- Open Access
Complete genome sequence of Eggerthella lenta type strain (VPI 0255T)
- Elizabeth Saunders1,
- Rüdiger Pukall2,
- Birte Abt2,
- Alla Lapidus1,
- Tijana Glavina Del Rio1,
- Alex Copeland1,
- Hope Tice1,
- Jan-Fang Cheng1,
- Susan Lucas1,
- Feng Chen1,
- Matt Nolan1,
- David Bruce1, 3,
- Lynne Goodwin1, 3,
- Sam Pitluck1,
- Natalia Ivanova1,
- Konstantinos Mavromatis1,
- Galina Ovchinnikova1,
- Amrita Pati1,
- Amy Chen4,
- Krishna Palaniappan4,
- Miriam Land1, 5,
- Loren Hauser1, 5,
- Yun-Juan Chang1, 5,
- Cynthia D. Jeffries1, 5,
- Patrick Chain1, 6,
- Linda Meincke1, 3,
- David Sims1, 3,
- Thomas Brettin1, 3,
- John C. Detter1, 3,
- Markus Göker2,
- Jim Bristow1,
- Jonathan A. Eisen1, 7,
- Victor Markowitz4,
- Philip Hugenholtz1,
- Nikos C. Kyrpides1,
- Hans-Peter Klenk2 and
- Cliff Han1, 3
- Published: 29 September 2009
Abstract
Eggerthella lenta (Eggerth 1935) Wade et al. 1999, emended Würdemann et al. 2009 is the type species of the genus Eggerthella, which belongs to the actinobacterial family Coriobacteriaceae. E. lenta is a Gram-positive, non-motile, non-sporulating pathogenic bacterium that can cause severe bacteremia. The strain described in this study has been isolated from a rectal tumor in 1935. Here we describe the features of this organism, together with the complete genome sequence, and annotation. This is the first complete genome sequence of the genus Eggerthella, and the 3,632,260 bp long single replicon genome with its 3123 protein-coding and 58 RNA genes is part of the Genomic Encyclopedia of Bacteria and Archaea project.
Keywords
- mesophile
- anaerobic
- human intestinal microflora
- pathogenic
- bacteremia
- Gram-positive
- Coriobacteriaceae
Introduction
Strain VPI 0255T (= DSM 2243 = ATCC 25559 = JCM 9979) is the type strain of the species Eggerthella lenta, which was first described in 1935 by Eggerth as ‘Bacteroides lentus’ [1], later in 1938 renamed by Prévot in ‘Eubacterium lentum’ [2], and was also known under the synonym ‘Pseudobacterium lentum’ Krasil’nikov 1949 [3]. The strain has been described in detail by Moore et al. in 1971 [4]. Based on 16S rRNA sequence divergence and the presence of unique phenotypic characters the strain was then transferred to the new genus Eggerthella as E. lenta (Kageyama et al. 1999, Wade et al. 1999 [5,6] In 2004 two novel Eggerthella species, E. hongkongensis and E. sinensis were characterized and described in addition [7]. Recently, E. hongkongensis was reclassified as Paraeggerthella hongkongensis [8]. Although the two Eggerthella species and P. hongkongensis are part of the human gut flora, they can be the agent of severe bacteremia. So far the pathogenic potential of the genera are poorly analyzed [7]. Here we present a summary classification and a set of features for E. lenta VPI 0255T, together with the description of the complete genomic sequencing and annotation.
Classification and features
Members of the species E. lenta have been isolated from several abscesses, from appendix tissues, peritoneal fluid and intestinal tumors. The organism is often involved in mixed infections with less fastidious bacteria. Difficulties in cultivation and identification are probably the reason why bacteremia caused by Eggerthella is rarely reported. Half of the cases of Eggerthella bacteremia are induced by the two novel species: E. sinensis and P. hongkongensis [7]. Stinear et al. described an isolate (AF304434) from human feces resembling E. lenta (98% identity) that carries an enterococcal vanB resistance locus probably received via lateral gene transfer or as a result of genetic mutations [9]. Clavel et al. investigated the occurrence and activity of dietary lignans activating bacterial communities in human feces and identified an E. lenta strain (AY937380) with 98.2% sequence similarity to strain VPI 0255T [10]. Lignans are a class of phytoestrogen which can be metabolized to the biologically active enterolignans, enterodiol and enterolactone. The human intestinal microbiota is essential for the conversation of the dietary lignans e.g. secoisolariciresinol diglucoside via secoisolariciresinol (SECO) to the enterolignans. Clavel and co-workers also reported that the dehydroxylation of SECO is catalyzed by Eggerthella lenta [11]. Based on 16S rRNA gene sequence analyses another five uncultured clones with 99% identity to E. lenta were reported at the NCBI BLAST server (status June 2009). These clones were derived from the analyses of feces samples from humans. e.g. associated with obesity [12,13], but also from marine metagenomes [14]
Phylogenetic tree of E. lenta strain VPI 0255T and all type strains of the genus Eggerthella as well as the type strains from all other genera of the family Coriobacteriaceae inferred from 1,373 aligned characters [15,16] of the 16S rRNA gene under the maximum likelihood criterion [17]. The branches are scaled in terms of the expected number of substitutions per site. Numbers above branches are support values from 1,000 bootstrap replicates if larger than 60%. Lineages with type strain genome sequencing projects registered in GOLD [18] are shown in blue, published genomes in bold, including two of which are reported in this issue of SIGS [19,20]
Scanning electron micrograph of E. lenta VPI 0255T (Manfred Rohde, Helmholtz Centre for Infection Biology, Braunschweig)
Classification and general features of B. cavernae HKI 0122T in accordance with the MIGS recommendations [21]
MIGS ID | Property | Term | Evidence code |
---|---|---|---|
Classification | Domain Bacteria | TAS [22] | |
Phylum Actinobacteria | TAS [23] | ||
Class Actinobacteria | TAS [24] | ||
Order Coriobacteriales | TAS [24] | ||
Suborder “Coriobacterineae” | TAS [25] | ||
Family Coriobacteriaceae | TAS [24] | ||
Genus Eggerthella | TAS [6] | ||
Species Eggerthella lenta | TAS [6] | ||
Type strain VPI 0255 | |||
Gram stain | positive | ||
Cell shape | rods, single or arranged in pairs and chains | ||
Motility | non-motile | ||
Sporulation | non-sporulating | ||
Temperature range | mesophile | TAS [4] | |
Optimum temperature | 37°C | TAS [4] | |
Salinity | 6.5% NaCl, poor to moderate growth | TAS [4] | |
MIGS-22 | Oxygen requirement | anaerobic | |
Carbon source | arginine | ||
Energy source | arginine | TAS [26] | |
MIGS-6 | Habitat | blood, human intestinal microflora | |
MIGS-15 | Biotic relationship | free living | NAS |
MIGS-14 | Pathogenicity | bacteremia | TAS [27] |
Biosafety level | 2 | TAS [28] | |
Isolation | rectal tumor | ||
MIGS-4 | Geographic location | not reported | |
MIGS-5 | Sample collection time | 1938 | TAS [1] |
MIGS-4.1 | Latitude-Longitude | not reported | |
MIGS-4.2 | |||
MIGS-4.3 | Depth | not reported | |
MIGS-4.4 | Altitude | not reported |
Chemotaxonomy
The cell wall of E. lenta strain VPI 0255T contains A1γ-type peptidoglycan glutamic acid occurred in D-form and diaminopimelic acid in meso configuration. Mycolic acids and teichonic acids were not reported. Strain VPI 0255T contains menaquinone MK-6 as the major respiratory lipoquinone (63.7%) and a lower amount of the methylmenaquinone MMK-6 (36.3%) [8,29,31]. As the predominant fatty acids the unbranched saturated 16:0 DMA (29.4%) and the monounsaturated fatty acid 18:1w9c (22.0%) were identified [5,6]. Polar lipids consist of two phospholipids, phosphatidylglycerol and diphosphatidylglycerol, and four glycolipids GL1–GL4 [8].
Genome sequencing and annotation
Genome project history
Genome sequencing project information
MIGS ID | Property | Term |
---|---|---|
MIGS-31 | Finishing quality | Finished |
MIGS-28 | Libraries used | Three genomic libraries: two Sanger libraries - 8 kb pMCL200 and fosmid pcc1Fos - and one 454 pyrosequence standard library |
MIGS-29 | Sequencing platforms | ABI3730, 454 GS FLX |
MIGS-31.2 | Sequencing coverage | 10.2× Sanger; 25.3× pyrosequence |
MIGS-30 | Assemblers | Newbler version 1.1.02.15, phrap |
MIGS-32 | Gene calling method | Prodigal, GenePRIMP |
Genbank ID | CP001726 | |
Genbank Date of Release | September 9, 2009 | |
GOLD ID | Gc01054 | |
NCBI project ID | 21093 | |
Database: IMG-GEBA | 2501533210 | |
MIGS-13 | Source material identifier | DSM 2243 |
Project relevance | Tree of Life, GEBA |
Growth conditions and DNA isolation
E. lenta strain VPI 0255T, DSM 2243, was grown anaerobically in DSMZ medium 209 (Eubacterium lentum Medium [32]) at 37°C. DNA was isolated from 1–1.5 g of cell paste using Qiagen Genomic 500 DNA Kit (Qiagen, Hilden, Germany) following the manufacturer’s protocol without modifications.
Genome sequencing and assembly
The genome was sequenced using a combination of Sanger and 454 sequencing platforms. All general aspects of library construction and sequencing can be found at the JGI website. 454 Pyrosequencing reads were assembled using the Newbler assembler version 1.1.02.15 (Roche). Large Newbler contigs were broken into 4,901 overlapping fragments of 1,000 bp and entered into the assembly as pseudo-reads. The sequences were assigned quality scores based on Newbler consensus q-scores with modifications to account for overlap redundancy and to adjust inflated q-scores. A hybrid 454/Sanger assembly was made using the parallel phrap assembler (High Performance Software, LLC). Possible mis-assemblies were corrected with Dupfinisher or transposon bombing of bridging clones [33]. Gaps between contigs were closed by editing in Consed, custom primer walk or PCR amplification. A total of 358 Sanger finishing reads were produced to close gaps, to resolve repetitive regions, and to raise the quality of the finished sequence. The final assembly consists of 39,464 Sanger and 471,609 pyrosequence (454) reads. Together all sequence types provided 35.5x coverage of the genome. The error rate of the completed genome sequence is less than 1 in 100,000.
Genome annotation
Genes were identified using Prodigal [34] as part of the Oak Ridge National Laboratory genome annotation pipeline, followed by a round of manual curation using the JGI GenePRIMP pipeline [35]. The predicted CDSs were translated and used to search the National Center for Biotechnology Information (NCBI) nonredundant database, UniProt, TIGRFam, 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 [36].
Genome properties
Graphical circular map of the genome. From outside to the center: Genes on forward strand (color by COG categories), Genes on reverse strand (color by COG categories), RNA genes (tRNAs green, rRNAs red, other RNAs black), GC content, GC skew.
Genome Statistics
Attribute | Value | % of Total |
---|---|---|
Genome size (bp) | 3,632,260 | 100.00% |
DNA Coding region (bp) | 3,211,405 | 88.41% |
DNA G+C content (bp) | 2,322,078 | 64.20% |
Number of replicons | 1 | |
Extrachromosomal elements | 0 | |
Total genes | 3,181 | 100.00% |
RNA genes | 58 | 1.67% |
rRNA operons | 3 | |
Protein-coding genes | 3,123 | 98.18% |
Pseudo genes | 53 | 1.67% |
Genes with function prediction | 2,255 | 70.89% |
Genes in paralog clusters | 629 | 19.77% |
Genes assigned to COGs | 2285 | 71.83% |
Genes assigned Pfam domains | 2316 | 72.81% |
Genes with signal peptides | 781 | 24.55% |
Genes with transmembrane helices | 990 | 31.12% |
CRISPR repeats | 1 |
Number of genes associated with the general COG functional categories
Code | Value | %age | Description |
---|---|---|---|
J | 142 | 4.5 | Translation, ribosomal structure and biogenesis |
A | 0 | 0.0 | RNA processing and modification |
K | 310 | 9.9 | Transcription |
L | 130 | 4.2 | Replication, recombination and repair |
B | 0 | 0.0 | Chromatin structure and dynamics |
D | 25 | 0.8 | Cell cycle control, mitosis and meiosis |
Y | 0 | 0.0 | Nuclear structure |
V | 80 | 2.6 | Defense mechanisms |
T | 201 | 6.4 | Signal transduction mechanisms |
M | 129 | 4.1 | Cell wall/membrane biogenesis |
N | 13 | 0.4 | Cell motility |
Z | 0 | 0.0 | Cytoskeleton |
W | 0 | 0.0 | Extracellular structures |
U | 51 | 1.6 | Intracellular trafficking and secretion |
O | 81 | 2.6 | Posttranslational modification, protein turnover, chaperones |
C | 293 | 9.4 | Energy production and conversion |
G | 79 | 2.5 | Carbohydrate transport and metabolism |
E | 180 | 5.8 | Amino acid transport and metabolism |
F | 60 | 1.9 | Nucleotide transport and metabolism |
H | 89 | 2.8 | Coenzyme transport and metabolism |
I | 69 | 2.2 | Lipid transport and metabolism |
P | 132 | 4.2 | Inorganic ion transport and metabolism |
Q | 32 | 1.0 | Secondary metabolites biosynthesis, transport and catabolism |
R | 262 | 8.4 | General function prediction only |
S | 195 | 6.2 | Function unknown |
- | 838 | 26.8 | Not in COGs |
Declarations
Acknowledgements
We would like to gratefully acknowledge the help of Gabriele Gehrich-Schröter for growing E. lenta cultures and Susanne Schneider for DNA extraction and quality analysis (both at DSMZ). This work was performed under the auspices of the US Department of Energy’s Office of Science, Biological and Environmental Research Program, and by the University of California, Lawrence Berkeley National Laboratory under contract No. DE-AC02-05CH11231, Lawrence Livermore National Laboratory under Contract No. DE-AC52-07NA27344, and Los Alamos National Laboratory under contract No. DE-AC02-06NA25396, as well as German Research Foundation (DFG) INST 599/1-1.
Authors’ Affiliations
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