189
Bassler BL. How bacteria talk to each other: regulation of gene expression by quorum sensing. Curr Opin Microbiol 1999; 2:582–587. PubMed http://dx.doi.org/10.1016/S1369-5274(99)00025-9
Henke JM, Bassler BL. Bacterial social engagements. Trends Cell Biol 2004; 14:648–656. PubMed http://dx.doi.org/10.1016/j.tcb.2004.09.012
Waters CM, Bassler BL. Quorum Sensing: Cell-to-Cell Communication in Bacteria. Annu Rev Cell Dev Biol 2005; 21:319–346. PubMed http://dx.doi.org/10.1146/annurev.cellbio.21.012704.131001
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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Riedel, T., Fiebig, A., Petersen, J. et al. Genome sequence of the Litoreibacter arenae type strain (DSM 19593T), a member of the Roseobacter clade isolated from sea sand. Stand in Genomic Sci 9, 117–127 (2013). https://doi.org/10.4056/sigs.4258318
- sea sand
- strictly aerobic
- virus-like structures
- carbon monoxide utilization
- sulfur oxidation
- Thalassobacter arenae