Non contiguous-finished genome sequence and description of Enterobacter massiliensis sp. nov.
© The Author(s) 2013
Published: 25 February 2013
Enterobacter massiliensis strain JC163T sp. nov. is the type strain of E. massiliensis sp. nov., a new species within the genus Enterobacter. This strain, whose genome is described here, was isolated from the fecal flora of a healthy Senegalese patient. E. massiliensis is an aerobic rod. Here we describe the features of this organism, together with the complete genome sequence and annotation. The 4,922,247 bp long genome (1 chromosome but no plasmid) exhibits a G+C content of 55.1% and contains 4,644 protein-coding and 80 RNA genes, including 5 rRNA genes.
Enterobacter massiliensis strain JC163T (= CSUR P161 = DSM 26120) is the type strain of E. massiliensis sp. nov. This bacterium is a Gram-negative, aerobic, flagellate, indole-positive bacillus that was isolated from the feces of a healthy Senegalese patient in a study aiming at cultivating all bacterial species in human feces . The current classification of prokaryotes, known as polyphasic taxonomy, relies on a combination of phenotypic and genotypic characteristics . However, as more than 3,000 bacterial genomes have been sequenced  and the cost of genomic sequencing is decreasing, we recently proposed to integrate genomic information in the description of new bacterial species [4–15].
Here we present a summary classification and a set of features for E. massiliensis sp. nov. strain JC163T (= CSUR P161 = DSM 26120), together with the description of the complete genomic sequencing and annotation. These characteristics support the circumscription of the species E. massiliensis. The genus Enterobacter (Hormaeche and Edwards, 1960) was created in 1960 . To date, this genus is comprised of 25 species [17–35] and 2 subspecies. Members of the genus were isolated mostly from the environment, in particular from plants and fruits, but are also frequently isolated from humans, notably in health-care associated infections, causing bacteremia, pneumonia or urinary tract infections . In addition, many Enterobacter spp. were isolated from the normal fecal flora.
Classification and features
A stool sample was collected from a healthy 16-year-old male Senegalese volunteer patient living in Dielmo (rural village in the Guinean-Sudanian zone in Senegal), who was included in a research protocol. Written assent was obtained from this individual. No written consent was needed from his guardians for this study because he was older than 15 years old (in accordance with the previous project approved by the Ministry of Health of Senegal and the assembled village population and as published elsewhere ).
Both this study and the assent procedure were approved by the National Ethics Committee of Senegal (CNERS) and the Ethics Committee of the Institut Fédératif de Recherche IFR48, Faculty of Medicine, Marseille, France (agreement numbers 09-022 and 11-017). Several other new bacterial species were isolated from this specimen using various culture conditions, including the recently described Alistipes senegalensis, Alistipes timonensis, Anaerococcus senegalensis, Bacillus timonensis, Clostridium senegalense, Peptoniphilus timonensis, Paenibacillus senegalensis, Herbaspirillum massiliense, Kurthia massiliensis, Brevibacterium senegalense, Aeromicrobium massiliense andCellulomonas massiliensis [4–15].
Classification and general features of Enterobacter massiliensis strain JC163T
Species Enterobacter massiliensis
Type strain: JC163T
Sample collection time
51 m above sea level
Strain JC163T exhibited catalase activity but not oxidase activity. Using the API 20E system, positive reactions were obtained for indole production, β-galactosidase and glucose, mannitol, sorbitol and rhamnose fermentation. E. massiliensis is susceptible to ticarcillin, imipenem, trimethoprim/sulfamthoxazole, gentamicin, amikacin, and colimycin but resistant to fosfomycin and nitrofurantoin. By comparison with E. arachidis, its phylogenetically-closest neighbor, E. massiliensis differed in arginine dihydrolase, ornithine decarboxylase, citrate and succinate fermentation .
Genome sequencing information
Genome project history
Paired-end 3 Kb library
454 GS FLX Titanium
Newbler version 2.5.3
Gene calling method
EMBL Date of Release
November 19, 2012
Study of the human gut microbiome
Growth conditions and DNA isolation
E. massiliensis strain JC163T, (= CSUR P161 = DSM 26120) was grown aerobically on BHI agar at 37°C. Four petri dishes were spread and resuspended in 3×100µl of G2 buffer. A first mechanical lysis was performed by glass powder on the Fastprep-24 device (Sample Preparation system, MP Biomedicals, USA) during 2×20 seconds. DNA was then treated with 2.5 µg/µL lysozyme (30 minutes at 37°C) and extracted through the BioRobot EZ 1 Advanced XL (Qiagen). The DNA was then concentrated and purified on a Qiamp kit (Qiagen). The yield and the concentration was measured by the Quant-it Picogreen kit (Invitrogen) on the Genios_Tecan fluorometer at 118 ng/µl.
Genome sequencing and assembly
A 3kb paired-end sequencing strategy (Roche, Meylan, France) was used. Five µg of DNA was mechanically fragmented on the Hydroshear device (Digilab, Holliston, MA, USA) with an enrichment size at 3–4kb. The DNA fragmentation was visualized using an Agilent 2100 BioAnalyzer on a DNA labchip 7500, with an optimal size of 4.648kb. The library was constructed according to the 454_Titanium paired end protocol (Roche). Circularization and nebulization were performed and generated a pattern with an optimal at 437 bp. Following PCR amplification through 15 cycles followed by double size selection, the single stranded paired-end library was then quantified on the Quant-it Ribogreen kit (Invitrogen) on the Genios_Tecan fluorometer at 122pg/µL. The library concentration equivalence was calculated as 5.12E+08 molecules/µL. The library was stored at −20°C until use. The library was clonally amplified with 1 cpb in 4 emPCR reactions with the GS Titanium SV emPCR Kit (Lib-L) v2 (Roche). The yield of the emPCR was 14.45%, in the 5 to 20% range recommended by the Roche procedure.
Approximately 790,000 beads were loaded on ¼ region of a GS Titanium PicoTiterPlate (PTP Kit 70x75, Roche) and pyrosequenced with the GS Titanium Sequencing Kit XLR70 and the GS FLX Titanium sequencer (Roche). The run was performed overnight and then analyzed on the cluster through the gsRunBrowser and Newbler assembler (Roche). A total of 283,817 passed filter wells generated 80.8 Mb with a length average of 284 bp. The passed filter sequences were assembled using Newbler with 90% identity and 40 bp as overlap. The final assembly identified 224 contigs arranged in 11 scaffolds and generated a genome size of 4.92 Mb.
Open Reading Frames (ORFs) were predicted using Prodigal  with default parameters but the predicted ORFs were excluded if they spanned a sequencing gap region. The predicted bacterial protein sequences were searched against the GenBank database  and the Clusters of Orthologous Groups (COG) databases using BLASTP. The tRNAScanSE tool  was used to find tRNA genes, whereas ribosomal RNAs were found by using RNAmmer  and BLASTN against the GenBank database. Signal peptides and numbers of transmembrane helices were predicted using SignalP  and TMHMM  respectively.
To estimate the mean level of nucleotide sequence similarity at the genome level between E. massiliensis strain JC163T, E. aerogenes strain KCTC 2190 (GenBank accession number CP002824), E. asburiae strain LF7a (CP003026), E. cancerogenus strain ATCC35316 (ABWM00000000), E. cloacae subsp. cloacae strain ATCC13047 (CP001918), E. cloacae subsp. dissolvens strain SDM (CP003678) and E. hormaechei strain ATCC49162 (AFHR00000000), we compared the ORFs only using BLASTN and the following parameters: a query coverage of > 70% and a minimum nucleotide length of 100 bp.
Nucleotide content and gene count levels of the genome
% of totala
Genome size (bp)
DNA coding region (bp)
DNA G+C content (bp)
Genes with function prediction
Genes assigned to COGs
Genes with peptide signals
Genes with transmembrane helices
Number of genes associated with the 25 general COG functional categories
RNA processing and modification
Replication, recombination and repair
Chromatin structure and dynamics
Cell cycle control, mitosis and meiosis
Signal transduction mechanisms
Cell wall/membrane biogenesis
Intracellular trafficking and secretion
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
Comparison with other Enterobacter species genomes
Here, we compared the genome of E. massiliensis strain JC163T with those of E. aerogenes strain KCTC 2190, E. asburiae strain LF7a, E. cancerogenus strain ATCC35316, E. cloacae subsp. cloacae strain ATCC13047, E. cloacae subsp. dissolvens strain SDM and E. hormaechei strain ATCC49162. The draft genome of E. massiliensis is smaller than those of E. aerogenes, E. cloacae subsp. cloacae and E. cloacae subsp. dissolvens (4.92, 5.28, 5.59 and 4.96Mb, respectively), but larger than those of E. asburiae, E. cancerogenus and E. hormaechei (3.81, 4.60 and 4.80, respectively). E. massiliensis has a similar G + C content to E. cloacae subsp. dissolvens (55.1%) but larger than E. aerogenes, E. asburiae and E. cloacae subsp. cloacae (54.8, 53.8 and 54.79%, respectively) and lower than E. cancerogenus and E. hormaechei (55.8 and 55.2%, respectively). E. massiliensis had a greater number of predicted genes than E. cancerogenus and E. cloacae subsp. dissolvens (4,724, 4,642 and 4,646, respectively), but a smaller number than E. aerogenes, E. asburiae, E. cloacae subsp. cloacae and E. hormaechei (5,021, 4,805, 5,627 and 4,779, respectively).
In addition, E. massiliensis shared a mean genome sequence similarity of 84.26% (range 70.05-100%), 83.89% (70.03-100%), 84.36% (70.05-100%), 84.14% (70.00-100%), 84.14% (70.05-100%) and 84.38% (70.24-100%) with E. aerogenes, E. asburiae, E. cancerogenus, E. cloacae subsp. cloacae, E. cloacae subsp. dissolvens and E. hormaechei, respectively.
On the basis of phenotypic, phylogenetic and genomic analyses, we formally propose the creation of Enterobacter massiliensis sp. nov. that contains strain JC163T. This bacterium was cultivated from a healthy Senegalese individual, from whom several other previously undescribed bacterial species were also cultivated through diversification of culture conditions [4–15], thus suggesting that the human fecal flora from humans remains partially unknown.
Description of Enterobacter massiliensis sp. nov.
Enterobacter massiliensis (mas.il.i.en’sis. L. gen. masc. n. massiliensis, of Massilia, the Latin name of Marseille where strain JC163T was first isolated and cultivated).
Colonies are 2 mm in diameter on Brain-Heart Infusion agar and are convex, opaque, light-cream colored and circular with regular margins. Cells are rods with tufts of polar flagella and a mean diameter of 1.02 µm and a mean length of 1.90 µm. Optimal growth is achieved in an aerobic atmosphere supplemented with 5% CO2. Weak growth is observed in microaerophilic conditions. No growth is observed under anaerobic conditions in the absence of CO2. Growth occurs between 25 and 45°C, with optimal growth occurring between 30 and 37°C. Cells stain Gram-negative, are non-endospore forming and are motile. Cells are positive for catalase and indole production. β-galactosidase and glucose, mannitol, sorbitol and rhamnose fermentation activities are present. Nitrate reduction, urease and oxidase activities are absent. Cells are susceptible to ticarcillin, imipenem, trimethoprim/sulfamethoxazole, gentamicin, amikacin, and colimycin, but resistant to fosfomycin and nitrofurantoin. The G+C content of the genome is 55.1%. The 16S rRNA and genome sequences are deposited in Genbank and EMBL under accession numbers JN657217 and CAEO00000000, respectively. The type strain JC163T (= CSUR P161 = DSM 26120) was isolated from the fecal flora of a healthy patient in Senegal.
This study was funded by the Mediterranee Infection Fundation. The authors thank Mr Julien Paganini at Xegen Company (www.xegen.fr) for automating the genomic annotation process.
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