- Open Access
Non-contiguous finished genome sequence and description of Collinsella massiliensis sp. nov.
- Published: 15 June 2014
Abstract
Collinsella massiliensis strain GD3T is the type strain of Collinsella massiliensis sp. nov., a new species within the genus Collinsella. This strain, whose genome is described here, was isolated from the fecal flora of a 53-year-old French Caucasoid woman who had been admitted to intensive care unit for Guillain-Barré syndrome. Collinsella massiliensis is a Gram-positive, obligate anaerobic, non motile and non sporulating bacillus. Here, we describe the features of this organism, together with the complete genome sequence and annotation. The genome is 2,319,586 bp long (1 chromosome, no plasmid), exhibits a G+C content of 65.8% and contains 2,003 protein-coding and 54 RNA genes, including 1 rRNA operon.
Keywords
- Collinsella massiliensis
- genome
- culturomics
- taxono-genomics
Introduction
Collinsella massiliensis strain GD3T (= CSUR P902 = DSM 26110) is the type strain of C. massiliensis sp. nov. This bacterial strain was isolated from the fecal flora of a 53-year-old French Caucasoid female admitted to the intensive care unit (ICU) in the Timone Hospital of Marseille, France, for Guillain-Barré syndrome. This study was part of a “culturomics” effort to cultivate all bacteria within human feces [1]. C. massiliensis is a Gram-positive, obligatly anaerobic, non-endospore forming, non-motile and rod shaped bacillus.
Thanks to the development of high throughput sequencers and the rapidly declining cost of genome sequencing, the number of sequenced bacterial genomes has reached almost 12,000 as of January 2nd, 2014, with an additional 18,000 sequencing projects ongoing [2]). In an effort to include genomic information among the genotypic criteria used for the taxonomic description of bacterial isolates, and not only rely on a combination of 16S rRNA gene phylogeny and nucleotide sequence similarity, G + C content and DNA-DNA hybridization [3–6]. We proposed a new strategy named taxono-genomics that we used to describe several new bacterial taxa [7–38].
In 1999, Kageyama et al. reclassified Eubacterium aerofaciens into a new genus named Collinsella [39] based on a 16S rRNA gene sequence divergence and the presence of a unique peptidoglycan type when compared to other members of the genus Eubacterium. In addition to the type species, C. aerofaciens [39], the genus Collinsella currently includes C. intestinalis [40], C. stercoris [40] and C. tanakaei [41]. All four species have been isolated from the human gastrointestinal tract.
In the present manuscript, we apply the taxono-genomics strategy to the description of Collinsella massiliensis sp. nov., and describe the complete genome sequencing and annotation of Collinsella massiliensis strain GD3T (= CSUR P902 = DSM 26110). These characteristics support the circumscription of the C. massiliensis species.
Classification and Features
Classification and general features of Collinsella massiliensis strain GD3T according to the MIGS recommendations [42].
MIGS ID | Property | Term | Evidence codea |
---|---|---|---|
Current classification | Domain Bacteria | TAS [43] | |
Phylum Actinobacteria | TAS [44] | ||
Class Actinobacteria | TAS [45] | ||
Order Coriobacteriales | |||
Family Coriobacteriaceae | TAS [47] | ||
Genus Collinsella | TAS [39] | ||
Species massiliensis | IDA | ||
Type strain GD3T | IDA | ||
Gram stain | Positive | IDA | |
Cell shape | Bacilli | IDA | |
Motility | Non motile | IDA | |
Sporulation | Non spore forming | IDA | |
Temperature range | Mesophilic | IDA | |
Optimum temperature | 37°C | IDA | |
MIGS-6.3 | Salinity | Unknown | NAS |
MIGS-22 | Oxygen requirement | Anaerobic | IDA |
Carbon source | Unknown | NAS | |
Energy source | Unknown | NAS | |
MIGS-6 | Habitat | Human gut | IDA |
MIGS-15 | Biotic relationship | Free living | IDA |
MIGS-14 | Pathogenicity | Unknown | IDA |
Biosafety level | 2 | ||
Isolation | Human feces | ||
MIGS-4 | Geographic location | France | IDA |
MIGS-5 | Sample collection time | January 2012 | IDA |
MIGS-4.1 | Latitude | 43.296482 | IDA |
MIGS-4.1 | Longitude | 5.36978 | IDA |
MIGS-4.3 | Depth | Surface | IDA |
MIGS-4.4 | Altitude | 0 m above sea level | IDA |
A consensus phylogenetic tree highlighting the position of Collinsella massiliensis strain GD3T relative to other type strains within the genus Collinsella. GenBank accession numbers are indicated in parentheses. Sequences were aligned using CLUSTALW and phylogenetic inferences obtained using the neighbor-joining method within the MEGA software. Numbers at the nodes are percentages of bootstrap values obtained analysis from1,000 REPLICTES to generate a majority consensus tree. Eggerthella lenta was used as an outgroup.
Gram staining of Collinsella massiliensis strain GD3T
Transmission electron microscopy of Collinsella massiliensis strain GD3T, made using a Morgagni 268D (FEI Electron Optics, Hillsboro, OR, USA) at an operating voltage of 60 kV. The scale bar represents 500 µm.
Differential characteristics of Collinsella massiliensis strain GD3T with other strains
Properties | C. massiliensis | C. intestinalis | C. aerofaciens | C. tanakei | C. stercoris |
---|---|---|---|---|---|
Cell diameter (µm) | 0.57 | 0.3–0.5 | 0.3–0.7 | 0.5–1.0 | 0.3–0.5 |
Oxygen requirement | anaerobic | anaerobic | anaerobic | anaerobic | anaerobic |
Gram stain | + | + | + | + | + |
Motility | − | − | na | − | − |
Endospore formation | − | − | − | na | − |
Production of | |||||
Alkaline phosphatase | + | + | − | + | + |
Acid phosphatase | + | + | − | + | + |
Catalase | − | na | na | − | na |
Oxidase | − | na | na | − | na |
Nitrate reductase | − | na | na | − | na |
Urease | − | na | − | − | na |
α-galactosidase | + | − | + | − | − |
β-galactosidase | + | − | + | − | + |
β-glucuronidase | − | − | − | + | − |
α-glucosidase | + | − | + | − | − |
β-glucosidase | − | − | − | + | + |
Esterase | − | na | − | − | na |
Esterase lipase | − | − | − | − | − |
Indole | − | na | na | − | na |
N-acetyl-β-glucosaminidase | − | + | − | − | + |
Alanine arylamidase | − | na | − | − | + |
Arginine arylamidase | − | na | + | + | na |
Cystin arylamidase | − | − | − | − | − |
Glutamic acid decarboxylase | − | na | − | − | na |
Glycine arylamidase | + | na | + | + | na |
Leucine arylamidase | − | + | + | + | + |
Leucyl-glycyl arylamidase | − | na | + | + | na |
Proline arylamidase | + | − | + | + | − |
Serine arylamidase | + | na | − | − | + |
Tyrosin arylamidase | − | na | − | − | + |
Valine arylamidase | − | − | + | − | − |
Utilization of | |||||
Glucose | − | + | + | + | + |
Mannose | − | + | + | + | + |
Galactose | − | + | + | na | + |
Fructose | − | + | + | na | + |
Maltose | − | − | + | + | + |
Cellobiose | − | − | − | + | + |
Lactose | − | − | + | + | + |
L-arabinose | − | − | − | − | − |
D-xylose | − | − | − | − | − |
Rhamnose | − | − | na | − | − |
Ribose | − | − | + | + | + |
Raffinose | − | − | na | na | − |
Glycogen | − | − | na | na | − |
Aesculin | − | − | − | − | − |
Mannitol | − | − | − | na | − |
Sorbitol | + | − | − | − | − |
Habitat | human gut | human gut | human gut | human gut | na |
Reference mass spectrum from Collinsella massiliensis strain GD3T. Spectra from 12 individual colonies were compared and a reference spectrum was generated.
Gel view comparing Collinsella massiliensis strain GD3T to other members of the family Coriobacteriaceae. The gel view displays the raw spectra of all loaded spectrum files arranged in a pseudo-gel-like look. The x-axis records the m/z value. The left y-axis displays the running spectrum number originating from subsequent spectra loading. The peak intensity is expressed by a Gray scale scheme code. The color bar and the right y-axis indicate the relation between the color a peak is displayed with and the peak intensity in arbitrary units. Displayed species are detailed in the left column.
Genome sequencing information
Genome project history
Project information
MIGS ID | Property | Term |
---|---|---|
MIGS-31 | Finishing quality | High-quality draft |
MIGS-28 | Libraries used | One 454 paired-end 5-kb library |
MIGS-29 | Sequencing platforms | 454 GS FLX Titanium |
MIGS-31.2 | Fold coverage | 92 × |
MIGS-30 | Assemblers | Newbler version 2.5.3 |
MIGS-32 | Gene calling method | Prodigal |
INSDC ID/GenBank ID | CAPI00000000 | |
BioProject ID | PRJEB541 | |
Genbank Date of Release | 17/12/2012 | |
Project relevance | Study of the human gut microbiome |
Growth conditions and DNA isolation
Collinsella massiliensis strain GD3T (= CSUR P902 = DSM 26110) was grown on 5% sheep blood-enriched Columbia agar (BioMerieux) at 37°C in anaerobic atmosphere. Bacteria grown on four Petri dishes were harvested and resuspended in 4x100µL of TE buffer. Then, 200µL of this suspension was diluted in 1ml TE buffer for lysis treatment that included a 30-minute incubation with 2.5 µg/µL lysozyme at 37°C, followed by an overnight incubation with 20 µg/µL proteinase K at 37°C. Extracted DNA was then purified using 3 successive phenol-chloroform extractions and ethanol precipitation at −20°C overnight. Following centrifugation, the DNA was resuspended in 52 µL TE buffer. The yield and concentration was measured by the Quant-it Picogreen kit (Invitrogen) on the Genios-Tecan fluorometer at 26.3 ng/µl.
Genome sequencing and assembly
Five µg of DNA was mechanically fragmented on Covaris device (KBioScience-LGC Genomics, Teddington, UK) using miniTUBE-red. The DNA fragmentation was visualized through an Agilent 2100 BioAnalyzer on a DNA labchip 7500 with an optimal size of 1.9kb. A 5 kb paired-end library was constructed according to the 454 GS FLX Titanium paired-end protocol (Roche). Circularization and nebulization were performed and generated a pattern with an optimal at 567 bp. After PCR amplification through 17 cycles followed by double size selection, the single stranded paired-end library was quantified with the Quant-it Ribogreen kit (Invitrogen) on the Genios Tecan fluorometer at 505pg/µL. The library concentration equivalence was calculated as 8.17E+09 molecules/µL. The library was stored at −20°C until further use.
The paired-end library was clonally amplified with 0.5cpb and 1cbp in 4 SV-emPCR reactions with the GS Titanium SV emPCR Kit (Lib-L) v2 (Roche). The yields of the emPCR reactions were 9.35 and 14.76% respectively, in the range of 5 to 20% from the Roche procedure. The library was loaded on a GS Titanium PicoTiterPlate PTP Kit 70x75 and sequenced with the GS Titanium Sequencing Kit XLR70 (Roche). The run was performed overnight and then analyzed on the cluster through the gsRunBrowser and Newbler assembler (Roche). A total, of 672,867 passed filter wells were obtained and generated 214.2Mb with a length average of 301bp. These sequences were assembled using Newbler (Roche) with 90% identity and 40bp as overlap. The final assembly identified 15 scaffolds and 118 large contigs (>1500bp) generating a genome size of 2.32 Mb which corresponds to a coverage of 92x genome equivalent.
Genome annotation
Open Reading Frames (ORFs) were predicted using Prodigal [51] with default parameters. However, when predicted ORFs spanned a sequencing gap region, they were excluded. The predicted bacterial protein sequences were searched against the GenBank [52] and Clusters of Orthologous Groups (COG) databases using BLASTP. The tRNAScan-SE [53] and RNAmmer [54] softwares were used to predict tRNAs and rRNAs, respectively. Signal peptides and numbers of transmembrane helices were predicted using SignalP [55] and TMHMM [56], respectively. Mobile genetic elements were predicted using PHAST [57] and RAST [58]. ORFans were identified if their BLASTP E-value was lower than 1e-03 for alignment length greater than 80 amino acids. If alignment lengths were smaller than 80 amino acids, we used an E-value of 1e-05. Such parameter thresholds have already been used in previous works to define ORFans. Artemis [59] and DNA Plotter [60] were used for data management and visualization of genomic features, respectively. Mauve alignment tool (version 2.3.1) was used for multiple genomic sequence alignment [61].
To estimate the mean level of nucleotide sequence similarity at the genome level between C. massiliensis and the other 4 members of the genus Collinsella (Table 6), we used the Average Genomic Identity Of gene Sequences (AGIOS) home-made software [7]. Briefly, this software combines the Proteinortho software [62] for detecting orthologous proteins between genomes compared two by two, then retrieves the corresponding genes and determines the mean percentage of nucleotide sequence identity among orthologous ORFs using the Needleman-Wunsch global alignment algorithm. C. massiliensis strain GD3T was compared to C. intestinalis strain DSM 13280 (GenBank accession number ABHX00000000), C. aerofaciens strain ATCC 25986 (AAVN00000000), C. stercoris strain DSM 13279 (ABXJ00000000), C. tanakaei strain YIT 12063 (ADLS00000000), Eggerthella lenta strain DSM 2243 (CP001726) and Coriobacterium glomerans strain PW2 (CP0002628).
Genome properties
Graphical circular map of the Collinsella massiliensis strain GD3T chromosome. From the outside in: open reading frames oriented in the forward (colored by COG categories) direction, open reading frames oriented in the reverse (colored by COG categories) direction, RNA operon (red), and tRNAs (green), GC content plot, and GC skew (purple: negative values, olive: positive values).
Nucleotide content and gene count levels of the genome
Attribute | Value | % of totala |
---|---|---|
Genome size (bp) | 2,319,586 | |
DNA G+C content (bp) | 1,526,287 | 65.8 |
DNA coding region (bp) | 1,997,199 | 86.10 |
Number of replicons | 1 | |
Extrachromosomal elements | 0 | |
Total genes | 2,054 | 100 |
RNA genes | 54 | 2.62 |
rRNA operons | 1 | |
Protein-coding genes | 2,003 | 97.37 |
Genes with function prediction | 1,503 | 73.06 |
Genes assigned to COGs | 1,370 | 66.60 |
Genes with peptide signals | 40 | 1.94 |
Genes with transmembrane helices | 471 | 22.89 |
CRISPR repeats | 2 |
Number of genes associated with the 25 general COG functional categories
Code | Value | % of totala | Description |
---|---|---|---|
J | 135 | 6.73 | Translation |
A | 0 | 0 | RNA processing and modification |
K | 113 | 5.64 | Transcription |
L | 79 | 3.94 | Replication, recombination and repair |
B | 0 | 0 | Chromatin structure and dynamics |
D | 18 | 0.89 | Cell cycle control, mitosis and meiosis |
Y | 0 | 0 | Nuclear structure |
V | 53 | 2.64 | Defense mechanisms |
T | 29 | 1.44 | Signal transduction mechanisms |
M | 81 | 4.04 | Cell wall/membrane biogenesis |
N | 2 | 0.09 | Cell motility |
Z | 0 | 0 | Cytoskeleton |
W | 0 | 0 | Extracellular structures |
U | 10 | 0.49 | Intracellular trafficking and secretion |
O | 39 | 1.94 | Posttranslational modification, protein turnover, chaperones |
C | 69 | 3.44 | Energy production and conversion |
G | 189 | 9.43 | Carbohydrate transport and metabolism |
E | 123 | 6.14 | Amino acid transport and metabolism |
F | 43 | 2.14 | Nucleotide transport and metabolism |
H | 28 | 1.39 | Coenzyme transport and metabolism |
I | 28 | 1.39 | Lipid transport and metabolism |
P | 46 | 2.29 | Inorganic ion transport and metabolism |
Q | 3 | 0.14 | Secondary metabolites biosynthesis, transport and catabolism |
R | 165 | 8.23 | General function prediction only |
S | 117 | 5.84 | Function unknown |
- | 500 | 24.96 | Not in COGs |
Comparison with other genomes
Distribution of functional classes of predicted genes of C. massiliensis sp. nov. strain GD3T (green) and other members of the genus Collinsella, Eggerthella lenta and Coriobacterium glomerans.
Genomes used in the genomic comparison and their main characteristics
Organism | GenBank id | Size (Mb) | GC% | Genes |
---|---|---|---|---|
Collinsella massiliensis GD3 | CAPI00000000 | 2.32 | 65.8 | 2,054 |
Collinsella intestinalis DSM 13280 | ABXH00000000 | 1.8 | 62.5 | 1,846 |
Collinsella aerofaciens ATCC 25986 | AAVN00000000 | 2.44 | 60.6 | 2,437 |
Collinsella stercoris DSM 13279 | ABXJ00000000 | 2.4 | 63.2 | 2,585 |
Collinsella tanakaei YIT 12063 | ADLS00000000 | 2.48 | 60.2 | 2,276 |
Eggerthella lenta DSM 2243 | CP001726 | 3.63 | 64.2 | 3,184 |
Coriobacterium glomerans PW2 | CP002628 | 2.12 | 60.4 | 1,858 |
Numbers of orthologous protein-coding genes shared among genomes
CM | CA | CI | CS | CT | EL | CG | |
---|---|---|---|---|---|---|---|
CM | 2,003 | 74.61 | 75.95 | 76.51 | 74.37 | 71.24 | 73.73 |
CA | 947 | 2,367 | 74.91 | 75.05 | 74.19 | 68.55 | 71.63 |
CI | 867 | 945 | 1,784 | 81.80 | 75.67 | 69.28 | 72.42 |
CS | 953 | 999 | 1,110 | 2,529 | 75.70 | 69.88 | 72.53 |
CT | 1,029 | 1,082 | 1,108 | 1,151 | 2,212 | 68.46 | 71.50 |
EL | 751 | 764 | 740 | 777 | 856 | 3,070 | 68.52 |
CG | 841 | 841 | 818 | 861 | 898 | 639 | 1,768 |
Conclusion
On the basis of phenotypic, phylogenetic and genomic analyses (taxono-genomics), we formally propose the creation of Collinsella massiliensis sp. nov. That contains strain GD3T as type strain. The strain was isolated from the fecal flora of a 53-year-old woman hospitalized in ICU in Marseille, France, due to a Guillain-Barré syndrome.
Description of Collinsella massiliensis strain sp. nov.
Collinsella massiliensis (mas.si.li.en’sis. L. masc. adj. massiliensis of Massilia, the Roman name of Marseille, France, where type strain GD3T was isolated).
Colonies are grey, translucent and 0.4 mm in diameter on blood-enriched Columbia agar. Cells are rod shaped with a mean diameter and length of 0.57 and 1.19 µm, respectively. Optimal growth is achieved anaerobically only. Growth occurs at 37 and 45°C, with optimal growth observed at 37°C.
Cells stain Gram-positive, are non-endospore forming and are non-motile. Cells are negative for catalase and oxidase. Positive reactions are observed for acid phosphatase, alkaline phosphatise, naphthol-AS-BI-phosphohydrolase, α-galactosidase, α-galactosidase, α-glucosidase, α-fucosidase, leucine arylamidase, proline arylamidase, arginine dihydrolase, serine arylamidase, glycine arylamidase and acidification of D-sorbitol, D-saccharose, xylitol, D-arabitol and potassium-5-ketogluconate. Negative reactions are observed for leucine arylamidase, valine arylamidase, cystin arylamidase, β-glucuronidase, nitrate reduction, urease, esterase (C4), esterase lipase (C8), lipase (C14), Trypsin, α-chemotrypsin, N-actetyl-β-glucosaminidase, α-mannosidase, α-fucosidase, histidin arylamidase, urease, phenylalanine arylamidase, tyrosin arylamidase, leucyl-glycyl arylamidase, alanine arylamidase, arginine arylamidase and fermentation of glycerol, erythritol, D-arabinose, L-arabinose, D-ribose, D-xylose, L-xylose, D-adonitol, methyl-β-D-xylopranoside, D-galactose, D-glucose, D-fructose, D-mannose, L-sorbose, L-rhamnose, dulcitol, inositol, D-mannitol, methyl-αD-xylopranoside, methyl-αD-glucopranoside, N-acetylglucosamine, amygdalin, arbutin, aesculin ferric citrate, salicin, D-cellobiose, D-maltose, D-lactose, D-mellibiose, D-trehalose, inulin, D-melezitose, D-raffinose, amidon, glycogen, gentiobiose, D-turanose, D-lyxose, D-tagatose, L-fucose, L-arabitol, potassium gluconate and potassium 2-ketogluconate. Positive reactions were recorded for acid phosphatase, naphthol-AS-BI-phosphohydrolase, α-galactosidase, alkaline phosphatase, leucine arylamidase, valine arylamidase, a-glucosidatse and β glucosidasee. Cells are susceptible to penicillin G, amoxicillin, amoxicillin-clavulanic acid, ceftriaxone, imipenem, metronidazole, vancomycin, rifampicin but resistant to erythromycin, gentamicin, ciprofloxacin and trimethoprim/sulfa-methoxazole.
The 16S rRNA and genome sequences are deposited in GenBank and EMBL under accession numbers JX424766 and CAPI00000000, respectively. The G+C content of the genome is 65.8%. The habitat of the microorganism is the human digestive tract. The type strain GD3T (= CSUR P902 = DSM 26110) was isolated from the fecal flora of a French Caucasoid woman who suffered from Guillain-Barré syndrome. This strain was isolated in Marseille, France.
Notes
Authors’ Affiliations
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