Dickeya solani
1. Classification
a. Higher order taxa
Domain: Bacteria; Phylum: Proteobacteria; Class: Gammaproteobacteria; Order: Enterobacterales; Family: Pectobacteriaceae; Species: Dickeya solani
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NCBI: [1] |
2. Description and significance
Dickeya solani (D. solani), previously classified as Erwinia chrysanthemi, is a bacterial species that was determined as a novel plant pathogen in 2004 and has gained attention as it has spread through Europe in the last two decades via seed tuber trade of potatoes [2,13]. D. solani primarily infects potato tubers and some ornamental plant species, leading to blackleg and soft rot in crops across Europe, causing significant economic losses [3]. Despite its low virulence, D. solani is able to infect potatoes under a wide variety of oxygen conditions, contributing to rapid transmission [4,5]. Due to its economic impact, particularly on potato crops, the mechanisms of D. solani’s spread are an area of active research.
3. Genome structure
Within D. solani’s circular genome there are 4,922,460 base pairs, of which 56.3% are guanine-cytosine pairings, 4,536 sequences code for genes, 75 sequences code for tRNAs, and 22 sequences code for rRNAs [6]. Genetically, D. solani is most similar to D. dadantii strain 3937 [6]. D. solani produces exopolygalacturonate lyase and galacturan 1,4-alpha-galacturonidase which enable D. solani to catabolize pectic substrates, a crucial component of soft rot disease [4,7]. Similar to D. dadantii, D. solani genome has four genes producing Cyt-like proteins toxic to pea aphids, six secretion systems identified with soft rot bacteria, genes for blue pigment production, and a quorum sensing system. D. solani contains Hcp and VgrG copies in the T6SS cluster which is conserved in other soft rot causing bacteria (4). D. solani encodes polyketide synthases (PKS), non-ribosomal peptide synthases (NRPS), and amino acid adenylation domain proteins implicated in D. solani’s virulent and competitive success relative to other Dickeya strains [4]. Presence of ATP-binding cassette transporter genes near the NRPS/PKS encoding regions suggests NRPS and PKS may be secreted. D. solani contains a diverse assortment of pectate lyases including pelB, pelC, pelD, pelE, and pelL and proteases including prtA, prtB and prtC. The variety of pectate lyase genes and protease genes allow D. solani to rapidly and efficiently degrade host cell tissues, contributing to high virulence. [9] A gene cluster encoding secondary metabolites is conserved from the soil bacterium Serratia odorifera [4]. D. solani appears to have acquired many genomic islands via horizontal gene transfer, and it is postulated these regions of the genome predominantly contribute to D. solani evolution. D. solani possesses antifungal, anti-oomycete, and bacteriophage invasion resistance genes which give D. solani competitive advantage [4].
4. Cell structure
D. solani is a Gram-negative, rod-shaped (bacillus) bacterium with multiple flagella. D. solani forms flat, circular colonies with undulate edges and raised margins [5]. The flagella aid in motility, allowing the bacterium to swim and swarm [7].
5. Metabolic processes
D. solani is a facultative anaerobe, capable of conducting both aerobic respiration and fermentation, depending on the amount of oxygen present. The percentage of oxygen-dependent genes in D. solani, including virulence genes, is much lower than those of other microorganisms, including other Dickeya species [5]. This feature allows D. solani to infect potatoes, its primary host, under a wide range of oxygen conditions [5]. After initial contact with a potential host, there is only a small change in transcription of plant-tissue specific virulence genes within D. solani, meaning that global reprogramming of D. solani’s metabolism is not required for the successful infection of a plant host [8]. The slow onset of this gene expression allows D. solani to colonize the host and grow into a larger bacterial population before beginning the infection process [8]. D. solani can often be found inhabiting the tubers of a potato plant, while D. Dianthicola, a related bacterium, can be found residing in the stems of the same plant [3]. Genome sequence analysis of D. solani and comparison to the genome of D. dianthicola revealed that each species had a few hundred genes to it, including metabolism-related genes. The metabolic differences between the two species include differences in carbon and nitrogen source utilization, allowing D. solani and D. dianthicola to exploit distinctive niches in the same habitat, contributing to their coexistence on the same host [9].
6. Ecology
D. solani is a plant pathogen that most commonly infects the tubers on potatoes, but can often be found on other ornamental plants [3]. Since its first observation in 2004, D. solani has been rapidly spreading throughout Europe and damaging crops, leading to significant economic losses. The pathogenic success of D. solani stems from its ability to maximize its metabolic activity in temperate climates. The recent rise in temperatures and precipitation rates in Europe have contributed to an increase in its population levels that is expected to continue [2]. D. solani is able to coexist with other bacterial pathogens in the same host plant, allowing it to colonize previously infected plants. It is more common for D. solani to inhabit the tubers, while related competitor D. dianthicola may reside in the stems [3].
7. Pathology
D. solani infection is a common cause of blackleg and soft-rot in potato stems and tubers, resulting in widespread crop loss in Europe [3]. The aggressive infection of D. solani is a result of its genetic diversity and mechanism of infection. D. solani interaction with host tissues induces the expression of a complex network of virulence genes, including pectin lyase genes, integral membrane proteins, and structural proteins, tailoring cellular metabolism and environmental interactions to increase infection efficiency [7]. D. solani has an increased capacity to instigate symptoms at a lower inoculum level than other Dickeya species, likely due to its assorted pectate lyase genes that encode for enzymes that more efficiently degrade plant cell walls [3,9]. The virulence of various strains of D. solani is affected by mutations in assorted genes, with strains that possess incomplete adhesion protein genes being more virulent than those that have complete cell adhesion protein genes [10]. Incomplete adhesion proteins cause increased mobility within a host and contribute to more aggressive infection and faster spread [10]. D. solani exploits alternative carbon sources not used by other pathogens, which facilitates coexistence with other organisms on the potato host [9]. D. solani has only 1% of its genes thermoregulated, allowing it to cause infection across a spectrum of environmental conditions [11]. However, optimal performance is observed at higher temperatures, where pectin lyase genes are upregulated and biofilm formation is stimulated [11].
8. Current Research
Current research on D. solani focuses on the characteristics that lead to its aggressiveness as a plant pathogen. Much of the recent literature on this bacterium focuses on its pathology, due to its high virulence and ability to rapidly spread; these characteristics allow D. solani to cause great economic losses in agriculture [12]. Research has shown that D. solani has the ability to infect hosts under a wider range of environmental conditions than comparable plant pathogens; only 1.46% of its genes are oxygen-dependent, making it more effective at infecting plants at different oxygen availabilities than other disease-causing species [5]. Much of the current research has also found that D. solani is able to infect potatoes under a larger range of temperatures and density load than other species. When comparing D. solani to other plant pathogenic bacteria in tubers, researchers found that D. solani was able to inoculate the tubers at densities and at a wider range of temperature of 21-27 ℃. [5]. Recent studies have investigated D. solani at the genomic level to understand the severity of its virulence. One recent study found that different D. solani strains had key variability in virulence features like production of proteases, cellulases, and motility, while the rest of its genome remained largely conserved [10]. When looking at the virulence of a strain with an intact adhesin gene, scientists found that its virulence was lower than strains where this gene had been disrupted. They concluded that D. solani’s aggressiveness as a pathogen is related to motility, rather than adherence to plant material [10]. Ultimately, D. solani is more virulent than other species, with greater variability among species strains that could factor into the aggressiveness of the bacterium [6]. In response to economic losses and the aggressiveness of D. solani in causing soft rot, research has also expanded into diagnostic methods and prevention of D. solani infection. One study looked at the diagnostic ability of serological testing on potato crops suspected of infection. Serological tests were found to lack the specificity to screen potato crops for D. solani effectively, with only 68% of isolates being identified by the antibodies [13]. Instead, new immunoassay technologies with increased sensitivity capabilities for D. solani are an active area of research and implementation [13]. Another study looked into 46 different bacteriophages as potential treatments to prevent D. solani infection. Researchers found 6 T7-like bacteriophages that, when combined in a viral cocktail and treated in vivo in the potatoes, significantly disease progression in the potatoes [14].
References
1. “Taxonomy Browser (Dickeya Solani).” National Center for Biotechnology Information, U.S. National Library of Medicine, https://www.ncbi.nlm.nih.gov/Taxonomy/Browser/wwwtax.cgi?mode=Info&id=1089444
2. Dees, M. W., Lebecka, R., Perminow, J. I. S., Czajkowski, R., Grupa, A., Motyka, A., Zoledowska, S., Śliwka, J., Lojkowska, E., & Brurberg, M. B. (2017). Characterization of Dickeya and Pectobacterium strains obtained from diseased potato plants in different climatic conditions of Norway and Poland. European Journal of Plant Pathology / European Foundation for Plant Pathology, 148(4), 839–851.
3. Blin, P., Robic, K., Khayi, S., Cigna, J., Munier, E., Dewaegeneire, P., Laurent, A., Jaszczyszyn, Y., Hong, K., Chan, K., Beury, A., Reverchon, S., Giraud, T., Hélias, V., & Faure, D. (2021). Pattern and causes of the establishment of the invasive bacterial potato pathogen Dickeya solani and of the maintenance of the resident pathogen D. dianthicola. Molecular Ecology, 30(2), 608–624. https://doi.org/10.1111/mec.15751
4. Garlant, L., Koskinen, P., Rouhiainen, L., Laine, P., Paulin, L., Auvinen, P., Holm, L., & Pirhonen, M. (2013). Genome Sequence of Dickeya solani, a New soft Rot Pathogen of Potato, Suggests its Emergence May Be Related to a Novel Combination of Non-Ribosomal Peptide/Polyketide Synthetase Clusters. Diversity (Basel), 5(4), 824–842. https://doi.org/10.3390/d504082
5. Lisicka, W., Fikowicz-Krosko, J., Jafra, S., Narajczyk, M., Czaplewska, P., & Czajkowski, R. (2018). Oxygen Availability Influences Expression of Dickeya solani Genes Associated With Virulence in Potato ( Solanum tuberosum L.) and Chicory ( Cichorium intybus L.). Frontiers in Plant Science, 9, 374–374. https://doi.org/10.3389/fpls.2018.00374] [6] [Khayi, S., Blin, P., Chong, T. M., Robic, K., Chan, K.-G., & Faure, D. (2018). Complete Genome Sequences of the Plant Pathogens Dickeya solani RNS 08.23.3.1.A and Dickeya dianthicola RNS04.9. Genome Announcements (Washington, DC), 6(4), UNSP e01447–17. https://doi.org/10.1128/genomeA.01447-17
6. Khayi, S., Blin, P., Chong, T. M., Robic, K., Chan, K.-G., & Faure, D. (2018). Complete Genome Sequences of the Plant Pathogens Dickeya solani RNS 08.23.3.1.A and Dickeya dianthicola RNS04.9. Genome Announcements (Washington, DC), 6(4), UNSP e01447–17. https://doi.org/10.1128/genomeA.01447-17
7. Potrykus, M., Hugouvieux‐Cotte‐Pattat, N., & Lojkowska, E. (2018). Interplay of classic Exp and specific Vfm quorum sensing systems on the phenotypic features of Dickeya solani strains exhibiting different virulence levels. Molecular Plant Pathology 19(5), 1238–1251. https://doi.org/10.1111/mpp.12614
8. Raoul des Essarts, Y., Pédron, J., Blin, P., Van Dijk, E., Faure, D., & Van Gijsegem, F. (2019). Common and distinctive adaptive traits expressed in Dickeya dianthicola and Dickeya solani pathogens when exploiting potato plant host. Environmental Microbiology, 21(3), 1004–1018. https://doi.org/10.1111/1462-2920.14519
9. Czajkowski, R., Fikowicz-Krosko, J., Maciag, T., Rabalski, L., Czaplewska, P., Jafra, S., Richert, M., Krychowiak-Maśnicka, M., & Hugouvieux-Cotte-Pattat, N. 2020. Genome-Wide Identification of Dickeya solani Transcriptional Units Up-Regulated in Response to Plant Tissues From a Crop-Host Solanum tuberosum and a Weed-Host Solanum dulcamara. In Frontiers in Plant Science Vol. 11. https://doi.org/10.3389/fpls.2020.580330
10. Golanowska, M., Potrykus, M., Motyka-Pomagruk, A., Kabza, M., Bacci, G., Galardini, M., Bazzicalupo, M., Makalowska, I., Smalla, K., Mengoni, A., Hugouvieux-Cotte-Pattat, N., & Lojkowska, E. (2018). Comparison of Highly and Weakly Virulent Dickeya solani Strains, With a View on the Pangenome and Panregulon of This Species. Frontiers in microbiology, 9, 1940. https://doi.org/10.3389/fmicb.2018.01940
11. Czajkowski, R., Kaczyńska, N., Jafra, S., Narajczyk, M., & Lojkowska, E. (2017). Temperature‐responsive genetic loci in pectinolytic plant pathogenic Dickeya solani. Plant Pathology, 66(4), 584–594. https://doi.org/10.1111/ppa.12618]
12. [Motyka-Pomagruk, A., Zoledowska, S., Misztak, A.E. et al. Comparative genomics and pangenome-oriented studies reveal high homogeneity of the agronomically relevant enterobacterial plant pathogen Dickeya solani. BMC Genomics 21, 449 (2020). https://doi.org/10.1186/s12864-020-06863-w
13. Toth, I. K., van der Wolf, J. M., Saddler, G., Lojkowska, E., Hélias, V., Pirhonen, M., Tsror Lahkim, L., & Elphinstone, J. G. (2011). Dickeya species: an emerging problem for potato production in Europe. Plant Pathology, 60(3), 385–399.
14. Carstens AB, Djurhuus AM, Kot W, Jacobs-Sera D, Hatfull GF, Hansen LH. Unlocking the Potential of 46 New Bacteriophages for Biocontrol of Dickeya Solani. Viruses. 2018; 10(11):621. https://doi.org/10.3390/v10110621
Edited by [M.C, N.K, A.L, R.L. and B.S], student of Jennifer Bhatnagar for BI 311 General Microbiology, 2021, Boston University.
