Genomic and metabolic comparison with Dickeya dadantii 3937 reveals the emerging Dickeya solani potato pathogen to display distinctive metabolic activities and T5SS/T6SS-related toxin repertoire
- Jacques Pédron†1, 2,
- Samuel Mondy†3,
- Yannick Raoul des Essarts3, 4,
- Frédérique Van Gijsegem†1, 2Email author and
- Denis Faure†3Email author
© Pédron et al.; licensee BioMed Central Ltd. 2014
Received: 20 December 2013
Accepted: 4 April 2014
Published: 15 April 2014
The pectinolytic enterobacteria of the Pectobacterium and Dickeya genera are causative agents of maceration-associated diseases affecting a wide variety of crops and ornamentals. For the past decade, the emergence of a novel species D. solani was observed in potato fields in Europe and the Mediterranean basin. The purpose of this study is to search by comparative genomics the genetic traits that could be distinctive to other Dickeya species and be involved in D. solani adaptation to the potato plant host.
D. solani 3337 exhibits a 4.9 Mb circular genome that is characterized by a low content in mobile elements with the identification of only two full length insertion sequences. A genomic comparison with the deeply-annotated model D. dadantii 3937 strain was performed. While a large majority of Dickeya virulence genes are shared by both strains, a few hundreds genes of D. solani 3337, mostly regrouped in 25 genomic regions, are distinctive to D. dadantii 3937. These genomic regions are present in the other available draft genomes of D. solani strains and interestingly some of them were not found in the sequenced genomes of the other Dickeya species. These genomic regions regroup metabolic genes and are often accompanied by genes involved in transport systems. A metabolic analysis correlated some metabolic genes with distinctive functional traits of both D. solani 3337 and D. dadantii 3937. Three identified D. solani genomic regions also regroup NRPS/PKS encoding genes. In addition, D. solani encodes a distinctive arsenal of T5SS and T6SS-related toxin-antitoxin systems. These genes may contribute to bacteria-bacteria interactions and to the fitness of D. solani to the plant environment.
This study highlights the genomic specific traits of the emerging pathogen D. solani and will provide the basis for studying those that are involved in the successful adaptation of this emerging pathogen to the potato plant host.
KeywordsPKS NRPS CDI Rhs Dickeya dadantii Dickeya solani Plant pathogen interactions
The pectinolytic enterobacteria of the Pectobacterium and Dickeya genera are causative agents of maceration-associated diseases affecting a wide variety of crops and ornamentals . During the past century, the species Pectobacterium atrosepticum and Pectobacterium carotovorum dominated the pathogenic populations in samples collected from black-leg and soft-rot symptoms of potato plants and tubers under temperate climates. Since the 1970’s, Dickeya strains, mostly D. dianthicola, were also detected in potato fields in Europe. More recently, in the 2000’s, a novel species called Dickeya solani[2, 3], emerged among the pectinolytic enterobacteria recovered from potato symptoms in several countries. The emergence and challenges of the Dickeya species in potato production have been deeply discussed by Toth et al..
Genetic markers and biochemical tests allowed to clearly distinguishing these novel pathogenic strains from the established Dickeya species, including D. dianthicola, D. dadantii, D. zeae, D. chrysanthemi, D. paradisiaca and D. dieffenbachia[4–7]. Aside the current effort on the taxonomic description of D. solani, questions arose about the origin, adaptation, ecology and, in an applied issue, the control of this emerging plant pathogen on potato cultures. Even if only a few genetic markers were analysed in several D. solani isolates from different countries, their high similarities suggested a clonal origin of D. solani populations affecting the potato plant host [4–6, 8]. Remarkably, under greenhouse conditions at a high temperature (28°C), when the two bacterial species D. solani and D. dianthicola are coinoculated, D. solani isolates outcompete those of the other Dickeya species, revealing a high efficiency for colonizing potato roots and stems [9, 10]. The genes and functions involved in these traits are still unknown.
For several decades, D. dadantii strain 3937 was widely used as a model system for research on the molecular biology and pathogenicity of pectinolytic enterobacteria. The D. dadantii 3937 strain remains, until today, the Dickeya isolate in which virulence factors and host-interacting functions are the most studied [1, 11]. Its annotated genome is available , hence is used for fruitful comparison with the released draft and completed genomes belonging to Dickeya and other plant pathogenic genera.
The D. solani strain 3337 (also named RNS 08.23.3.1A) has been isolated from potato in France in 2008  and its aggressiveness on potato plants has been confirmed . In this paper, we reported a genomic and metabolic comparison of the D. solani strain 3337 and D. dadantii strain 3937.
Bacterial strains, culture conditions and metabolic assays
D. solani 3337 (=RNS 08.23.3.1A)  and D. dadantii 3937  were routinely cultured in TY medium (tryptone 5 g/L, yeast extract 3 g/L, agar 1.5%) at 30°C. The metabolic abilities of D. solani 3337 and D. dadantii 3937 were investigated using the carbon source microplates PM1 and PM2A and the nitrogen source microplate PM3B (Biolog, France). Sodium pyruvate was used as a carbon source for testing the nitrogen sources. The experiment was duplicated. According manufacturer’s instructions, OD590nm (Tecan spectrophotometer) was read at the inoculation time (ti) and after a 48 h incubation (tf); variation ΔOD = tf-ti was calculated for each of the tested nitrogen and carbon sources. A ΔODvalue < 0.25 indicated that bacteria did not metabolize the nutrients; 0.25 ≤ ΔOD < 1 revealed a weak metabolic activity and ΔOD ≥ 1 referred to a very efficient metabolic activity.
Genome sequencing of D. solani3337
Two DNA-libraries were constructed by Eurofins Genomics (France) using the TruSeq(TM) SBS v3 sequencing kit: a shotgun (SG) paired-end library with a fragment size between 150 to 500 bp and a long jumping distance (LJD) mate-pair library with an insert-size average of 5.7 kbp. The two libraries were sequenced using 2×100 bp paired-end read module of IlluminaHiSeq 2000 by Eurofins Genomics (France). Reads were trimmed on quality and length. Sequence assembly was carried out using the CLC Genomics Workbench v5 (CLC bio, Aarhus, Denmark) with a read length of 0.5 and a similarity of 0.8. Forty-two contigs were obtained with a length ranging from 2.1 to 483 kbp. The scaffolding was processed using SSPACE basic v2.0 .
In silico finishing
The in silico finishing of some gaps was carried out by mapping (read length of 0.9 and similarity of 0.95) the mate-pair reads on each of the 5 kbp contig-ends since the de novo assembly software faced difficulty during assembly in repeated regions. We used the borders of the gap regions as anchor and retrieved the reads in both orientations in order to perform a new de novo assembly on these regions. The mapped reads were collected and both orientation R1 and R2 were retrieved. The reads were used for de novo local assembling (read length of 0.5 and similarity of 0.8). Additional gaps were closed by Sanger sequencing of PCR amplicons.
Annotation of the D. solani 3337 genome and comparison with D. dadantii3937
The functional annotation of predicted genes of D. solani 3337 was achieved using the RAST server  with the Glimmer 3 gene caller . As the genome annotation of D. dadantii 3937 was performed in 2004 with the version 2 of Glimmer, this genome was also re-annotated with the same RAST server in order to compare genes predicted with the same algorithm. In D. solani 3337, the remaining gaps affect 15 genes that were not considered in the subsequent analysis.
Synteny analysis was performed by using the MAUVE software . Average nucleotide identity (ANI blast) was computed using the Jspecies package . Genome to genome comparison was performed by bi-directional protein-protein BLAST sequence comparison of translated open reading frames (ORFs) with a 10-5 e-value threshold. Genes of both species were considered as strain-specific if identity of the encoded protein was lower than 80% of full-length amino acids sequence. For comparison, average identity level of the proteins encoded by conserved genes, calculated as the mean of all identity percentages, is 96%. If local alignments were too short as regard to the length of similar sequences, we performed a nucleotide BLAST on full-length DNA sequences with similar thresholds (10-5 e-value, 80% identity of full length sequence). This allowed us to eliminate false strain-specific genes. In some cases, identities were lower than 80% due to differences in predicted ORF length. Such differences in length of similar sequences was the consequence of wrong prediction of start codons or when two predicted ORFs in one species matched with one ORF in the other one. All similar but strain-specific sequences that differ by more than 10% in length were manually analysed to detect putative wrong start codon prediction or occurrence of stop codons that could explain the interruption of one ORF.
Comparison of the D. solani 3337 genome with other Dickeyadraft genomes
The D. dadantii 3937 genome resulted from Sanger genomics. The production of reads mimicking Illumina reads of the D. dadantii 3937 genome was performed using Metasim . A set of 2,000,000 reads derived from the D. dadantii 3937 genome with an average size of 100 nucleotides were produced and used for mapping approaches as described below.
The Illumina reads of D. solani 3337 and simulated reads from D. dadantii 3937 were mapped using the draft genomes of the four D. solani strains IPO2, MK10, MK16 and LMG25865  and the D. dadantii genome and draft genomes of the strains D. dadantii 3937, NCPPB3537 and NCPPB898. Two mappings were performed at high (0.95 of identity on 0.9 of read length) and mild stringency threshold (0.8 of identity on 0.5 of read length). Using such in silico DNA-DNA hybridizations, a high proportion of mapped reads will indicate a strong identity between genome sequences. Then, the mapping files constructed using high stringency parameters were processed for SNP analysis.
In addition, the presence of genomic clusters in the D. solani and D. dadantii species was searched with a nucleotide BLAST analysis using the sequences of the specific clusters as queries against a database constituted by the D. solani and D. dadantii genomes (e-value threshold = 10-50).
The search for the presence of D. solani-specific and D. dadantii 3937 specific-genes in other Dickeya species was performed by bi-directional protein-protein BLAST sequence comparison (e-value threshold 10-5) with the D. paradisiaca 703 strain (formerly named D. dadantii 703, GenBank accession number CP001654), the D. zeae 586 strain (formerly named D. dadantii GCF_000025065.1) and the D. chrysanthemi 1591 strain (formerly named D. zeae CP001655) as reclassified by Pritchard et al..
Genome accession numbers
The D. solani 3337 genome sequence has been deposited at DDBJ/EMBL/GenBank under the accession n°AMYI00000000. Sequence data used in this article can be found in the GenBank/EMBL data libraries under the following accession numbers: D. solani strains IPO2222 (CM001859), MK10 (CM001859), MK16 (CM001842), LMG25865 (CM001860), and D. dadantii strains 3937 (CP002038), NCPPB3537 (CM001982), NCPPB898 (CM001976).
Results and discussion
General features of the D. solani3337 genome
The published sequence of D. solani 3337 is composed of eleven contigs (from 4.5 kbp to 1.11 Mbp) grouped in a single scaffold with 1,075 coverage in average. The in silico approach permits to close 32 gaps and to map the 7 rrs regions. Hence, the D. solani 3337 genome consists of a unique 4.9 Mb circular chromosome with a 56.1% GC content and contains no plasmid. These features are in accordance with data of the Dickeya genome and draft genomes that are available in public databases [7, 21]. Using the RAST server with the Glimmer 3 caller, gene prediction and automatic annotation predicted 4530 protein-coding sequences, 72 tRNA genes and 7 rRNA regions.
Comparative genomics between D. solani 3337 and D. dadantii3937: an overview
To go further into the D. solani 3337 genome analysis, we took advantage of the manually annotated genome of the model D. dadantii 3937 strain . To allow a precise comparison, a novel gene prediction with Glimmer 3 was achieved on the D. dadantii 3937 genome leading to the prediction of 4740 protein-coding sequences and 97 RNA genes. Noticeably, 526 new genes were identified with the Glimmer 3 software as compared to the previous gene prediction but only 27 have a known or predicted function. All the other CDS are annotated as hypothetical and 85% (448) are smaller than 60 amino acids.
Genes conserved in both strains were identified by performing bidirectional best hit analysis at the protein level and retaining only the genes that encode proteins exhibiting at least 80% identity on full length amino acid sequence. Manual check of remaining genes allowed the identification of additional conserved genes excluded from the previous test because of prediction or alignment ambiguities (see Methods for details). About 3700 genes have homologues in both strains. This corresponds to 78-82% of the total protein-coding sequences. This is in fact comparable to the core genome size of certain bacterial species such as Porphyromonas gingivalis or Streptococcus pneumoniae[22, 23] and is considerably larger than that of other enterobacterial species such as E. coli. The closeness of both strains is supported by the 94% average nucleotide identity (ANI) value, an analysis that has emerged as one of the predominant genomics alternatives to DNA-DNA hybridization and stated that two strains belong to the same species if their pairwise ANI values are higher than 96% . It is also in accordance with previous taxonomic studies that place D. solani and D. dadantii species close to each other [21, 6].
Most virulence genes are conserved between D. solani 3337 and D. dadantii3937
The main virulence factors
The main virulence determinants in soft rot enterobacteria are plant cell wall degrading enzymes (PCWDEs) that cause extensive tissue maceration during the latter stages of infection [1, 11]. The D. dadantii genome contains 23 pectinases encoding genes including pectate and pectin lyases, polygalacturonases, pectin-methyl and acetyl esterases. All corresponding genes are present in D. solani except the pectin lyase encoding pnlH gene (see below) and the pehK gene (locus tag Dda3937_00206) encoding a predicted polygalacturonase that is present in all 4 Dickeya for which complete genomes are available, several Pectobacterium strains and several other enterobacteria. Both strains shared the same battery of cellulases and extracellular proteases as well as iron uptake systems, production of antioxydants like indigoidine and systems involved in defence against the plant oxidative burst or antimicrobial peptides [25–27, 1, 11]. Concerning protection to osmotic stress however, the ousA gene encoding the major osmoprotectant uptake system in D. dadantii 3937 is missing in D. solani. Interestingly, an ousA disruption in D. dadantii 3937 highly enhanced bacterial virulence on potato tubers and enhanced Pel production in vitro under micro-aerobiosis conditions. This might be correlated to the observation that the less NaCl-tolerant Dickeya strains are the more virulent in potato tubers .
Proteins secretion systems of type 1 to 6 and toxin/antitoxin systems
Production of plant hormones
Among genes that may be involved in plant-bacteria interactions, it should be noted that the D. dadantii iaaMH genes (Dda3937_01279 and 01280) allowing the production of an auxin plant hormone, do not have counterparts in D. solani. Accordingly, D. solani produces only minute amounts of indolic compounds related to auxins as compared to D. dadantii.
Virulence regulatory pathways
In D. dadantii, a complex regulatory network composed of several global regulators  out of whom the GacAS two-component systems, the PecS and MfbR members of the MarR family of regulators, or the recently discovered new quorum-sensing system Vfm, have been shown to control virulence gene expression in planta[35–38]. All these regulators are present in D. solani. Out of the 17 members of the MarR family present in D. dadantii 3937 however, 3 corresponding genes (Dda3937_01219, 01245 and 03163; MfhR, MfiR and MfeR) are missing in D. solani 3337. These regulators were shown to be dispensable for full virulence expression in D. dadantii but they might have a role in other parts of the bacterial life cycle since in different bacteria, regulators of this family are involved in the sensing of signalling molecules . By contrast, all D. dadantii regulators of the LacI family are present in D. solani. This family of regulators are very often related to global metabolism and some of them are involved in virulence in D. dadantii 3937 . In addition, D. solani possesses functional arcB and soxS genes, two genes involved respectively in the aerobiosis/anaerobiosis switch and in oxidative defence regulation that are either mutated (arcB) or absent (soxS) in D. dadantii 3937 .
Strain-specific genes in D. solani 3337 and D. dadantii3937: an overview
Overview of D. solani 3337 and D. dadantii 3937 specific encoding protein genes
D. solani 3337
D. dadantii 3937
Hypothetical proteins (<60 aa)
Proteins with undefined function
Proteins with predicted function
The D. solani 3337 genome is poor in mobile elements and phage-related genes and defective for CRISPR
Insertion sequences (IS) and transposable elements may promote genome plasticity and contribute to bacterial adaptability . While about 40% of the D. dadantii 3937 strain-specific genes of known or predicted function (147 genes) are related to mobile elements or phages functions, only 30 such genes were identified in D. solani. This is due in part to the presence of a Tn4371 ICE (Integrative Conjugative Element) family element in GR5 (Additional file 2: Table S3)  and a complete prophage with morphogenesis genes related to Haemophilus HP1 and HP2 genes in D. dadantii 3937 (see Figure 1, Additional file 2: Table S3). Unlike D. solani 3337, D. dadantii 3937 also harbors a region with CRISPR (Clustered Regularly Interspaced Short Palindromic Repeats) sequences and associated genes (GR10, Additional file 2: Table S3). CRISPR are thought to provide acquired resistance to viruses in prokaryotes, as recently demonstrated in Streptococcus thermophilus. Beside this, D. dadantii 3937 possesses two times more genes related to transposases (37 versus 15) than D. solani 3337. Accordingly, detection of IS elements using the ISBiotoul server (http://www-is.biotoul.fr) reveals the presence of only 2 full length IS (IS110 family: 3673879–3675 442; IS3/IS407 family: 2569337–2570527) in D. solani while 19 full length IS are present in D. dadantii 3937. Remarkably, the D. solani IS110-related sequence is inserted into a transposase gene in the GR16 region that contains in total 6 of the 15 D. solani transposase-related genes and a T6SS-related Hcp encoding gene (ID 3387). The other IS is surrounded by genes related to phage components in the GR11 region.
Genomic regions present in D. solani 3337 and absent in D. dadantii 3937
Presence of horizontal transfer signature
Presence in other Dickeya
Urea transport and metabolism
D. chrysanthemi 1591 (8 genes/13)
NRPS - PKS
D. zeae 586 (5 genes/9)
Transport - metabolism
Transport - metabolism
D. zeae 586 (4 genes/20)
Transport - metabolism
PKS - NRPS
D. paradisiaca 703 (whole cluster)
Transport - metabolism
D. paradisiaca 703 (whole cluster)
D. zeae 586 (13 genes/20)
Transport - metabolism
D. zeae 586 (9 genes/16)
PKS - NRPS
Transport - metabolism
Galactonate transport and metabolism
Distinctive metabolic properties between D. solani 3337 and D. dadantii 3937
Each module allows the addition of one unit of the synthesized polymer. The core module of PKS consists of an acyl carrier protein (ACP) domain for unit loading and a beta-ketosynthase (KS) domain for condensation. For PKS activity, an acyltransferase (AT) domain is also required. This AT activity may be provided either by an AT domain incorporated in each module or by discrete free-standing acyltransferase enzymes in the case of trans-AT PKSs. The core module of NRPS consists of an adenylation (A) domain for the selection of one amino acid, a peptidyl carrier protein (PCP) and a condensation domain (C) for catalysing peptide bond formation . Among the D. solani genomic regions, GR3 regroups 7 genes related to metabolism among which 3 genes encoding NRPS that regroup 4 synthetic modules, one trans-acetyltransferase and a trans-AT PKS of 4 modules. This gene cluster appears to be specific to some Dickeya since it is found only in D. zeae 586 in databases. GR9 regroups 14 metabolic genes among which 7 genes encoding trans-AT PKS modules and two trans-AT encoding genes. This gene cluster is present in D. paradisiaca 703 and in Serratia odorifera. GR19 is also a complex gene cluster regrouping a mix of 3 genes encoding NRPS modules and 4 PKS related genes. Beside 11 genes related to production of secondary metabolites, this cluster also encodes one regulatory protein and 2 proteins involved in transport systems. This gene cluster has counterparts in Serratia and partly in Xenorhabdus bovienii.
Differential metabolic abilities of D. dadantii 3937 and D. solani 3337
PM plates name
Compound source name
D. dadantii 3937
D. solani 3337
PM1 MicroPlate™ carbon sources
PM2A MicroPlate™ carbon sources
PM3B MicroPlate™ nitrogen sources
The 25 GRs of D. solani 3337 are also present in all available draft genomes of D. solani
Blast analysis revealed that all the 25 GRs of D. solani 3337 are present in the genomes of the D. solani strains IPO2222, MK10, MK16 and LMG25865. Similarly, MAUVE analysis shows a complete synteny between these D. solani genomes except that the big inversion between rrs operons found in D. solani 3337 strain as compared to D. dadantii 3937 is not present in other D. solani strains.
The high genome similarity among D. solani isolates is confirmed with SNP analysis. Only 200 to 300 SNPs were detected between the genome of D. solani 3337 and the other D. solani genomes (Figure 6C). In contrast, at least 80,000 SNPs were detected between the D. dadantii 3937 genome and the genome of the other tested D. dadantii strains (Figure 6D).
The genome comparison between the potato isolate D. solani 3337 and the model D. dadantii 3937 only highlights small differences in the arsenal of Dickeya virulence factors characterized so far. By contrast, the two strains diverge in their battery of T5SS/T6SS-related toxin-antitoxin systems and harbour distinctive metabolic capacities. In particular, D. solani possesses 3 gene clusters regrouping NRPS/PKS genes known to be involved in the biosynthesis of complex secondary metabolites that were shown in other systems to have antibiotic activities or even to be important in virulence against plants . Importantly, the D. solani-specific gene clusters are conserved in all draft genomes of D. solani that are available until today. These clusters are thus promising for deciphering the molecular mechanisms supporting the recent emergence and lifestyle of the D. solani species.
Non-ribosomal peptide synthase
This work is supported by CNRS (Gif-sur-Yvette), Comité Nord Plants de Pomme de Terre (CNPPT/SIPRE), Fédération Nationale des Producteurs de Plants de Pomme de Terre (FN3PT/RD3PT) and Association Nationale de la Recherche et de la Technologie (ANRT-CIFRE n°1282/2011). We thank Slimane Khayi (PhD University Paris Sud-University of Meknes) for calculating SNP number between D. solani 3337 and Ds0432-1, and David Bonnaffé (ICMMO, University Paris Sud) for providing galactonate and galactonate γ-lactone.
NOTE ADDED IN PROOF: during the submission process of the manuscript, the genome of the D. solani strain Ds0432-1  was released (GenBank AMWE00000000). It exhibits similar genomic characteristics as D. solani 3337. 87 SNPs were detected between the genome of D. solani strain 3337 and strain Ds0432-1.
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