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Abstract:

Xanthan is a virulence factor produced by Xanthomonas spp. We previously demonstrated that this exopolysaccharide is not only essential for pathogenicity by contributing with bacterial survival but also its pyruvate substituents interfere with some plant defense responses. Deepening our studies about xanthan properties and structure, the aim of this work was to analyze the characteristics of xanthan produced by Xanthomonas in different culture media. We analyzed the xanthan produced by Xanthomonas citri subsp. citri (Xcc) in leaf extracts from grapefruit (a susceptible host of this bacterium) and compared it with the xanthan produced in a synthetic culture medium. We found that the xanthan produced in the grapefruit extract (Xan-GLE) presented shorter and more disordered molecules than xanthan produced in the synthetic medium (Xan-PYM). Besides, Xan-GLE resulted less viscous than Xan-PYM. The disordered molecular conformation of Xan-GLE could be attributed to its higher pyruvilation degree and lower acetylation degree compared with those detected in Xan-PYM. Meanwhile, the difference in the viscosity of both xanthans could be due to their molecules length. Finally, we cultured Xcc in the presence of the Xan-GLE or Xan-PYM and observed the formation of biofilm-like structures in both cases. We found significant differences in biofilm architecture between the two conditions, being the biofilm produced in presence of Xan-GLE similar to that formed in canker lesions developed in lemon plant leaves. Together, these results show how xanthan structure and properties changed when Xcc grew in a natural substrate and can contribute to better understand the biological role of xanthan. © © The Author(s) 2019. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.

Registro:

Documento: Artículo
Título:Changes in the physico-chemical properties of the xanthan produced by Xanthomonas citri subsp. citri in grapefruit leaf extract
Autor:Conforte, V.P.; Yaryura, P.M.; Bianco, M.I.; Rodríguez, M.C.; Daglio, Y.; Prieto, E.; Schilardi, P.; Vojnov, A.A.
Filiación:Instituto de Ciencia y Tecnología Dr. César Milstein, Fundación Pablo Cassará, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Saladillo, Ciudad de Buenos Aires, 2468 (C1440FFX), Argentina
Centro de Investigaciones y Transferencia (CIT Villa María), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Instituto de Ciencias Básicas y Aplicadas, Universidad Nacional de Villa María., Av. Arturo Jauretche 1555, (5900), Villa María, Córdoba, Argentina
Niversidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales, Departamento de Biodiversidad y Biología Experimental, Ciudad Universitaria-Pabellón 2, C1428EGA., Ciudad Autónoma de Buenos Aires, Argentina
Universidad de Buenos Aires, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Centro de Investigación en Hidratos de Carbono (CIHIDECAR), Facultad de Ciencias Exactas y Naturales Pabellón II, 3er P, Ciudad Universitaria, Buenos Aires, 1428, Argentina
Universidad Nacional de la Plata (UNLP), Instituto de Investigaciones Fisicoquímicas Teóricas y Aplicadas, Consejo Nacional de Investigaciones Científicas y Tecnológicas INIFTA - CONICET), Diagonal 113 y 64 S/N La Plata, Buenos Aires, Argentina
Palabras clave:grapefruit leaf extract; xanthan; Xanthomonas citri subsp. citri
Año:2019
Volumen:29
Número:3
Página de inicio:269
Página de fin:278
DOI: http://dx.doi.org/10.1093/glycob/cwy114
Título revista:Glycobiology
Título revista abreviado:Glycobiology
ISSN:09596658
CODEN:GLYCE
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_09596658_v29_n3_p269_Conforte

Referencias:

  • Allaway, D., Schofield, N.A., Leonard, M.E., Gilardoni, L., Finan, T.M., Poole, P.S., Use of differential fluorescence induction and optical trapping to isolate environmentally induced genes (2001) Environ Microbiol., 3, pp. 397-406
  • Aslam, S.N., Newman, M.A., Erbs, G., Morrissey, K.L., Chinchilla, D., Boller, T., Jensen, T.T., Molinaro, A., Bacterial polysaccharides suppress induced innate immunity by calcium chelation (2008) Curr Biol., 18, pp. 1078-1083
  • Bergmann, D., Furth, G., Mayer, C., Binding of bivalent cations by xanthan in aqueous solution (2008) J Biol Macromol., 43, pp. 245-251
  • Bianco, M.I., Toum, L., Yaryura, P.M., Mielnichuk, N., Gudesblat, G.E., Roeschlin, R., Marano, M.R., Vojnov, A.A., Xanthan pyruvilation is essential for the virulence of Xanthomonas campestris pv campestris (2016) Mol Plant Microbe Interact., 29, pp. 688-699
  • Cadmus, M., Knutson, C., Lagoda, A., Pittsley, J., Burton, K., Synthetic media for production of quality xanthan gum in 20 liter fermentors (1978) Biotechnol Bioeng., 20, pp. 1003-1014
  • Cadmus, M.C., Rogovin, S.P., Burton, K.A., Pittsley, J.E., Knutson, C.A., Jeanes, A., Colonial variation in Xanthomonas campestris NRRL B-1459 and characterization of the polysaccharide from a variant strain (1976) Can J Microbiol., 22, pp. 942-948
  • Capron, I., Alexandre, S., Muller, G., An atomic force microscopy study of the molecular organisation of xanthan (1998) Polymer (Guildf)., 39, pp. 5725-5730
  • Chou, F.L., Chou, H.C., Lin, Y.S., Yang, B.Y., Lin, N.T., Weng, S.F., Tseng, Y.H., The Xanthomonas campestris gumD gene required for synthesis of xanthan gum is involved in normal pigmentation and virulence in causing black rot (1997) Biochem Biophys Res Commun., 233, pp. 265-269
  • Costacurta, A., Mazzafera, P., Rosato, Y.B., Indole-3-acetic acid biosynthesis by Xanthomonas axonopodis pv citri is increased in the presence of plant leaf extracts (1998) FEMS Microbiol Lett., 159, pp. 215-220
  • Da Silva, A.C.R., Ja, F., Reinach, F.C., Farah, C.S., Furlan, L.R., Quaggio, R.B., Monteiro-Vitorello, C.B., Alves, L.M., Comparison of the genomes of two Xanthomonas pathogens with differing host specificities (2002) Nature, 417, pp. 459-463
  • De Weert, S., Vermeiren, H., Mulders, I.H., Kuiper, I., Hendrickx, N., Bloemberg, G.V., Vanderleyden, J., Lugtenberg, B.J., Flagella-driven chemotaxis towards exudate components is an important trait for tomato root colonization by Pseudomonas fluorescens (2002) Mol Plant Microbe Interact., 15, pp. 1173-1180
  • Dentini, M., Crescenzi, V., Blasi, D., Conformational properties of xanthan derivatives in dilute aqueous solution (1984) J Biol Macromol., 6, pp. 93-98
  • Dharmapuri, S., Sonti, R.V., A transposon insertion in the gumG homologue of Xanthomonas oryzae pv oryzae causes loss of extracellular polysaccharide production and virulence (1999) FEMS Microbiol Lett., 179, pp. 53-59
  • Dow, J.M., Crossman, L., Findlay, K., He, Y.Q., Feng, J.X., Tang, J.L., Biofilm dispersal in Xanthomonas campestris is controlled by cell-cell signaling and is required for full virulence to plants (2003) Proc Natl Acad Sci U S A., 100, pp. 10995-11000
  • Dow, J.M., Daniels, M.J., Pathogenicity determinants and global regulation of pathogenicity of Xanthomonas campestris pv (1994) Campestris. Curr Top Microbiol Immunol., 192, pp. 29-41
  • Dunger, G., Relling, V.M., Tondo, M.L., Barreras, M., Ielpi, L., Orellano, E.G., Ottado, J., Xanthan is not essential for pathogenicity in citrus canker but contributes to Xanthomonas epiphytic survival (2007) Arch Microbiol., 188, pp. 127-135
  • Faria, S., De Petkowicz, O.C.L., De Morais, S.A.L., Terrones, M.G.H., De Resende, M.M., De França, F.P., Cardoso, V.L., Characterization of xanthan gum produced from sugar cane broth (2011) Carbohydr Polym., 86, pp. 469-476
  • Felipe, V., Romero, A.M., Montecchia, M.S., Vojnov, A.A., Bianco, M.I., Yaryura, P.M., Xanthomonas vesicatoria virulence factors involved in early stages of bacterial spot development in tomato (2018) Plant Pathol
  • Fischer, S.E., Miguel, M.J., Mori, G.B., Effect of root exudates on the exopolysaccharide composition and the lipopolysaccharide profile of Azospirillum brasilense Cd under saline stress (2003) FEMS Microbiol Lett., 219, pp. 53-62
  • Flemming, H.-C., Wingender, J., The biofilm matrix (2010) Nat Rev Microbiol., 8, p. 623
  • Galván, E.M., Ielmini, M.V., Patel, Y.N., Bianco, M.I., Franceschini, E.A., Schneider, J.C., Ielpi, L., Xanthan chain length is modulated by increasing the availability of the polysaccharide copolymerase protein GumC and the outer membrane polysaccharide export protein GumB (2012) Glycobiology., 23, pp. 259-272
  • Goto, M., Yaguchi, Y., Hyodo, H., Ethylene production in citrus leaves infected with Xanthomonas citri and its relation to defoliation (1980) Physiol Plant Pathol., 16, pp. 343-350
  • Gottwald, T.R., Sun, X., Riley, T., Graham, J.H., Ferrandino, F., Taylor, E.L., Geo-referenced spatiotemporal analysis of the urban citrus canker epidemic in Florida (2002) Phytopathology., 92, pp. 361-377
  • Hestrin, S., The reaction of acetylcholine and other carboxylic acid derivatives with hydroxylamine, and its analytical application (1949) J Biol Chem., 180, pp. 249-261
  • Heydorn, A., Nielsen, A.T., Hentzer, M., Sternberg, C., Givskov, M., Ersbøll, B.K., Molin, S., Quantification of biofilm structures by the novel computer program COMSTAT (2000) Microbiology., 146, pp. 2395-2407
  • Holzwarth, G., Ogletree, J., Pyruvate-free xanthan (1979) Carbohydrate Res., 76, pp. 277-280
  • Holzwarth, G., Prestridge, E., Multistranded helix in xanthan polysaccharide (1977) Science., 197, pp. 757-759
  • Jansson, P.E., Kenne, L., Lindberg, B., Structure of extracellular polysaccharide from Xanthomonas campestris (1975) Carbohydr Res., 45, pp. 275-282
  • Kang, K., Pettitt, D., Xanthan, gellan, welan, and rhamsan (1993) Industrial Gums, pp. 341-397. , 3rd edn. Cambridge, MA: Academic Press-Elsevier
  • Katzen, F., Ferreiro, D.U., Oddo, C.G., Ielmini, M.V., Becker, A., Puhler, A., Ielpi, L., Xanthomonas campestris pv campestris gum mutants: Effects on xanthan biosynthesis and plant virulence (1998) J Bacteriol., 180, pp. 1607-1617
  • Kemp, B.P., Horne, J., Bryant, A., Cooper, R.M., Xanthomonas axonopodis pv manihotis gumD gene is essential for EPS production and pathogenicity and enhances epiphytic survival on cassava (Manihot esculenta) (2004) Physiol Mol Plant Pathol., 64, pp. 209-218
  • Kennedy, J., Bradshaw, I., Production, properties and applications of Xanthan (1984) Prog Ind Microbiol., 19, pp. 319-371
  • Kim, S.Y., Kim, J.G., Lee, B.M., Cho, J.Y., Mutational analysis of the gum gene cluster required for xanthan biosynthesis in Xanthomonas oryzae pv oryzae (2009) Biotechnol Lett., 31, pp. 265-270
  • Kirby, A.R., Gunning, A.P., Morris, V.J., Imaging xanthan gum by atomic force microscopy (1995) Carbohydr Res., 267, pp. 161-166
  • Koepsell, H., Sharpe, E., Microdetermination of pyruvic and α-ketoglutaric acids (1952) Arch Biochem Biophys., 38, pp. 443-449
  • Malamud, F., Homem, R.A., Conforte, V.P., Yaryura, P.M., Castagnaro, A.P., Marano, M.R., Morais Do Amaral, A., Vojnov, A.A., Identification and characterization of biofilm formation-defective mutants of Xanthomonas citri subsp (2013) Citri Microbiol., 159, pp. 1911-1919
  • Malamud, F., Torres, P.S., Roeschlin, R., Rigano, L.A., Enrique, R., Bonomi, H.R., Castagnaro, A.P., Vojnov, A.A., The Xanthomonas axonopodis pv citri flagellum is required for mature biofilm and canker development (2011) Microbiology., 157, pp. 819-829
  • Mehta, A., Rosato, Y.B., Differentially expressed proteins in the interaction of Xanthomonas axonopodis pv citri with leaf extract of the host plant (2001) PROTEOMICS: Int Ed., 1, pp. 1111-1118
  • Milas, M., Rinaudo, M., Conformational investigation on the bacterial polysaccharide xanthan (1979) Carbohydr Res., 76, pp. 189-196
  • Morillo, J.A., Aguilera, M., Ramos-Cormenzana, A., Monteoliva-Sánchez, M., Production of a metal-binding exopolysaccharide by Paenibacillus jamilae using two-phase olive-mill waste as fermentation substrate (2006) Curr Microbiol., 53, pp. 189-193
  • Morris, E., Molecular origin of xanthan solution properties (1977) Extracellular Microbial Polysaccharides, pp. 81-89. , In: Sandford PA, Laskin A, editors. Washington, US: American Chemical Society
  • Murga, R., Stewart, P.S., Daly, D., Quantitative analysis of biofilm thickness variability (1995) Biotechnol Bioeng., 45, pp. 503-510
  • Møller, S., Sternberg, C., Andersen, J.B., Christensen, B.B., Ramos, J.L., Givskov, M., Molin, S., In situ gene expression in mixed-culture biofilms: Evidence of metabolic interactions between community members (1998) Appl Environ Microbiol., 64, pp. 721-732
  • Palaniraj, A., Jayaraman, V., Production, recovery and applications of xanthan gum by Xanthomonas campestris (2011) J Food Eng., 106, pp. 1-12
  • Patil, S.V., Salunkhe, R.B., Patil, C.D., Patil, D.M., Salunke, B.K., Bioflocculant exopolysaccharide production by Azotobacter indicus using flower extract of Madhuca latifolia L (2010) Appl Biochem Biotechnol., 162, pp. 1095-1108
  • Peters, H.-U., Suh, I.-S., Schumpe, A., Deckwer, W.-D., The pyruvate content of xanthan polysaccharide produced under oxygen limitation (1993) Biotechnol Lett., 15, pp. 565-566
  • Rigano, L.A., Payette, C., Brouillard, G., Marano, M.R., Abramowicz, L., Torres, P.S., Yun, M., Dufour, V., Bacterial cyclic beta-(1,2)-glucan acts in systemic suppression of plant immune responses (2007) Plant Cell., 19, pp. 2077-2089
  • Rigano, L.A., Siciliano, F., Enrique, R., Sendin, L., Filippone, P., Torres, P.S., Questa, J., Vojnov, A.A., Biofilm formation, epiphytic fitness, and canker development in Xanthomonas axonopodis pv citri (2007) Mol Plant Microbe Interact., 20, pp. 1222-1230
  • Rinaudo, M., Role of substituents on the properties of some polysaccharides (2004) Biomacromolecules., 5, pp. 1155-1165
  • Sandford, P.A., Watson, P.R., Knutson, C.A., Separation of xanthan gums of differing pyruvate content by fractional precipitation with alcohol (1978) Carbohydr Res., 63, pp. 253-256
  • Shatwell, K.P., Sutherland, I.W., Ross-Murphy, S.B., Influence of acetyl and pyruvate substituents on the solution properties of xanthan polysaccharide (1990) J Biol Macromol., 12, pp. 71-78
  • Sherwood, M.T., Improved synthetic medium for the growth of Rhizobium (1970) J Appl Bacteriol., 33, pp. 708-713
  • Shivakumar, S., Vijayendra, S., Production of exopolysaccharides by Agrobacterium sp CFR-24 using coconut water-A byproduct of food industry (2006) Lett Appl Microbiol., 42, pp. 477-482
  • Simon, R., High frequency mobilization of gram-negative bacterial replicons by the in vitro constructed Tn5-Mob transposon (1984) Mol Gen Genet MGG., 196, pp. 413-420
  • Smith, I., Symes, K., Lawson, C., Morris, E., Influence of the pyruvate content of xanthan on macromolecular association in solution (1981) J Biol Macromol., 3, pp. 129-134
  • Souw, P., Demain, A.L., Nutritional Studies on Xanthan Production by Xanthomonas campestris NRRL B1459 (1979) Appl Environ Microbiol., 37, pp. 1186-1192
  • Stankowski, J.D., Mueller, B.E., Zeller, S.G., Location of a second O-acetyl group in xanthan gum by the reductive-cleavage method (1993) Carbohydr Res., 241, pp. 321-326
  • Stoodley, P., Cargo, R., Rupp, C.J., Wilson, S., Klapper, I., Biofilm material properties as related to shear-induced deformation and detachment phenomena (2002) J Ind Microbiol Biotechnol., 29, pp. 361-367
  • Sutherland, I., Xanthomonas polysaccharides-improved methods for their comparison (1981) Carbohydr Polym., 1, pp. 107-115
  • Sutherland, I.W., Biofilm exopolysaccharides: A strong and sticky framework (2001) Microbiology., 147, pp. 3-9
  • Swarup, S., Yang, Y., Kingsley, M.T., Gabriel, D.W., An Xanthomonas citri pathogenicity gene, pthA, pleiotropically encodes gratuitous avirulence on nonhosts (1992) Mol Plant Microbe Interact., 5, pp. 204-213
  • Tako, M., Asato, A., Nakamura, S., Rheological aspects of the intermolecular interaction between xanthan and locust bean gum in aqueous media (1984) Agricu Biol Chem., 48, pp. 2995-3000
  • Torres, P.S., Malamud, F., Rigano, L.A., Russo, D.M., Marano, M.R., Castagnaro, A.P., Zorreguieta, A., Vojnov, A.A., Controlled synthesis of the DSF cell-cell signal is required for biofilm formation and virulence in Xanthomonas campestris (2007) Environ Microbiol., 9, pp. 2101-2109
  • Trilsbach, G., Xanthan formation by Xanthomonas campestris under different culture conditions (1984) Eur Congr Biotechnol 3rd Meet, 2, pp. 65-70
  • Vojnov, A.A., Marano, M.R., Biofilm formation and virulence in bacterial plant pathogens (2016) Virulence Mechanisms of Plan-pathogenic Bacteria, pp. 21-34. , In: Wang N, Jones JB, Sundin GW, White F, Hogenhout S, Roper C, De La Fuente L, Ham LH, editors. Minnesota, US: The American Phytopathological Society
  • Vu, B., Chen, M., Crawford, R.J., Ivanova, E.P., Bacterial extracellular polysaccharides involved in biofilm formation (2009) Molecules., 14, pp. 2535-2554
  • Xiao, J., Klein, M.I., Falsetta, M.L., Lu, B., Delahunty, C.M., Yates, J.R., III, Heydorn, A., Koo, H., The exopolysaccharide matrix modulates the interaction between 3D architecture and virulence of a mixed-species oral biofilm (2012) PLoS Pathog., 8, p. e1002623
  • Yun, M.H., Torres, P.S., El Oirdi, M., Rigano, L.A., Gonzalez-Lamothe, R., Marano, M.R., Castagnaro, A.P., Vojnov, A.A., Xanthan induces plant susceptibility by suppressing callose deposition (2006) Plant Physiol., 141, pp. 178-187

Citas:

---------- APA ----------
Conforte, V.P., Yaryura, P.M., Bianco, M.I., Rodríguez, M.C., Daglio, Y., Prieto, E., Schilardi, P.,..., Vojnov, A.A. (2019) . Changes in the physico-chemical properties of the xanthan produced by Xanthomonas citri subsp. citri in grapefruit leaf extract. Glycobiology, 29(3), 269-278.
http://dx.doi.org/10.1093/glycob/cwy114
---------- CHICAGO ----------
Conforte, V.P., Yaryura, P.M., Bianco, M.I., Rodríguez, M.C., Daglio, Y., Prieto, E., et al. "Changes in the physico-chemical properties of the xanthan produced by Xanthomonas citri subsp. citri in grapefruit leaf extract" . Glycobiology 29, no. 3 (2019) : 269-278.
http://dx.doi.org/10.1093/glycob/cwy114
---------- MLA ----------
Conforte, V.P., Yaryura, P.M., Bianco, M.I., Rodríguez, M.C., Daglio, Y., Prieto, E., et al. "Changes in the physico-chemical properties of the xanthan produced by Xanthomonas citri subsp. citri in grapefruit leaf extract" . Glycobiology, vol. 29, no. 3, 2019, pp. 269-278.
http://dx.doi.org/10.1093/glycob/cwy114
---------- VANCOUVER ----------
Conforte, V.P., Yaryura, P.M., Bianco, M.I., Rodríguez, M.C., Daglio, Y., Prieto, E., et al. Changes in the physico-chemical properties of the xanthan produced by Xanthomonas citri subsp. citri in grapefruit leaf extract. Glycobiology. 2019;29(3):269-278.
http://dx.doi.org/10.1093/glycob/cwy114