Genome sequence and description of Timonella senegalensis gen. nov., sp. nov., a new member of the suborder Micrococcinae
© The Author(s) 2013
Published: 15 June 2013
Timonella senegalensis strain JC301T gen. nov., sp. nov. is the type strain of T. senegalensis gen. nov., sp. nov., a new species within the newly proposed genus Timonella. This bacterial strain was isolated from the fecal flora of a healthy Senegalese patient. In this report, we detail the features of this organism, together with the complete genome sequence and annotation. Timonella senegalensis strain JC301T exhibits the highest 16S rRNA similarity (95%) with Sanguibacter marinus, the closest validly published bacterial species. The genome of T. senegalensis strain JC301T is 3,010,102-bp long, with one chromosome and no plasmid. The genome contains 2,721 protein-coding genes and 72 RNA genes, including 5 rRNA genes. The genomic annotation revealed that T. senegalensis strain JC301T possesses the complete complement of enzymes necessary for the de novo biosynthesis of amino acids and vitamins (except for riboflavin and biotin), as well as the enzymes involved in the metabolism of various carbon sources, chaperone genes, and genes involved in the regulation of polyphosphate and glycogen levels.
KeywordsTimonella senegalensis genome culturomics taxono-genomics
Timonella senegalensis strain JC301T (= CSUR P167 = DSMZ 25696) is the type strain of T. senegalensis gen. nov., sp. nov. This bacterium is a Gram-positive, facultatively anaerobic, flagellated, 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 4,000 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 [4–22].
Here we present a summary classification and a set of features for T. senegalensis gen. nov., sp. nov. strain JC301T (= CSUR P167 = DSMZ 25696) together with the description of the complete genomic sequencing and annotation. These characteristics support the circumscription of a novel genus, Timonella gen. nov. within the suborder Micrococcineae, with Timonella senegalensis gen. nov., sp. nov. as the type species.
The suborder Micrococcineae was created in 1997  and currently comprises eighteen different families that mostly includes Gram-positive bacteria. Members of the suborder Micrococcineae are usually present in soil, water, terrestrial, marine environments, humans and animal intestinal microbiota.
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 Aeromicrobium massiliense sp. nov., Alistipes senegalensis sp. nov., Alistipes timonensis sp. nov., Anaerococcus senegalensis sp. nov., Brevibacterium senegalense sp. nov., Cellulomonas massiliensis sp. nov., Clostridium senegalense sp. nov., Enterobacter massiliensis sp. nov., Herbaspirillum massiliense sp. nov., Kurthia massiliensis sp. nov., Paenibacillus senegalensis sp. nov., Peptoniphilus timonensis sp. nov., and Senegalemassilia anaerobia gen. nov., sp. nov. [5–16, 18,19].
Classification and general features of Timonella senegalensis strain JC301T according to the MIGS recommendations 
Species Timonella senegalensis
Type strain JC301T
short, irregular rods
growth in BHI medium + 1% NaCl
primarily aerobic, facultatively anaerobic
broad variety of sugars
Sample collection time
51 m above sea level
Differential characteristics of Timonella senegalensis gen. nov., sp. nov., strain JC301T, Cellulomonas fimi strain ATCC484, Oerskovia turbata strain ATCC 25835 and Sanguibacter keddieii strain ST-74T
Cell diameter (µm)
Cell Wall (major constituents)
alanine, glutamic acid and glucosamine
rhamnose, mannose, fucose and glucosamine
alanine, glutamic acid, glucosamine, muramic acid, galactose, lysine
alanine, glutamic acid, rhamnose and glucosamine
soil, decaying plant materials and clinical specimens
blood of healthy cow
Genome sequencing information
Genome project history
Shot Gun, Paired-end 3 Kb library
454 GS FLX Titanium
Newbler version 2.5.3
Gene calling method
Genbank Date of Release
June 1, 2012
Study of the human gut microbiome
Growth conditions and DNA isolation
T. senegalensis sp. gen. nov. strain JC301T (= CSUR P167 = DSMZ 25696) was grown aerobically on 5% sheep blood-enriched BHI agar at 37°C. The growth from four Petri dishes was collected and resuspended in 4×500 µl of TE buffer and stored at −20°C. Then, 500 µl of this suspension was thawed, centrifuged for 3 minutes at 10,000 rpm and resuspended in 4×100 µL of G2 buffer (EZ1 DNA Tissue Kit, Qiagen). An initial mechanical lysis was performed with glass powder and the Fastprep-24 device (Sample Preparation System, MP Biomedicals, USA) using two 20-seconds cycles. DNA was then treated with 2.5 µg/µL lysozyme for 30 minutes at 37°C and extracted using the BioRobot EZ1 Advanced XL (Qiagen). The DNA was then concentrated and purified using a QIAmp Kit (Qiagen). The yield and the concentration were measured at 754 ng/µL using the Quant-it Picogreen Kit (Invitrogen) on the Genios Tecan fluorometer.
Genome sequencing and assembly
DNA (5 µg) was mechanically fragmented with a Hydroshear device (Digilab, Holliston, MA, USA) with an enrichment size of 3–4 kb. The DNA fragmentation was visualized using the Agilent 2100 BioAnalyzer on a DNA Labchip 7500 with an optimal size of 3.3 kb. The library was constructed using the 454 GS FLX Titanium paired-end protocol. Circularization and nebulization were performed and generated a pattern with an optimal size of 544 bp. After PCR amplification for 15 cycles and double size selection, the single-stranded paired-end library was then quantified using a Quant-it Ribogreen Kit (Invitrogen) using the Genios Tecan fluorometer. The library concentration equivalence was calculated as1.99× 109 molecules/µL. The library was stored at −20°C until further use.
The shotgun library was clonally amplified with 0.5 cpb and the paired-end library was amplified with 1 cpb in four emPCR reactions using the GS Titanium SV emPCR Kit (Lib-L) v2 (Roche). The yields of the emPCR were 16.25% for the shotgun library and 15.92% for the paired-end library. These yields fall into the expected 5 to 20% range as per the Roche protocol.
Approximately 790,000 beads for a quarter region and 340,000 beads for an eighth region were loaded on the GS Titanium PicoTiterPlate PTP Kit 70×75 and sequenced with the GS FLX Titanium Sequencing Kit XLR70 (Roche). The run was performed overnight and then analyzed on a cluster using the gsRunBrowser and Newbler assembler (Roche). For the shotgun sequencing, 794,539 passed-filter wells were obtained. The sequencing generated 77.43 Mb with an average length of 190 bp. The passed-filter sequences were assembled using Newbler with 90% identity and 40 bp as overlap. The final assembly identified 78 contigs (between 1,468 bp and 199,104 bp) generated a genome size of 3.0 Mb, which corresponds to coverage of 22.05 genome equivalents.
Open Reading Frames (ORFs) were predicted using Prodigal  with default parameters but the predicted ORFs were excluded if they were spanning 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. 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. To estimate the mean level of nucleotide sequence similarity at the genome level between T. senegalensis strain JC301T, Sanguibacter keddieii strain ST-74T (GenBank accession number CP001819) and Cellulomonas fimi strain ATCC 484 (GenBank accession number CP002666), we identified orthologous proteins using the Proteinortho software (version 1.4) and the following criteria: 30% amino acid identity and a E-value of 1e-05. The average percentages of nucleotide sequence identity between corresponding orthologous sets were then determined using the Needleman-Wunsch algorithm global alignment technique. Artemis  was used for data management and DNA Plotter  was used for visualization of genomic features. Mauve alignment tool was used for multiple genomic sequence alignment and visualization .
Nucleotide content and gene count levels of the genome
% of totala
Genome size (bp)
DNA coding region (bp)
DNA G+C content (bp)
Number of replicons
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
Genome comparison with Sanguibacter keddieii and Cellulomonas flavigena
Numbers of orthologous protein shared between genomes (upper right triangle), average percentage similarity of nucleotides corresponding to orthologous protein shared between genomes (lower left triangle) and the numbers of proteins per genome (bold).
Experimentally, T. senegalensis strain JC301T was able to grow under aerobic conditions and to utilize a variety of carbon substrates. Genome annotation clearly confirmed that this strain was able to use these carbon sources and to catabolize them via different pathways (glycolysis, pentose phosphate, TCA cycles and Entner-Doudoroff pathways). Strain JC301T could effectively catabolize a variety of carbon substrates, such as D-fructose, L-arabinose, ribose, D-raffinose, xylose, D-galacturonate and D-glucuronate. Glycogen is a major intracellular carbon source reserve polymer. It is accumulated under conditions of limiting growth when an excess of carbon is available and other nutrients are deficient . In strain JC301T, both the genes encoding the proteins required for glycogen biosynthesis and glycogen degradation are present, suggesting that it can survive for a longer period under carbohydrate starvation conditions. A variety of enzymes are present, including those required for gluconeogenesis and fermentation to lactate and acetate, as well as production of butyrate from branched amino acids. Acetyl-CoA can be used for anabolic purposes (fatty acid synthesis) or converted to acetate and butyrate. All four genes that encode enzymes for butyrate fermentation are found in the genome, including acetyl-CoA acetyltransferase, 3-hydroxybutyryl-CoA dehydrogenase, crotonase, and butyryl-CoA dehydrogenase.
Fatty acid biosynthesis and oxidation
T. senegalensis strain JC301T uses the non-mevalonate pathway for isoprenoid biosynthesis. All genes necessary for fatty acid and phospholipid biosynthesis are present. The strain also possesses the genes necessary for fatty acid biosynthesis initiation, keto group reduction, dehydration, and enoyl reduction. A cardiolipin synthetase gene is predicted in the JC301T genome. This enzyme is found almost exclusively in certain bacterial membranes (plasma membrane and hydrogenosomes) and functions to generate an electrochemical potential for substrate transport and ATP synthesis . In addition, the strain has genes of the fatty acid beta-oxidation system, suggesting that it can use fatty acids as carbon sources.
All genes required for de novo inosine monophosphate synthesis appear to be present in the T. senegalensis genome. Genes for uracil monophosphate synthesis are also organized in an operon interrupted by a conserved hypothetical ORF. The ORFs that encode the enzymes of uracil monophosphate (UMP) biosynthesis are closely related to the Gram-positive S. keddieii. Nucleoside monophosphate kinases for all types of nucleotides are present. Deoxyribonucleotides can be synthesized under both aerobic and anaerobic conditions by ribonucleoside-diphosphate and ribonucleoside-triphosphate reductases. Enzymes necessary for the purine and pyrimidine salvage pathway are also present. The purine salvage enzymes and uracil phosphoribosyltransferase are highly homologous to the corresponding enzymes of Gram-positive bacteria. Thymidine monophosphate is formed by thymidylate synthase from dUMP, providing the only interconversion pathway between pyrimidine nucleotides. In addition, there are four genes from the xanthine/uracil permease family of proteins involved in the transport of free bases. Thus, T. senegalensis can use exogenous bases and nucleosides. The pst operon encodes a phosphate-binding periplasmic protein, transport protein PstC, and a permease protein (PstA). All genes for phosphate lyase or other phosphonate degradation enzymes are present, suggesting that phosphates can be transported and further used.
Respiration and proton transfer
All key proteins and protein complexes known to be important in aerobic complexes are present in the genome of T. senegalensis, including genes responsible for the synthesis of terminal cytochrome or quinol oxidases or complexes I, II, and III of the aerobic respiratory chain and ORFs for the synthesis of quinones or menaquinones. Two genes required for anaerobic respiration, arsenate reductase and ferredoxin reductase are present in the genome. Several proteins contributing to the proton gradient, including a proton:sodium-glutamate symporter, a sodium:proton antiporter, a V-type H+-translocating ATP synthase (EC 22.214.171.124), and a Na+-transporting ATP synthase (EC 126.96.36.199) are present in the genome.
Transcription and translation
The T. senegalensis components of the transcriptional apparatus, consisting of the genes encoding the αββ′β″ and ω subunits of RNA polymerase (RNAP), are similar to those of a Gram-positive polymerase. For transcription termination, one gene encodes a Rho factor similar to that of S. keddieii. In addition, homologs of NusA and NusB are also present. All the typical prokaryotic translation initiation factors, IF-1, IF-2, and IF-3, are present. Two ORFs for the elongation factor EF-G as well as EF-Tu, EF-Ts, and EF-p (elongation factor for peptide bond synthesis) genes are also present. T. senegalensis encodes three peptide chain release factors, RF-1, RF-2 and RF-3. Large and small ribosomal subunit proteins for the assembly of the ribosome are present in the genome. Modifying proteins such as ribosomal protein alanine acetyltransferase and large ribosomal subunit pseudouridine synthase subunits A, B, and D are present. Sixty-four ORFs code for tRNAs for all 20 amino acids. All types of tRNA ligases are present in the genome.
Approximately 5% of the ORFs in the genome are dedicated to transport of a variety of compounds by primary and secondary transport systems. These transporters are energized by ATP, sodium, or proton gradients. There are 40 complete ABC transporter operons. The predominant substrates for ABC transporters appear to be oligopeptides and iron compounds. In contrast, there are three ABC transporters for amino acids. There are ABC transporters for other metal ions such as cobalt, nickel, manganese, zinc, and copper. The transmembrane sodium gradient appears to be as important for transport as the proton gradient. Most of the amino acid transporters are sodium-dependent. There are two potassium uptake systems: one is a sodium symporter, and the other is a proton symporter. Eight predicted sodium:proton antiporters are present in the genome. T. senegalensis uses these antiporters to balance ion gradients and to adjust to the pH changes in the gut environment. There are transporters for all of the essential ions and all the L-amino acids.
Adaptability to human gut
Strain JC301T was isolated from the human gut, suggesting that it can use substrates present in the colon. Accordingly, the complete pathway for gluconic acid degradation, including gluconate kinase and 6-phosphogluconate dehydrogenase was identified, in agreement with gluconate utilization.
The presence of stress-induced genes reflect the ability to cope with digestive (acid and bile) stresses. Regulation of intracellular pH is crucial for survival. Genome analysis of strain JC301T revealed a complete atpBEFHAGDC operon, which is induced by acid and bile salts . These stimuli also induce pyruvate-flavodoxin oxidoreductase and succinate dehydrogenase, involved in electron transport and ATP synthesis, as well as glutamate decarboxylase and aspartate ammonia-lyase, which regulates the homeostasis of intracellular pH . Proteins involved in protection and repair of DNA are crucial for survival. Genome analysis demonstrated the presence of members of the SOS response including lexA, recA and uvrABC in T. senegalensis and S. keddieii. Moreover, the helix-destabilizing single-stranded DNA-binding protein (SSB), involved in DNA recombination and repair , as well as Dps (DNA-binding proteins from starved cells), which protects DNA against oxidative stress , are present in the genome. This reflects the ability to modulate envelope properties. In addition, strain JC301T possesses an arsenal of genes for disulfide-reduction and elimination of reactive oxygen species, required for survival and activity within the gut against oxidative stress induced by bile. The occurrence of a sodium/bile acid symporter also reflects adaptation to the gut environment . Moreover, genes encoding multidrug resistance transporters are present in T. senegalensis and S. keddieii, indicating an ability to cope with toxic compounds. The presence of two genes encoding heavy metal translocating P-type ATPases further suggests an adaptation to toxic environments. Thus, the genome content suggests T. senegalensis has significant environmental adaptation ability. Further genome analysis revealed the presence of several genes required for the inducibility of the different aspects of the chaperone and protease machinery. This suggests an ability to efficiently and rapidly adapt to stressful environments, such as would be found in a human host.
Description of Timonella gen. nov.
Timonella (Ti.mon.el′la N.L. fem. N. Timonella, from Timone, the name of the hospital in Marseille where strain JC301T was first cultivated).
Gram-positive rods. Facultatively anaerobic. Mesophilic. Motile. catalase-positive. Absent oxidase. Positive for urease, arginine dihydrolase, indole production, β-glucuronidase, mannose fermentation, alkaline phosphatase alcaline, arginine arylamidase, leucyl glycine arylamidase and histidine arylamidase. Habitat: human digestive tract. Type species: Timonella senegalensis.
Description of Timonella senegalensis gen. nov., sp. nov.
Timonella senegalensis (se.ne.gal.e′n.sis. L. gen. masc. n. senegalensis, pertaining to Senegal, the country from which the patient came).
Gram-positive, catalase-positive, oxidase-negative and facultatively anaerobic. Cells are irregular, non-endospore forming, short, irregular motile rods with a mean diameter of 0.59 µm. Colonies are white, circular and convex with entire edges on 5% sheep blood agar in aerobic atmosphere at 37°C. Diffusible pigments are not produced. Optimal growth occurs under aerobic conditions. Grows at 30–37 °C (optimum 37 °C). Cells are positive for urease, arginine dihydrolase, indole production, β-glucuronidase, mannose fermentation, alkaline phosphatase alcaline, arginine arylamidase, leucyl glycine arylamidase and histidine arylamidase (API50CH). Cells have nitrate reduction ability and β-galactosidase activity (API 20 NE kit). Positive reactions for L-arabinose, D-galactose, D-glucose, D-maltose, D-saccharose, gentiobiose, arbutine, esculine, salicine (API 50 CH). A weak reaction was obtained for pyroglutamyl arylamidase. Susceptible to amoxicillin, imipenem, ciprofloxacin and gentamicin but resistant to trimethoprim/sulfamethoxazole and metronidazole. The potential pathogenesis of the type strain JC301T is unknown.
The type strain is JC301T (= CSUR P167 = DSMZ 25696) was isolated from the fecal flora of a healthy patient from Dielmo (a rural village in the Guinean-Sudanian zone in Senegal). The genomic DNA G+C content of the type strain is 61.4 mol%. The 16S rRNA gene sequences were deposited in GenBank with the accession number JN657220. The whole-genome shotgun sequence of T. senegalensis strain JC301T has been deposited in GenBank/DDBJ/EMBL under accession number CAHH00000000.
The authors thank the Xegen Company (www.xegen.fr) for automating the genomic annotation process. This study was funded by the Mediterranee Infection Foundation.
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