Pectobacterium atrosepticum

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1. Classification

a. Higher order taxa

Bacteria; Proteobacteria; Gammaproteobacteria; Enterobacteriales; Enterobacteriacea; Pectobacterium (1).

Species: Pectobacterium atrosepticum (1).

2. Description and significance

Pectobacterium atrosepticum (P. atrosepticum) is a Gram-negative species of phytopathogenic bacteria that falls under the family of Enterobacteriacea (1). P. atrosepticum is rod-shaped, motile, and does not form spores (2). The bacteria is found in temperate regions (3), where it is responsible for causing blackleg in potatoes, an infection that leads to the soft rot, decay, and eventual death of the crop (4). P. atrosepticum is important to human society due to the harmful economical effects it has on the agricultural industry (4). Genetic factors contributing to pathogenicity and virulence in P. atrosepticum have yet to be described. Current research seeks to gain a deeper understanding of optimal growth conditions for P. atrosepticum, as well as pathogenic effects of the microbe on a variety of different plants (4).

3. Genome structure

P. atrosepticum consists of a singular circular chromosome with 5,064,019 base pairs (3). Plasmids consisting of 32,444 base pairs appear in 3-4 copies per P. atrosepticum cell (5). The microbe's genome has a 50.97% guanine-cytosine (GC) content (3). The genome contains 7 rRNA operons, 76 tRNA, and 25 noncoding RNAs (3). Additionally, P. atrosepticum contains 4,491 coding sequences (CDS), 393 of which are involved in the bacterium's pathogenicity (3). P. atrosepticum contains several horizontally acquired genomic islands, implying the occurrence of horizontal gene transfer (3). Furthermore, many of the CDS are located within the genomic islands, indicating that horizontal gene transfer contributes to the microbe's pathogenicity (3). P. atrosepticum is the only known Gram-negative bacteria to contain all six protein secretion systems within its genome, including Type I secretion system (T1SS), Type II secretion system (T2SS), Type III secretion system (T3SS), Type IV secretion system (T4SS), Type V secretion system (T5SS), and Type VI secretion system (T6SS). T1SS, T2SS, and T3SS are especially important in P. atrosepticum due to the production of plant cell-wall degrading enzymes such as pectinase and cellulase, which contribute to the bacterium’s ability to cause rotting in potatoes (3). Additionally, the genome of P. atrosepticum contain horizontally acquired islands with genes coding for antibiotic production, opine catabolism, and nitrogen fixation enzymes such as nitrogenase, which allow the bacteria to survive in different environments (3).

4. Cell structure

P. atrosepticum is a Gram-negative, rod-shaped, non-spore forming bacterium that is motile due to its ability to swarm on surfaces (2). The cell wall consists of an outer membrane, an inner cytoplasmic membrane, and a peptidoglycan layer in the periplasmic space. The bacteria are arranged either singly or in pairs (2). P. atrosepticum has the ability to produce extracellular pectinolytic enzymes during infection of plants (2). Infection is accomplished by P. atrosepticum’s production of bacterial emboli in the xylem vessels, cells found within the water conducting tissue of plants (6). Bacterial emboli are multicellular structures consisting of bacteria in a polysaccharide gel matrix (6).

5. Metabolic processes

P. atrosepticum can metabolize a diverse amount of compounds including starch, lactose, maltose, sucrose, fructose, nucleotide sugar, amino sugar, propanoate, fatty acids, and pyruvate (8). This species of Pectobacterium contains catalase activity and is capable of metabolizing carbohydrates through both fermentation and oxidation (9). P. atrosepticum is capable of producing polyphenol oxidase activity with the help of the enzyme laccase (10). Laccase makes it possible for the cell to perform oxidation of ferulic acid in the presence of copper. Polyphenol oxidase-catalyzed polymerization of o-quinones causes the black pigment that is seen in the blackleg disease found in potatoes (10).

6. Ecology

While other species in this genus can survive in a wide variety of environments, P. atrosepticum can only host themselves in potato plants found in temperate climates (11). The optimal temperature for infection is 27०C (12). When not actively causing disease in crops, the bacteria cycle through a series of phases where they grow in the soil, on the surface of the plant, and then lay dormant within plant tissues (13). Once P. atrosepticum makes its way inside, it occupies the intercellular spaces and vascular tissues of the pores and wounds (13). When environmental conditions (specifically temperature and water and oxygen supply) become favorable, the bacteria can begin to cause infection (13). While oxygen availability and temperature are important factors, the presence of free water is most important for P. atrosepticum development (13).

7. Pathology

P. atrocepticum results in blackleg disease in potatoes by producing degrading enzymes pectinase and cellulase that cause tissue maceration (13). Pathogenicity of this bacterium is most effective in a lower climate, specifically between 26°C and 30°C (14). Besides growing in an optimal temperature, the bacteria must be supplied the appropriate amount of oxygen. When there is a high availability of free water in the environment, oxygen sources within the potato crop become depleted. The lack of oxygen prevents the oxygen-dependent plant from initiating defense mechanisms that destroy the P. atrosepticum found in the plant tissue (13). The main disease-causing method is the production of pectinase and cellulase which are secreted in a series of bacterial secretion systems (Type I, II, and III). Cellulase works to break down the cell walls while pectinase makes use of pectin to generate tissue collapse, cell leakage, and cell damage (15). The exoenzymes also help release nutrients that allow the bacteria to grow. In certain cases P. atrosepticum is not the only bacteria present in the affected areas of potato crops (14). When the mother root-tuber of a potato rots and decays, the bacteria are released into the soil and can therefore be transmitted through rain or ground water to adulterate neighboring tubers (12).

8. Current Research

Current research is assessing the recent upward trend of blackleg and soft rot incidence in seed potato crops in regions of Europe, specifically Great Britain. The high incidence of these longstanding problems reached a peak in Great Britain in the 1960s and agriculture has seen a decrease in the prevalence of the plant diseases until suspicions of the bacteria re-entering the soil in recent years (18). When multiple bacteria are present in the soil and roots of crops, temperature modulates which of the present pathogens will override the other and affect the mother tuber (18). Testing for the confirmed P. atrosepticum within the soil in the potato farms of Great Britain allows for plans of adaptation of the agriculture treatment and maintenance going forward in the presence of climate change. With the trend of dryer summers in Europe, the crops are at risk for drastic temperature changes as well as fluctuations in soil moisture (18). When there is moisture and higher concentrations of rainwater, the bacteria can more readily colonize potato roots and enter the vascular system of progeny tubers. Inducing the anaerobic conditions on the surface of the mother tubers favors bacterial growth, resulting in blackleg disease, stem rot, and lead to plant death (18). Research regarding the soil moisture as well as optimal temperatures for growth of P. atrosepticum will help with plans for rainwater harvesting equipment, irrigation technology, and as a last resort, geographical relocation of crop cultivation. Most recently, the genes of P. atrosepticum have been tested in an attempt to identify the differences of the gene expression within planta as compared to in vitro conditions. Through studying the effects of plant pathogens on tobacco plants and observing the colonization of the roots, the enzymatic reactions of the bacteria will be observed. The analysis of the RNA sequencing of P. atrosepticum has been used to attempt to identify the asymptomatic stage of the bacteria’s colonization, transitioning from point of colonization to soft-rot associated symptoms of the tobacco plants (14). Two strategies of tobacco colonization were observed to recognize this symptomless spread of the bacteria: 1) the initial, symptomless stage and spread of P. atrosepticum through xylem vessels, known as the stealth strategy and 2) the manifestation of soft-rot symptoms, known as the brute force strategy (14). Research regarding the effects of P. atrosepticum on a variety of different plants will expand knowledge on the pathogenicity of this bacterium.

9. References

(1) Taxonomy Browser. Pectobacterium atrosepticum. NCBI. https://www.ncbi.nlm.nih.gov/Taxonomy/Browser/wwwtax.cgi?mode=Info&id=29471&lvl=3&lin=f&keep=1&srchmode=1&unlock.

(2) Buttimer, C., Hendrix, H., Lucid, A., Neve, H., Noben, J., Franz, C., . . . Coffey, A. (2018). Novel N4-like bacteriophages of pectobacterium atrosepticum. Pharmaceuticals (Basel, Switzerland), 11(2) doi:10.3390/ph11020045

(3) Bell, K. S., Sebaihia, M., Pritchard, L., Holden, M. T. G., Hyman, L. J., Holeva, M. C.,Haselkorn, R. (2004). Genome sequence of the enterobacterial phytopathogen erwinia carotovora subsp. atroseptica and characterization of virulence factors. Proceedings of the National Academy of Sciences of the United States of America, 101(30), 11105-11110. doi:10.1073/pnas.0402424101

(4) Kõiv, V., Roosaarel, M., Vedler1 E., Kivistik, P.A., Toppi1, K., Schryer, D.W., Remm, M., Tenson, T., Mäe, A. (2015). Microbial population dynamics in response to Pectobacterium atrosepticum infection in potato tubers. Scientific Report 5. doi:10.1038/srep11606.

(5) Nikolaichik, Y., Gorshkov, V., Gogolev, Y., Valentovich, L., & Evtushenkov, A. (2014). Genome sequence of pectobacterium atrosepticum strain 21A. Genome Announcements, 2(5) doi:10.1128/genomeA.00935-14

(6) Gorshkov, V. Y., Daminova, A. G., Mikshina, P. V., Petrova, O. E., Ageeva, M. V., Salnikov, V. V., . . . Gogolev, Y. V. (2016). Pathogen‐induced conditioning of the primary xylem vessels – a prerequisite for the formation of bacterial emboli by pectobacterium atrosepticum. Plant Biology, 18(4), 609-617. doi:10.1111/plb.12448

(7) Babujee L., Apodaca J., Balakrishnan V., Liss P., Kiley P., Charkowski A., et al. (2012). Evolution of the metabolic and regulatory networks associated with oxygen availability in two phytopathogenic enterobacteria. BMC Genomics 13:110. Doi: 10.1186/1471-2164-13-110.

(8) Pectobacterium atrosepcticum SCRI1043. Kyoto Encyclopedia of Genes and Genomes. Retrieved from https://www.genome.jp/kegg-bin/show_organism?menu_type=pathway_maps&org=eca.

(9) Czajkowski, R., Pérombelon, M., Jafra, S., Lojkowska, E., Potrykus, M., van der Wolf, J., Sledz, W. (2015). Detection, identification and differentiation of Pectobacterium and Dickeya species causing potato blackleg and tuber soft rot: a review. The Annals of Applied Biology, 166(1), 18–38. doi:http://doi.org/10.1111/aab.12166

(10) Gorshkov, V., Tarasova, N., Gogoleva, N., Osipova, E., Petrova, O., Kovtunov, E., & Gogolev, Y. (2017). Polyphenol oxidase from pectobacterium atrosepticum: Identification and cloning of gene and characteristics of the enzyme. Journal of Basic Microbiology, 57(12), 998-1009. doi:10.1002/jobm.201700413.

(11) Toth, I.K., Bell, K.S., Holeva, M.C., Birch, P.R.J. (2002). Soft rot erwiniae: from genes to genomes. Molecular Plant Pathology. 4, 17-30. Doi: https://doi.org/10.1046/j.1364-3703.2003.00149.x.

(12) Pérombelon, M.C.M., Lumb, V.M., Hyman, L.J. (1987). A rapid method to identify and quantify soft rot erwinias on seed potato tubers. EPPO Bull. 17, 25–35. Doi: https://doi.org/10.1111/j.1365-2338.1987.tb00004.x

(13) Pérombelon, M.C.M., Salmond, G.P.C. (1995). Bacterial soft rots. Pathogenesis and Host Specificity in Plant Diseases. 1, 1–20.

(14) Gorshkov, V., Gubaev, R., Petrova, O., Daminova, A. Gogoleva, N., Ageeva, M., Parfirova, O., Prokchorchik, M., Nikolaichik, Y., Gogolev, Y. (2018). Transcriptome profiling helps to identify potential and true molecular switches of stealth to brute force behavior in Pectobacterium atrosepticum during systemic colonization of tobacco plants. European Journal of Plant Pathology. https://doi.org/10.1007/s10658-018-1496-6

(15) Pérombelon, M.C.M. (2002). Potato diseases caused by soft rot erwinias: an overview of pathogenesis. Plant Pathology. 51, 1-12. Doi: https://doi.org/10.1046/j.0032-0862.2001.Shorttitle.doc.x.

(16) Wikipedia. (2018). [Blackleg disease in potato]. Retrieved from https://en.wikipedia.org/wiki/ Streptomyces_scabies

(17) Wikipedia. (2013). [Blackleg of Potato Wilt in Field]. Retrieved from https://commons.wikimedia.org/wiki/File:Blackleg_of_Potato_Wilt_in_Field.png

(18) Skelsey, P., Humphris, S.N., Campbell, E.J., Toth, I.K. (2018).Threat of establishment of non-indigenous potato blackleg and tuber soft rot pathogens in Great Britain under climate change. PLOS ONE Medicine Journal. https://doi.org/10.1371/journal.pone.0205711