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Genome sequence of Shimia str. SK013, a representative of the Roseobacter group isolated from marine sediment

Standards in Genomic Sciences volume 11, Article number: 25 (2016) Cite this article

Abstract

Shimia strain SK013 is an aerobic, Gram-negative, rod shaped alphaproteobacterium affiliated with the Roseobacter group within the family Rhodobacteraceae. The strain was isolated from surface sediment (0–1 cm) of the Skagerrak at 114 m below sea level. The 4,049,808 bp genome of Shimia str. SK013 comprises 3,981 protein-coding genes and 47 RNA genes. It contains one chromosome and no extrachromosomal elements. The genome analysis revealed the presence of genes for a dimethylsulfoniopropionate lyase, demethylase and the trimethylamine methyltransferase (mttB) as well as genes for nitrate, nitrite and dimethyl sulfoxide reduction. This indicates that Shimia str. SK013 is able to switch from aerobic to anaerobic metabolism and thus is capable of aerobic and anaerobic sulfur cycling at the seafloor. Among the ability to convert other sulfur compounds it has the genetic capacity to produce climatically active dimethyl sulfide. Growth on glutamate as a sole carbon source results in formation of cell-connecting filaments, a putative phenotypic adaptation of the surface-associated strain to the environmental conditions at the seafloor. Genome analysis revealed the presence of a flagellum (fla1) and a type IV pilus biogenesis, which is speculated to be a prerequisite for biofilm formation. This is also related to genes responsible for signalling such as N-acyl homoserine lactones, as well as quip-genes responsible for quorum quenching and antibiotic biosynthesis. Pairwise similarities of 16S rRNA genes (98.56 % sequence similarity to the next relative S. haliotis) and the in silico DNA-DNA hybridization (21.20 % sequence similarity to S. haliotis) indicated Shimia str. SK013 to be considered as a new species. The genome analysis of Shimia str. SK013 offered first insights into specific physiological and phenotypic adaptation mechanisms of Roseobacter-affiliated bacteria to the benthic environment.

Introduction

The Roseobacter group is known for its worldwide distribution and its broad metabolic versatility in a great variety of marine habitats [1–3]. About 25 % of all Roseobacter species with validly published names (42 out of 168) have a benthic origin [4]. In marine sediments, they can contribute up to 11 of all 16S rRNA genes and up to 10 % of total cell counts [5, 6], but still little is known about the specific distribution and physiology of roseobacters in this habitat.

Shimia str. SK013, analysed in the present study, was isolated from the top centimeter of Skagerrak sediments at a water depth of 114 m below sea level (mbsl) [7]. The strain is affiliated with the genus Shimia which was first proposed by Choi and Cho in 2006 [8] in honor of Dr. Jae H. Shim, for his contributions to marine plankton ecology in Korea. According to Pujalte et al. [4], the genus Shimia consists of four species, with a fifth species Shimia sagamensis recently included. Members of the genus Shimia were isolated from different marine habitats: e.g. S. haliotis was isolated from the intestinal tract of the abalone Haliotis discus hannai [9], S. biformata from surface sea water [10], S. isoporae from reef building corals [11] and S. marina from a fish farm biofilm [8]. The new species affiliated to the genus Shimia ( Shimia sagamensis ) was isolated from cold seep sediment [12]. The sequenced genome of Shimia str. SK013 will allow for genetic comparison between the strain and other organisms of benthic origin, additional sediment-derived roseobacters and close relatives isolated from different habitats.

Here, we present the genome of Shimia str. SK013 with special emphasis on the genes involved in sulfur cycling such as dimethylsulfoniopropionate (DMSP) degradation and dimethyl sulfoxide reduction, as well as other anaerobic pathways such as nitrate reduction. The second focus is on genes which may be indicative for biofilm formation (pili, flagella and quorum sensing) as an adaptation to their surface-associated lifestyle.

Organism information

Classification and features

Sediment samples were collected in July 2011 during a cruise with the RV ‘Heincke’ (expedition HE361) to the eastern North Sea. The strain was isolated from surface sediment (0–1 cm) of the Skagerrak (Site 27, 57°61.28′N, 8°58.18′E) at 114 mbsl from an aerobic enrichment culture. Shimia str. SK013 is a Gram-negative, motile, rod shaped bacterium with a length of 1.8 to 2.0 μm and a width of approximately 0.5 μm (Table 1; Fig. 1). Colonies are small, slightly domed and white to transparent on artificial sea water medium agar plates, but cream-coloured or beige in marine broth medium agar plates. The strain is mesophilic (range: 10–35 °C, Topt = 30 °C), neutrophilic (optimum pH: 6–7) and halophilic (optimum: 2–3 % w/v). Shimia str. SK013 grows well in liquid medium but relatively slowly on agar-solidified marine broth and artificial sea water medium. The strain is able to utilize various substrates such as glucose, lactose, glutamate, mannose, xylose, acetate and citrate. When Shimia str. SK013 grows in ASW medium with glutamate as sole carbon source, cell-connecting filaments that might represent bundle-forming pili or specialized flagella are induced (Fig. 1). However, these structures were not observed in cultures amended with any other tested substrate (see above). The 16S rRNA gene sequence of Shimia str. SK013 (1453 bp) was analysed using ARB [13] and revealed 98.56 % sequence similarity to the next relative, Shimia haliotis . Furthermore, in the phylogenetic tree, Shimia str. SK013 is branching together with the other Shimia species except Shimia biformata (Fig. 2).

Table 1 Classification and general features of Shimia str. SK013 in accordance with the MIGS recommendations published by the Genome Standards Consortium [46]
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Fig. 1
figure 1

Micrographs of Shimia str. SK013. a Transmission electron micrograph (TEM) showing aggregation of cells and long fibers (b) Scanning electron micrograph (SEM) of cells grown on glutamate with formation of cell-connecting fibers (c) TEM of a single cell with cell-connecting fibers (d) Closer view (TEM) on a bundle of fibers

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Fig. 2
figure 2

The 16S rRNA tree highlighting the position of Shimia str. SK013 relative to the other species within the genus Shimia and other type strains within the Roseobacter group. Maximum likelihood (ML; substitution model = GTR) tree, using 1453 aligned characters, was rooted by Paracoccus denitrificans another member of the Rhodobacteraceae family with ARB [12]. Branches were scaled in terms of the expected number of substitutions per site. Numbers adjacent to branches are support values from 1000 ML bootstrap replicates (left) and from 1000 maximum-parsimony bootstrap replicates (right); values below 50 % were neglected

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Genome sequencing information

Genome project history

Shimia str. SK013 was selected for draft genome sequencing based on its physiological and phenotypical features and its benthic origin. The information related to this project is summarized in Table 2. The draft genome is deposited in the Genomes On Line Database [14] and in the Integrated Microbial Genome database [15]. The Whole Genome Shotgun project has been deposited at DDBJ/EMBL/GenBank under the accession number LAJH00000000.1.

Table 2 Genome sequencing project information
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Growth conditions and genomic DNA preparation

Shimia str. SK013 was enriched and isolated from agar plates containing artificial sea water medium [16] with DMS (100 μM) and lactate (5 mM) as substrates, incubated at 15 °C. The genomic DNA extraction was performed using a DNA isolation kit (MO BIO, Carlsbad, CA, USA), following the manufactures instructions.

Genome sequencing and assembly

Whole-genome sequencing was performed using the Illumina technology. Preparation of paired-end sequencing library with the Illumina Nextera XT library preparation kit and sequencing of the library using the Genome Analyzer IIx were performed as described by the manufacturer (Illumina, San Diego, CA, USA). A total of 11,098,582 paired-end reads were derived from sequencing and trimmed using Trimmomatic version 0.32 [17]. De novo assembly of all trimmed reads with SPAdes version 3.5.0 [18] resulted in 28 contigs and 137.9-fold coverage. A summary of project information is shown in Table 2.

Genome annotation

Protein-coding genes were identified as part of the genome annotation pipeline the Integrated Microbial Genomes Expert Review platform using Prodigal v2.50. The predicted CDS were translated and used to search the CDD, KEGG, UniProt, TIGRFam, Pfam and InterPro databases. These data sources were combined to assert a product description for each predicted protein. Non-coding genes and miscellaneous features were predicted using tRNAscan-SE [19], RNAmmer [20], Rfam [21], TMHMM [22] and SignalP [23]. Additional gene prediction analyses and functional annotation were performed within the IMG-Expert Review platform [24].

Genome properties

The genome analysis showed the presence of 28 scaffolds corresponding to one large chromosome with a total length of 4,049,808 bp and a G + C content of 57.22 % (Table 3). The absence of additional extrachromosomal elements was inferred based on the absence of RepABC, RepA, RepB and DnaA-like modules for plasmid replication and maintenance that are characteristic for Rhodobacteraceae [25]. In total, 4,028 genes were predicted, in which 3,981 were protein-coding genes and 47 RNA genes. About 82.35 % were protein-coding genes with a putative function while those remaining were annotated as hypothetical proteins. The genome statistics are further provided in Table 3 and in Fig. 3. The distribution of genes into functional categories (clusters of orthologous groups) is shown in Table 4.

Table 3 Genome statistics of Shimia str. SK013
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Fig. 3
figure 3

Graphical representation of the genome of Shimia str. SK013. From outside to inside (1–15 color circles): sequence of Shimia str. SK013 (1st circle) is compared to the other species within the genus Shimia and other type strains within the Roseobacter group, (16th circle): G + C content of Shimia str. SK013. Comparisons and visualizations are performed with BRIG [53]

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Table 4 Number of genes associated with general COG functional categories
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Insights from the genome sequence

The genome of Shimia str. SK013 contains genes for sulfur cycling that might enable anaerobic growth. Genes for quorum sensing and quorum quenching might support roseobacters to thrive in complex microbial communities found in sediments. Genome comparison (Table 5; Fig. 3) revealed that Shimia str. SK013 shares the respective genes with a selection of surface-associated roseobacters and the other two Shimia species whose genomes are available. It is well documented that roseobacters are involved in the transformation of DMSP by demethylation or by using the cleavage pathway [6, 26, 27]. Anaerobically, some roseobacters are capable of DMSO reduction resulting in the release of the climatically active DMS [5, 27]. Genes for the DMSP lyase (Shim_05930) and demethylase (Shim_7490) as well as for the DMSO reductase (Shim_34610) found in Shimia str. SK013 indicate their functional role in DMSP degradation and DMSO conversion. All three genes are also present within the genome of S. haliotis and in those of a selection of surface-associated roseobacters (Table 6): S. haliotis (Ga0070219_1011011, 101620, 103192), Octadecabacter arcticus (OA238_c10540, c20430, c35930), Roseobacter litoralis (RLO149_c019880, c022350, c001820) and Leisingera nanhaiensis (Leina_00726, 01164, 02539). Shimia marina is missing the genes for DMSP lyase, but also contains genes for DMSP demethylase (Ga0069993_10296, 102173) and DMSO reductase (Ga0069993_106210). Interestingly, the genome of Shimia str. SK013 simultaneously contained genes for a sulfite reductase (Shim_12650), sulfur dehydgrogenase (SoxC; Shim_11330), sulfur oxidizing proteins (SoxXYZ; Shim_11380, 11370, 11360) and sulfur oxidation (SoxA; Shim_11350). Other than in the Roseobacter group-affiliated fosmid found in German tidal-flat sediments [6], the soxD gene and the rDSR gene are not present.

Table 5 Genome statistics comparison with available genomes of Shimia species
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Table 6 Highlighted genes of Shimia str. SK013 present in other roseobacters
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We observed all genes necessary for the denitrification pathway such as nitrate reductase (Shim_01900), nitrite reductase (Shim_01920), nitric oxide reductase (Shim_02650) and nitrous oxide reductase (Shim_02640). Shimia str. SK013 contains a periplasmic nitrate reductase composed of five subunits [28] such as NapA (Shim_18270), NapB (Shim_18300), NapD (Shim_18260), NapE (Shim_04260) and NapG (Shim_18280). The presence of periplasmic nitrate reductase genes suggest the potential for anaerobic respiration [29] in Shimia str. SK013, whereas the genus Shimia has been described as strictly aerobic until now [8]. Interestingly, anaerobic respiration was also observed in Leisingera nanhaiensis [30] and Phaeobacter inhibens T5T [31], which were originally described as strictly aerobic. The genes involved in nitrogen regulation (Shim_09380) and nitrogen fixation regulation (Shim_29520) were also found in the genome of Shimia str. SK013. Denitrification genes in Shimia str. SK013 showed a strong resemblance to those present in S. haliotis , with the exception the genes coding for nitrite reductase and nitrogen fixation regulation (nitrate reductase and subunits; Ga0070219_10142 to 10145, nitric oxide reductase; Ga0070219_106169; nitrous oxide reductase; Ga0070219_106170, nitrogen regulation; Ga0070219_101812). S. marina showed only the presence of genes for nitrate reduction (Ga0069993_10650), nitrite reduction (Ga0069993_10648), nitrogen regulation (Ga0069993_102260) and nitrogen fixation regulation (Ga0069993_105163). A comparative search revealed the presence of all the genes involved in the nitrogen cycle that were mentioned above for Oceanicola nanhaiensis (SIAM614_16412, 31426, 14520, 22007), Roseobacter litoralis (RLO149_c039850, c031550, c017950, c035140), Phaeobacter arcticus (Phaar_03838, 02837, 01419, 03079, 04163) and Sulfitobacter pontiacus (PM01_06655, 15855, 12625, 02530). Furthermore, the genome of Shimia str. SK013 revealed genes for the utilization of methylated amines, such as a trimethylamine methyltransferase (mttB) (Shim_09600, 31260).

The conspicuous morphological trait of cell-connecting filaments in Shimia str. SK013 (Fig. 1) led to the search for the presence of genes involved in the formation of pili and flagella. The bacterial flagellum is one of the signal transduction systems with complex proteins which enables the bacterial reorientation and motility [32]. So far three different types of flagella gene clusters (FGCs) were described, designated fla1, fla2 and fla3 in Rhodobacteraceae that originated from FGC duplications [33]. Genome analysis revealed the presence of a single compact flagella gene cluster of the fla1-type on the chromosome (contig_000021; Shim_33080 to Shim_33420) that contains all genes necessary for the assembly of a functional flagellum. Recently, Frank et al. [33] showed for the plasmid curing mutant of Marinovum algicola DG898, which is lacking the 143-kb plasmid pMaD5 with a fla2-type FGC, a conspicuous morphological similarity with the filamentous structures observed in the current study for Shimia str. SK013 (Fig. 1). The bundles of filaments were explained by the presence of an additional chromosome-encoded fla1-type flagellum in Marinovum . However, genes for type IV pilus biogenesis, which were found in Shimia str. SK013 (Shim_13020, Shim_37620) are also present in the genome of M. algicola DG898 (MALG_02262) and thus, it is remains unclear if the conspicuous bundles at the cell pole are caused by pilus and/or flagellum formation.

As the described morphological traits are often related to a surface-associated lifestyle, we also searched the genome of Shimia str. SK013 for genes involved in the production of signalling molecules and quorum sensing as indicators for the communication within biofilms. Earlier studies showed that quorum sensing signals are mainly associated with virulence [34, 35], but recent investigations revealed that these signalling molecules play a significant role in basic metabolic processes [36, 37]. The presence of genes for the production of N-acylhomoserine lactones (AHLs) (Shim_31370) and homoserine lactones (Shim_16180) that are part of the quorum sensing system indicate that Shimia str. SK013 uses this form of bacterial communication. In contrast, the newly established genome only contains a few additional genes which interfere with quorum sensing such as quorum quenching or antibiotic biosynthesis related genes (AHL acylase QuiP precursor; Shim_09300) [38–40]. When compared to other selected roseobacters, these three signal molecule genes were also found in Roseobacter litoralis (RLO149_c018030, c029420, c006500) and Sediminimonas qiahouensis (G568DRAFT_00799, 01106, 03483). This finding was proven by an antiSMASH analysis [41] of the Shimia str. SK013 genome, indicating the presence of the type I polyketide synthase (PKS), the homoserine lactone cluster and the bacteriocin gene cluster.

Pairwise similarities of 16S rRNA genes of Shimia str. SK013 and the next relative, Shimia haliotis were 98.56 %. A genome comparison of Shimia str. SK013 with the available draft genomes from the KMG-2 project, Genomic encyclopedia of Bacteria and Archaea (GEBA) [42, 43] of Shimia haliotis DSM 28453 (IMG ID: 2619619046) and Shimia marina DSM 26895 (IMG ID: 2619618961) was conducted using the online analysis tool “Genome-Genome-Distance Calculator” 2.0 (GGDC). The results of the in silico calculated DNA-DNA hybridization (DDH) of Shimia str. SK013 suggests that the given genome might belong to a new species based on the low percentages obtained (Table 7). According to the GGDC tool, formula 2 was recommended for the comparison between the draft genomes as it provides higher DDH correlations than Average Nucleotide Identity (ANI) implementations [44, 45]. The analysis showed that Shimia str. SK013 only shared a genome sequence similarity of 21 % with Shimia haliotis DSM 28453 and 20 % with Shimia marina DSM 26895 and thus represents neither a new isolate of the species S. haliotis nor of S. marina . A direct comparison with the available Shimia genomes revealed further differences such as the IMG pathway counts (representing the number of metabolites and macromolecular complexes) and horizontally transferred gene counts (Table 5). Until now, genome sequences of S. bioformata, S. isoporae and Shimia sagamensis are not available for additional in silico calculated DNA-DNA hybridization or direct genome comparisons. However, as S. haliotis was identified as the closest relative by 16S rRNA gene analysis with a 66/60 % bootstrap support, the DDH data provide strong evidence that Shimia str. SK013 represents a new species within the genus Shimia .

Table 7 Digital DDH similarities between Shimia str. SK013 and other Shimia species, calculated in silico with the GGDC server version 2.0 [45]a
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Conclusions

The genome analysis of Shimia str. SK013 revealed distinctive genes responsible for DMSP utilization, DMSO, nitrate and nitrite reduction which indicate that this strain is a facultative anaerobic bacterium. The presence of genes responsible for signalling can serve as a guide for identification of quorum sensing compounds, as well as antibiotics potentially responsible for quorum quenching. Based on genome comparison and DNA-DNA hybridization with the next relatives, Shimia str. SK013 might represent a new species and should be considered for species description.

Abbreviations

AHLs:

acyl homoserine lactones

ASW:

artificial sea water

BFP:

bundle-forming pili

DMS:

dimethyl sulfide

DMSO:

dimethyl sulfoxide

DMSP:

dimethylsulfoniopropionate

FGC:

flagella gene clusters

GGDC:

Genome-Genome-Distance Calculator

KMG:

1000 microbial genomes

mbsl:

meters below sea level

PKS:

polyketide synthase

SignalP:

signal peptides

TMHMM:

transmembrane helices hidden markov models

References

  1. Wagner-Döbler I, Biebl H. Environmental biology of the marine Roseobacter lineage. Annu Rev Microbiol. 2006;60:255–80.

    Article  PubMed  Google Scholar 

  2. Brinkhoff T, Giebel HA, Simon M. Diversity, ecology, and genomics of the Roseobacter clade: a short overview. Arch Microbiol. 2008;189:531–9.

    Article  CAS  PubMed  Google Scholar 

  3. Luo H, Moran MA. Evolutionary ecology of the marine Roseobacter clade. Microbiol Mol Biol Rev. 2014;78:573–87.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Pujalte MJ LT, Ruvira MA, Arahal DR, Maciàn MC. In: Roseonberg EDLE, Thompson F, Lory S, Stackebrandt E, editors. The Family Rhodobacteraceae. Berlin: Springer; 2014.

    Chapter  Google Scholar 

  5. Gonzàlez JM, Kiene RP, Moran MA. Transformation of sulfur compounds by an abundant lineage of marine bacteria in the alpha-subclass of the class Proteobacteria. Appl Environ Microbiol. 1999;65:3810–9.

    PubMed  PubMed Central  Google Scholar 

  6. Lenk S, Moraru C, Hahnke S, Arnds J, Richter M, Kube M, et al. Roseobacter clade bacteria are abundant in coastal sediments and encode a novel combination of sulfur oxidation genes. ISME J. 2012;6:2178–87.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Kanukollu S, Wemheuer B, Herber J, Billerbeck S, Lucas J, Daniel R, et al. Distinct compositions of free-living, particle-associated and benthic communities of the Roseobacter group in the North Sea. FEMS Microbiol Ecol. 2016;92. doi:10.1093/femsec/fiv145.

  8. Choi DH, Cho BC. Shimia marina gen. nov., sp. nov., a novel bacterium of the Roseobacter clade isolated from biofilm in a coastal fish farm. Int J Syst Evol Microbiol. 2006;56:1869–73.

    Article  CAS  PubMed  Google Scholar 

  9. Hyun DW, Kim MS, Shin NR, Kim JY, Kim PS, Whon TW, et al. Shimia haliotis sp nov., a bacterium isolated from the gut of an abalone, Haliotis discus hannai. Int J Syst Evol Microbiol. 2013;63:4248–53.

    Article  CAS  PubMed  Google Scholar 

  10. Hameed A, Shahina M, Lin SY, Lai WA, Hsu YH, Liu YC, et al. Shimia biformata sp. nov., isolated from surface seawater, and emended description of the genus Shimia Choi and Cho 2006. Int J Syst Evol Microbiol. 2013;63:4533–9.

    Article  CAS  PubMed  Google Scholar 

  11. Chen MH, Sheu SY, Chen CA, Wang JT, Chen WM. Shimia isoporae sp. nov., isolated from the reef-building coral Isopora palifera. Int J Syst Evol Microbiol. 2011;61:823–7.

    Article  CAS  PubMed  Google Scholar 

  12. Nogi Y, Mori K, Uchida H, Hatada Y. Shimia sagamensis sp. nov., a marine bacterium isolated from cold-seep sediment. Int J Syst Evol Microbiol. 2015;65:2786–90.

    Article  CAS  PubMed  Google Scholar 

  13. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar ARB, et al. A software environment for sequence data. Nucleic Acids Res. 2004;32:1363–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Liolios K, Chen IM, Mavromatis K, Tavernarakis N, Hugenholtz P, Markowitz VM, et al. The Genomes On Line Database (GOLD) in 2009: status of genomic and metagenomic projects and their associated metadata. Nucleic Acids Res. 2010;38:D346–54.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Markowitz VM, Mavromatis K, Ivanova NN, Chen IMA, Chu K, Kyrpides NC. IMG ER: a system for microbial genome annotation expert review and curation. Bioinformatics. 2009;25:2271–8.

    Article  CAS  PubMed  Google Scholar 

  16. Süss J, Engelen B, Cypionka H, Sass H. Quantitative analysis of bacterial communities from Mediterranean sapropels based on cultivation-dependent methods. FEMS Microbiol Ecol. 2004;51:109–21.

    Article  PubMed  Google Scholar 

  17. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19:455–77.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Lowe TM, Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 1997;25:955–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. 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;35:3100–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Nawrocki EP, Burge SW, Bateman A, Daub J, Eberhardt RY, Eddy SR, et al. Rfam 12.0: updates to the RNA families database. Nucleic Acids Res. 2015;43:D130–7.

    Article  PubMed  PubMed Central  Google Scholar 

  22. 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;305:567–80.

    Article  CAS  PubMed  Google Scholar 

  23. Bendtsen JD, Nielsen H, von Heijne G, Brunak S. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol. 2004;340:783–95.

    Article  PubMed  Google Scholar 

  24. Markowitz VM, Chen IM, Palaniappan K, Chu K, Szeto E, Pillay M, et al. IMG 4 version of the integrated microbial genomes comparative analysis system. Nucleic Acids Res. 2014;42:D560–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Petersen J. Phylogeny and compatibility: plasmid classification in the genomics era. Arch Microbiol. 2011;193:313–21.

    CAS  PubMed  Google Scholar 

  26. Newton RJ, Griffin LE, Bowles KM, Meile C, Gifford S, Givens CE, et al. Genome characteristics of a generalist marine bacterial lineage. Isme j. 2010;4:784–98.

    Article  CAS  PubMed  Google Scholar 

  27. Moran MA, Gonzalez JM, Kiene RP. Linking a bacterial taxon to sulfur cycling in the sea: Studies of the marine Roseobacter group. Geomicrobiol J. 2003;20:375–88.

    Article  CAS  Google Scholar 

  28. Potter LC, Cole JA. Essential roles for the products of the napABCD genes, but not napFGH, in periplasmic nitrate reduction by Escherichia coli K-12. Biochem J. 1999;344:69–76.

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Stewart V, Lu Y, Darwin AJ. Periplasmic nitrate reductase (NapABC enzyme) supports anaerobic respiration by Escherichia coli K-12. J Bacteriol. 2002;184:1314–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Breider S, Teshima H, Petersen J, Chertkov O, Dalingault H, Chen A, et al. Genome sequence and emended description of Leisingera nanhaiensis strain DSM 24252(T) isolated from marine sediment. Stand Genomic Sci. 2014;9:687–703.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Dogs M, Voget S, Teshima H, Petersen J, Davenport K, Dalingault H, et al. Genome sequence of Phaeobacter inhibens type strain (T5(T)), a secondary metabolite producing representative of the marine Roseobacter clade, and emendation of the species description of Phaeobacter inhibens. Stand Genomic Sci. 2013;9:334–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Poggio S, Abreu-Goodger C, Fabela S, Osorio A, Dreyfus G, Vinuesa P, et al. A complete set of flagellar genes acquired by horizontal transfer coexists with the endogenous flagellar system in Rhodobacter sphaeroides. J Bacteriol. 2007;189:3208–16.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Frank O, Göker M, Pradella S, Petersen J. Ocean’s twelve: Flagellar and biofilm chromids in the multipartite genome of Marinovum algicola DG898 exemplify functional compartmentalization. Environ Microbiol. 2015;17:4019–34.

    Article  CAS  PubMed  Google Scholar 

  34. Ramboarina S, Fernandes PJ, Daniell S, Islam S, Simpson P, Frankel G, et al. Structure of the bundle-forming pilus from enteropathogenic Escherichia coli. J Biol Chem. 2005;280:40252–60.

    Article  CAS  PubMed  Google Scholar 

  35. Craig L, Pique ME, Tainer JA. Type IV pilus structure and bacterial pathogenicity. Nat Rev Micro. 2004;2:363–78.

    Article  CAS  Google Scholar 

  36. Waters CM, Bassler BL. Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol. 2005;21:319–46.

    Article  CAS  PubMed  Google Scholar 

  37. An JH, Goo E, Kim H, Seo YS, Hwang I. Bacterial quorum sensing and metabolic slowing in a cooperative population. Proc Natl Acad Sci U S A. 2014;111:14912–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Park SY, Kang HO, Jang HS, Lee JK, Koo BT, Yum DY. Identification of extracellular N-acylhomoserine lactone acylase from a Streptomyces sp. and its application to quorum quenching. Appl Environ Microbiol. 2005;71:2632–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Lin YH, Xu JL, Hu J, Wang LH, Ong SL, Leadbetter JR, et al. Acyl-homoserine lactone acylase from Ralstonia strain XJ12B represents a novel and potent class of quorum-quenching enzymes. Mol Microbiol. 2003;47:849–60.

    Article  PubMed  Google Scholar 

  40. Huang JJ, Petersen A, Whiteley M, Leadbetter JR. Identification of QuiP, the product of gene PA1032, as the second acyl-homoserine lactone acylase of Pseudomonas aeruginosa PAO1. Appl Environ Microbiol. 2006;72:1190–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Weber T, Blin K, Duddela S, Krug D, Kim HU, Bruccoleri R, et al. antiSMASH 3.0—a comprehensive resource for the genome mining of biosynthetic gene clusters. Nucleic Acids Res. 2015;43:W237–W43.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Kyrpides NC, Woyke T, Eisen JA, Garrity G, Lilburn TG, Beck BJ, et al. Genomic encyclopedia of type strains, phase I: the one thousand microbial genomes (KMG-I) project. Stand Genomic Sci. 2014;9:1278–84.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Kyrpides NC, Hugenholtz P, Eisen JA, Woyke T, Göker M, Parker CT, et al. Genomic encyclopedia of bacteria and archaea: sequencing a myriad of type strains. PLoS Biol. 2014;12:e1001920.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Auch AF, von Jan M, Klenk HP, Göker M. Digital DNA-DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand Genomic Sci. 2010;2:117–34.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. Bmc Bioinformatics. 2013;14. doi:10.1186/1471-2105-14-60.

  46. Field D, Garrity G, Gray T, Morrison N, Selengut J, Sterk P, et al. The minimum information about a genome sequence (MIGS) specification. Nat Biotechnol. 2008;26:541–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Woese CR, Kandler O, Wheelis ML. Towards a natural system of organisms: proposal for the domains archaea, bacteria, and eucarya. Proc Natl Acad Sci U S A. 1990;87:4576–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Garrity GM BJ, Lilburn T, Phylum XIV. In: DJ Brenner NK, Staley JT, Garrity GM, editors. Proteobacteria phyl. nov. second edition, part B (The Gammaproteobacteria). New York: Springer; 2005.

  49. Garrity GMBJ, Lilburn T, Class I. In: Garrity GM BD, Krieg NR, Staley JT, editors. Alphaproteobacteria class. nov. Secondth ed. New York: Springer; 2005.

    Google Scholar 

  50. List of new names and new combinations previously effectively, but not validly, published. Int J Syst Evol Microbiol. 2006;56:1–6.

  51. Garrity GM BJ, Lilburn T, Family I. In: Garrity GM BD, Krieg NR, Staley JT, editors. Rhodobacteraceae fam. nov. Secondth ed. New York: Springer; 2005.

    Google Scholar 

  52. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium Nat Genet. 2000;25:25–9.

    CAS  PubMed  Google Scholar 

  53. Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA. BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics. 2011;12:402.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors acknowledge the crew and the scientific party of the RV Heincke (expedition HE361), especially Judith Lucas for sampling and starting the enrichment cultures as well as Michael Pilzen and Jutta Graue for their assistance during sampling. Furthermore, we thank Jana Feldkamp and Frank Meyerjurgens for technical assistance and our students, Leon Dluglosch, David Nivia, Eva-Lena Nordmann and Katrin Grosser for preliminary physiological experiments and microscopy pictures. We would also extend our thanks to Marco Dogs, Sven Breider and Thorsten Brinkhoff for valuable discussions during genome analysis and Candice Raeburn for proofreading. This work was mainly conducted in the frame of the Roseobacter collaborative research center Transregio-SFB 51, supported by the German Research Foundation (DFG). The work conducted by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231.

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Authors and Affiliations

  1. Institute for Chemistry and Biology of the Marine Environment (ICBM), Oldenburg, Germany

    Saranya Kanukollu, Marion Pohlner, Verona Vandieken, Heribert Cypionka & Bert Engelen

  2. Department of Genomic and Applied Microbiology and Göttingen Genomics Laboratory, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany

    Sonja Voget

  3. Leibniz Institute DSMZ – German Collection of Microorganisms and Cell Cultures, Braunschweig, Germany

    Jörn Petersen & Markus Göker

  4. Department of Energy Joint Genome Institute, Genome Biology Program, Walnut Creek, California, USA

    Nikos C. Kyrpides, Tanja Woyke & Nicole Shapiro

  5. Department of Biological Sciences, Faculty of Science, King Abdulaziz University, Jeddah, Saudi Arabia

    Nikos C. Kyrpides

  6. School of Biology, Newcastle University, Newcastle upon Tyne, UK

    Hans-Peter Klenk

Authors
  1. Saranya Kanukollu
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  2. Sonja Voget
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  12. Bert Engelen
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Corresponding author

Correspondence to Bert Engelen.

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Competing interests

The authors declare that they have no competing interests.

Authors’ contributions

SK, SV wrote the manuscript and analysed the annotated genome and comparative genomes. MP calculated the phylogenetic tree. VV contributed in phenotypic data. JP analysed the annotated genome. MG, NC, TW, NS and HPK provided sequenced, assembled and annotated genomes of Shimia species and other roseobacters. HC provided analytical facilities and edited the manuscript. BE planned, helped to execute the study and edited the manuscript. All authors read and approved the final manuscript.

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Kanukollu, S., Voget, S., Pohlner, M. et al. Genome sequence of Shimia str. SK013, a representative of the Roseobacter group isolated from marine sediment. Stand in Genomic Sci 11, 25 (2016). https://doi.org/10.1186/s40793-016-0143-0

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Keywords

Environmental Microbiome

ISSN: 2524-6372