Genome sequence of the Leisingera aquimarina type strain (DSM 24565T), a member of the marine Roseobacter clade rich in extrachromosomal elements
- Thomas Riedel1,
- Hazuki Teshima2,
- Jörn Petersen3,
- Anne Fiebig3,
- Karen Davenport2,
- Hajnalka Daligault2,
- Tracy Erkkila2,
- Wei Gu2,
- Christine Munk2,
- Yan Xu2,
- Amy Chen4,
- Amrita Pati5,
- Natalia Ivanova5,
- Lynne A. Goodwin2, 5,
- Patrick Chain2,
- John C. Detter2, 5,
- Manfred Rohde1,
- Sabine Gronow3,
- Nikos C. Kyrpides5,
- Tanja Woyke5,
- Markus Göker3Email author,
- Thorsten Brinkhoff6 and
- Hans-Peter Klenk3
© The Author(s) 2013
Published: 30 July 2013
Leisingera aquimarina Vandecandelaere et al. 2008 is a member of the genomically well characterized Roseobacter clade within the family Rhodobacteraceae. Representatives of the marine Roseobacter clade are metabolically versatile and involved in carbon fixation and biogeochemical processes. They form a physiologically heterogeneous group, found predominantly in coastal or polar waters, especially in symbiosis with algae, in microbial mats, in sediments or associated with invertebrates. Here we describe the features of L. aquimarina DSM 24565T together with the permanent-draft genome sequence and annotation. The 5,344,253 bp long genome consists of one chromosome and an unusually high number of seven extrachromosomal elements and contains 5,129 protein-coding and 89 RNA genes. It was sequenced as part of the DOE Joint Genome Institute Community Sequencing Program 2010 and of the activities of the Transregional Collaborative Research Centre 51 funded by the German Research Foundation (DFG).
Keywordsmarine biofilm ovoid-shaped halotolerant heterotrophic quorum sensing plasmid thiosulfate oxidation carbon monoxide utilization Rhodobacteraceae Alphaproteobacteria
Strain R-26159T (= DSM 24565T = LMG 24366T = CCUG 55860T) is the type strain of the species Leisingera aquimarina , one of the three species currently with a validly published name in the genus Leisingera; the other ones are the type species L. methylohalidivorans [1,2] and L. nanhaiensis . The genus Leisingera is a member of the widespread Roseobacter clade, present in various marine habitats . Strain R-26159T was isolated from a marine electroactive biofilm grown on a stainless-steel cathode, which was exposed to natural seawater at the ISMAR-CNR Marine Station within the harbor of Genova (Italy) . The genus Leisingera was named after Thomas Leisinger for his work on the bacterial methyl halide metabolism ; the species epithet aquimarina refers to the Neolatin adjective marinus, from the sea, from seawater. PubMed records do not currently indicate any follow-up research with strain R-26159T after the initial description of L. aquimarina .
Here we present a summary classification and a set of features for L. aquimarina DSM 24565T, together with the description of the genomic sequencing and annotation.
Classification and features of the organism 16S rRNA analysis
A representative genomic 16S rRNA gene sequence of L. aquimarina DSM 24565T was compared using NCBI BLAST [5,6] 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 Phaeobacter (31.4%), Ruegeria (25.9%), Silicibacter (16.1%), Roseobacter (14.4%) and Nautella (3.9%) (127 hits in total). Regarding the four hits to sequences from other members of the genus, the average identity within HSPs was 99.4%, whereas the average coverage by HSPs was 99.3%. Among all other species, the one yielding the highest score was Leisingera methylohalidivorans (NR_025637), which corresponded to an identity of 99.2% and an HSP coverage of 100.0%. (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 FJ202534 (Greengenes short name ‘and White Plague Disease-Induced Changes Caribbean Coral Montastraea faveolata kept aquarium 23 days clone SGUS1024’), which showed an identity of 97.8% and an HSP coverage of 100.0%. The most frequently occurring keywords within the labels of all environmental samples which yielded hits were ‘coral’ (4.7%), ‘caribbean’ (3.8%), ‘faveolata’ (3.5%), ‘chang’ (3.4%) and ‘white’ (3.3%) (117 hits in total). Environmental samples which yielded hits of a higher score than the highest scoring species were not found, which might indicate that the species is rarely found in the environment.
Morphology and physiology
The utilization of carbon compounds by L. aquimarina DSM 24565T grown at 20°C was 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 [31,32], using its functionality for statistically estimating parameters from the respiration curves and translating them 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 were regarded as ambiguous. At 28°C the strain reacted poorly, with positive reactions only for 1% NaCl, 4% NaCl and lithium chloride. This is in accordance with the comparatively low median of the temperature range of the strain .
Classification and general features of L. aquimarina DSM 24565T according to the MIGS recommendations .
Species Leisingera aquimarina
Subspecific genetic lineage (strain)
Reference for biomaterial
Vandecandelaere et al. 2008
Halophile, 1–7% NaCl (w/v)
Relationship to oxygen
Yeast extract, peptone, betaine
Marine biofilm on stainless steel cathode
ISMAR-CNR Marine Station, Genoa harbor, Italy
Genome sequencing and annotation
Genome project history
Genome sequencing project information
Improved high quality draft
Two genomic libraries: Illumina standard (short PE), Illumina CLIP (long PE)
Illumina HiSeq 2000, PacBio
699 × Illumina; unknown × PacBio
Allpath version 39750, Velvet 1.1.05, phrap version SPS - 4.24
Gene calling method
Prodigal 1.4, GenePRIMP
GenBank Date of Release
NCBI project ID
Source material identifier
Tree of Life, carbon cycle, sulfur cycle, environmental
Growth conditions and DNA isolation
A culture of L. aquimarina DSM 24565T was grown in the DSMZ medium 514 (BACTO Marine Broth)  at 20°C. Genomic DNA was isolated from 0.5–1 g of cell paste using Jetflex Genomic DNA Purification Kit (GENOMED 600100) following the standard protocol provided by the manufacturer but modified by the use of additional 20 µl proteinase K and 40 minute incubation. DNA is available through the DNA Bank Network .
Genome sequencing and assembly
The draft genome was generated using Illumina data . For this genome, we constructed and sequenced an Illumina short-insert paired-end library with an average insert size of 270 bp which generated 13,668,574 reads and an Illumina long-insert paired-end library with an average insert size of 8047.58 +/− 2682.23 bp which generated 11,512,166 reads totaling 3,777 Mbp of Illumina data (Feng Chen, unpublished). All general aspects of library construction and sequencing can be found at the JGI web site . The initial draft assembly contained 64 contigs in 18 scaffold(s). The initial draft data was assembled with Allpaths  and the consensus was computationally shredded into 10 kbp overlapping fake reads (shreds). The Illumina draft data was also assembled with Velvet , and the consensus sequences were computationally shredded into 1.5 kbp overlapping fake reads (shreds). The Illumina draft data was assembled again with Velvet using the shreds from the first Velvet assembly to guide the next assembly. The consensus from the second Velvet assembly was shredded into 1.5 kbp overlapping fake reads. The fake reads from the Allpaths assembly and both Velvet assemblies and a subset of the Illumina CLIP paired-end reads were assembled using parallel phrap (High Performance Software, LLC) . Possible mis-assemblies were corrected with manual editing in Consed [37,39,40]. Gap closure was accomplished using repeat resolution software (Wei Gu, unpublished), and sequencing of bridging PCR fragments with PacBio (Cliff Han, unpublished) technologies. A total of 57 PCR PacBio consensus sequences were completed to close gaps and to raise the quality of the final sequence. The final assembly is based on 3,777 Mbp of Illumina draft data, which provides an average 699 × coverage of the genome.
Genes were identified using Prodigal  as part of the JGI 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) nonredundant database, UniProt, TIGR-Fam, Pfam, PRIAM, KEGG, COG, and InterPro databases. Additional gene prediction analysis and functional annotation was 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 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
General genomic features of the chromosome and extrachromosomal replicons from Leisingera aquimarina strain DSM 24565T.
Integrated Microbial Genome (IMG) locus tags of L. aquimarina DSM 24565T genes for the initiation of replication, toxin/antitoxin modules and two representatives of type IV secretion systems (T4SS) that are required for conjugation. The locus tags are accentuated in blue1,2,3.
Type IV Secretion
The locus tags of all replicases, plasmid stability modules and the large virB4 and virD4 genes of type IV secretion systems are presented in Table 6. A characteristic T4SS comprising the relaxase VirD2 and the coupling protein VirD4 as well as the complete virB gene cluster for the transmembrane channel is located on the chromosome . Its functional role is unclear, but very closely related T4SS are detected on plasmids of e.g. Dinoroseobacter shibae DSM 16493T , Leisingera nanhaiensis DSM 24252T and Phaeobacter caeruleus DSM 24564T . Furthermore, the largest plasmid pAqui_A249 contains the complete F factor conjugation transfer (tra) region with 20 genes (Aqui_4678 to Aqui_4697). It exhibits only weak homology with the typical type IV secretion system of the Roseobacter clade, which is represented by the chromosomal counterpart, but it resembles the F sex factor of Escherichia coli that is the paradigm for bacterial conjugation .
The 243 kb RepABC-13 type plasmid pAqui_B243 is predominated by seven ABC-transporters. Even more conspicuous is the presence of a couple of pentose phosphate pathway genes including an operon of genes of the Entner-Doudoroff pathway (Aqui_4914 to Aqui_4917; EC 188.8.131.52; EC 184.108.40.206; EC 220.127.116.11; EC 18.104.22.168) that is generally used in Roseobacters to convert D-fructose-6-phosphate to D-glyceraldehyde-3-phosphate . The exclusive missing gene within this operon is the chromosome encoded 6-phosphogluconolactonase (Aqui_2983; EC 22.214.171.124). The presence of a glycolytic 6-phosphofructokinase (PFK; Aqui_4950; EC 126.96.36.199) is a genetic novelty in this group of marine bacteria, because the current opinion was that “the typical pfk gene is absent from all sequenced Roseobacter clade genomes and glucose is hence probably catabolized via the Entner-Doudoroff pathway and not via classical glycolysis” . However, the putative functionality of the Embden-Meyerhoff-Parnas pathway (glycolysis) has to be validated e.g. via pulse-chase experiments with 13C labeled glucose . Finally, the plasmid pAqui_B243 contains the phosphoenolpyruvate synthase (Aqui_4951; EC 188.8.131.52) that is required together with the chromosomal phosphoenolpyruvate carboxylase (Aqui_0364; EC 184.108.40.206) for prokaryotic CO2 fixation and the formation of oxaloacetate from pyruvate.
The 148 kb RepB-I type plasmid pAqui_D148 contains a complete rhamnose operon  and many genes that are required for polysaccharide biosynthesis. This extrachromosomal replicon also harbors two siderophore synthetase genes (Aqui_4320; Aqui_4321), two outer membrane receptors for Fe-transport (Aqui_4319; Aqui_4360) and genes of a putative ABC-type Fe3+ siderophore transport system (Aqui_4361 to Aqui_4364).
The 140 kb RepA-I type plasmid pAqui_E140 is largely predominated by glycosyltransferases, polysaccharide biosynthesis as well as cell-wall biogenesis genes, and it contains an operon for GDP-mannose metabolism (Aqui_5058 to Aqui_5055).
The 126 kb DnaA-like I replicon pAqui_F126 contains a large type VI secretion system (T6SS) with a size of about 30 kb. The role of this export system that has been first described in the context of bacterial pathogenesis, but recent findings indicate a more general physiological role in defense against eukaryotic cells and other bacteria in the environment . Homologous T6S systems are present on the DnaA-like I plasmids of Leisingera methylohalidivorans DSM 14336T (pMeth_A285) and Phaeobacter caeruleus DSM 24564T (pCaer_C109) as well as the RepC-8 type plasmid of Phaeobacter daeponensis DSM23529T (pDaep_A276).
Genome analysis of strain L. aquimarina DSM 24565T revealed further the presence of genes encoding LuxI as well as LuxR homologues, which are involved in quorum sensing (QS), an already known feature of several members of the Roseobacter clade . QS is a bacterial communication system used by many bacterial species to coordinate special behaviors based on bacterial population density . Whereas two genes encode a N-acyl-L-homoserine lactone synthase (LuxI, Aqui_0074, Aqui_4264), some genes were identified to encode LuxR homologues (response and transcriptional regulators, e.g., Aqui_0075 and Aqui_3114).
Furthermore, several genes forming a putative operon are involved in the oxidation of (e.g., Aqui_3422 to Aqui_3426) indicating the oxidation of thiosulfate into sulfate to produce energy. Additionally genes for carbon monoxide utilization (Aqui_2391 and Aqui_2392, Aqui_2518, Aqui_2520, Aqui_3522, Aqui_5216 and Aqui_5217) were observed.
Interestingly, also a gene encoding a sensor of blue light using FAD (BLUF, Aqui_2375) was detected, indicating possible blue-light depending signal transduction.
DDH similarities between L. aquimarina DSM 24565T and the other Leisingera and Phaeobacter species (with genome-sequenced type strains) †
L. nanhaiensis (2512047090)
L. methylohalidivorans (2512564009)
P. arcticus (2516653081)
P. caeruleus (2512047087)
P. daeponensis (2516493020)
P. gallaeciensis (AOQA01000000)
P. inhibens (2516653078)
The authors would like to gratefully acknowledge the assistance of Iliana Schröder for growing L. aquamarina cultures and Evelyne-Marie Brambilla for DNA extraction and quality control (both at the DSMZ). The work conducted by the U.S. Department of Energy Joint Genome Institute was supported by the Office of Science of the U.S. Department of Energy under contract No. DE-AC02-05CH11231; the work conducted by the members of the Roseobacter consortium was supported by the German Research Foundation (DFG) Transregio-SFB 51. We also thank the European Commission which supported phenotyping via the Microme project 222886 within the Framework 7 program.
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