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Abstract:

In natural environments most bacteria live in multicellular structures called biofilms. These cell aggregates are enclosed in a self-produced polymeric extracellular matrix, which protects the cells, provides mechanical stability and mediates cellular cohesion and adhesion to surfaces. Although important advances were made in the identification of the genetic and extracellular factors required for biofilm formation, the mechanisms leading to biofilm matrix assembly, and the roles of extracellular proteins in these processes are still poorly understood. The symbiont Rhizobium leguminosarum requires the synthesis of the acidic exopolysaccharide and the PrsDE secretion system to develop a mature biofilm. PrsDE is responsible for the secretion of the Rap family of proteins that share one or two Ra/CHDL (cadherin-like-) domains. RapA2 is a calcium-dependent lectin with a cadherin-like β sheet structure that specifically recognizes the exopolysaccharide, either as a capsular polysaccharide (CPS) or in its released form [extracellular polysaccharide (EPS)]. In this study, using gain and loss of function approaches combined with phenotypic and microscopic studies we demonstrated that RapA lectins are involved in biofilm matrix development and cellular cohesion. While the absence of any RapA protein increased the compactness of bacterial aggregates, high levels of RapA1 expanded distances between cells and favored the production of a dense matrix network. Whereas endogenous RapA(s) are predominantly located at one bacterial pole, we found that under overproduction conditions, RapA1 surrounded the cell in a way that was reminiscent of the capsule. Accordingly, polysaccharide analyses showed that the RapA lectins promote CPS formation at the expense of lower EPS production. Besides, polysaccharide analysis suggests that RapA modulates the EPS size profile. Collectively, these results show that the interaction of RapA lectins with the polysaccharide is involved in rhizobial biofilm matrix assembly and remodeling. © 2016 Vozza, Abdian, Russo, Mongiardini, Lodeiro, Molin and Zorreguieta.

Registro:

Documento: Artículo
Título:A Rhizobium leguminosarum CHDL- (cadherin-Like-) lectin participates in assembly and remodeling of the biofilm matrix
Autor:Vozza, N.F.; Abdian, P.L.; Russo, D.M.; Mongiardini, E.J.; Lodeiro, A.R.; Molin, S.; Zorreguieta, A.
Filiación:Fundación Instituto Leloir, IIBBA-CONICET, Buenos Aires, Argentina
Instituto de Bioquímica y Biología Molecular, Departamento de Ciencias Biológicas, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, Centro Científico Technológico COINCET La Plata, La Plata, Argentina
Department of Systems Biology, Technical University of Denmark, Lyngby, Denmark
Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, Lyngby, Denmark
Palabras clave:Biofilms; Exopolysaccharides; Extracellular matrix; Lectins; Rhizobium; gentamicin; kanamycin; lectin; polysaccharide; Rap protein; spectinomycin; streptomycin; tetracycline; Article; bacterial strain; biofilm; cell adhesion; confocal laser scanning microscopy; controlled study; gel filtration chromatography; immunodetection; immunofluorescence; nonhuman; phenotype; plasmid; polymerase chain reaction; protein analysis; proton nuclear magnetic resonance; Rhizobium leguminosarum; scanning electron microscopy; sedimentation; Western blotting
Año:2016
Volumen:7
Número:OCT
DOI: http://dx.doi.org/10.3389/fmicb.2016.01608
Título revista:Frontiers in Microbiology
Título revista abreviado:Front. Microbiol.
ISSN:1664302X
CAS:gentamicin, 1392-48-9, 1403-66-3, 1405-41-0; kanamycin, 11025-66-4, 61230-38-4, 8063-07-8; spectinomycin, 1695-77-8, 21736-83-4, 23312-56-3; streptomycin, 57-92-1; tetracycline, 23843-90-5, 60-54-8, 64-75-5, 8021-86-1
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_1664302X_v7_nOCT_p_Vozza

Referencias:

  • Abdian, P.L., Caramelo, J.J., Ausmees, N., Zorreguieta, A., RapA2 is a calcium-binding lectin composed of two highly conserved cadherin-like domains that specifically recognize Rhizobium leguminosarum acidic exopolysaccharides (2013) J. Biol. Chem, 288, pp. 2893-2904
  • Abdian, P.L., Lellouch, A.C., Gautier, C., Ielpi, L., Geremia, R.A., Identification of essential amino acids in the bacterial alpha-mannosyltransferase aceA (2000) J. Biol. Chem, 275, pp. 40568-40575
  • Albersheim, P., Nevins, D.J., English, P.D., Karr, A., A method for the analysis of sugars in plant cell-wall polysaccharides by gas-liquid chromatography (1967) Carbohydr. Res, 5, pp. 340-345
  • Ausmees, N., Jacobsson, K., Lindberg, M., A unipolarly located, cell-surface-associated agglutinin, RapA, belongs to a family of Rhizobium-adhering proteins (Rap) in Rhizobium leguminosarum bv. trifolii (2001) Microbiology, 147, pp. 549-559
  • Beringer, J.E., R factor transfer in Rhizobium leguminosarum (1974) J. Gen. Microbiol, 84, pp. 188-198
  • Berk, V., Fong, J.C., Dempsey, G.T., Develioglu, O.N., Zhuang, X., Liphardt, J., Molecular architecture and assembly principles of Vibrio cholerae biofilms (2012) Science, 337, pp. 236-239
  • Borlee, B.R., Goldman, A.D., Murakami, K., Samudrala, R., Wozniak, D.J., Parsek, M.R., Pseudomonas aeruginosa uses a cyclic-di-GMP-regulated adhesin to reinforce the biofilm extracellular matrix (2010) Mol. Microbiol, 75, pp. 827-842
  • Branda, S.S., Vik, S., Friedman, L., Kolter, R., Biofilms: the matrix revisited (2005) Trends Microbiol, 13, pp. 20-26
  • Cao, L., Yan, X., Borysenko, C.W., Blair, H.C., Wu, C., Yu, L., CHDL: a cadherin-like domain in Proteobacteria and Cyanobacteria (2005) FEMS Microbiol. Lett, 251, pp. 203-209
  • Cheng, H.P., Walker, G.C., Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti (1998) J. Bacteriol, 180, pp. 5183-5191
  • Costerton, J.W., Lewandowski, Z., DeBeer, D., Caldwell, D., Korber, D., James, G., Biofilms, the customized microniche (1994) J. Bacteriol, 176, pp. 2137-2142
  • Danhorn, T., Fuqua, C., Biofilm formation by plant-associated bacteria (2007) Annu. Rev. Microbiol, 61, pp. 401-422
  • Davey, M.E., O'Toole, G.A., Microbial biofilms: from ecology to molecular genetics (2000) Microbiol. Mol. Biol. Rev, 64, pp. 847-867
  • De Ruiter, G.A., Schols, H.A., Voragen, A.G.J., Rombouts, F.M., Carbohydrate analysis of water-soluble uronic-acid containing polysaccharides with high-performance anion-exchange chromatography using methanolysis combined with TFA hydrolysis is superior to four other methods (1992) Anal. Biochem, 207, pp. 176-185
  • Downie, J.A., The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots (2010) FEMS Microbiol. Rev, 34, pp. 150-170
  • Downie, J.A., Rossen, L., Knight, C.D., Robertson, J.G., Wells, B., Johnston, A.W., Rhizobium leguminosarum genes involved in early stages of nodulation (1985) J. Cell Sci. Suppl, 2, pp. 347-354
  • Economou, A., Hamilton, W.D., Johnston, A.W., Downie, J.A., The Rhizobium nodulation gene nodO encodes a Ca2(+)-binding protein that is exported without N-terminal cleavage and is homologous to haemolysin and related proteins (1990) EMBO J, 9, pp. 349-354
  • Filisetti-Cozzi, T.M., Carpita, N.C., Measurement of uronic acids without interference from neutral sugars (1991) Anal. Biochem, 197, pp. 157-162
  • Finnie, C., Hartley, N.M., Findlay, K.C., Downie, J.A., The Rhizobium leguminosarum prsDE genes are required for secretion of several proteins, some of which influence nodulation, symbiotic nitrogen fixation and exopolysaccharide modification (1997) Mol. Microbiol, 25, pp. 135-146
  • Finnie, C., Zorreguieta, A., Hartley, N.M., Downie, J.A., Characterization of Rhizobium leguminosarum exopolysaccharide glycanases that are secreted via a type i exporter and have a novel heptapeptide repeat motif (1998) J. Bacteriol, 180, pp. 1691-1699
  • Fischer, E.R., Hansen, B.T., Nair, V., Hoyt, F.H., Dorward, D.W., Scanning electron microscopy (2012) Curr. Protoc. Microbiol, , Chapter 2, Unit2B2
  • Flemming, H.C., Wingender, J., The biofilm matrix (2010) Nat. Rev. Microbiol, 8, pp. 623-633
  • Frederix, M., Edwards, A., Swiderska, A., Stanger, A., Karunakaran, R., Williams, A., Mutation of praR in Rhizobium leguminosarum enhances root biofilms, improving nodulation competitiveness by increased expression of attachment proteins (2014) Mol. Microbiol, 93, pp. 464-478
  • Fujishige, N.A., Kapadia, N.N., De Hoff, P.L., Hirsch, A.M., Investigations of Rhizobium biofilm formation (2006) FEMS Microbiol. Ecol, 56, pp. 195-206
  • Heyraud, A., Courtois, J., Dantas, L., Colin-Morel, P., Courtois, B., Structural characterization and rheological properties of an extracellular glucuronan produced by a Rhizobium meliloti M5N1 mutant strain (1993) Carbohydr. Res, 240, pp. 71-78
  • Hollingsworth, R.I., Abe, M., Sherwood, J.E., Dazzo, F.B., Bacteriophage-induced acidic heteropolysaccharide lyases that convert the acidic heteropolysaccharides of Rhizobium trifolii into oligosaccharide units (1984) J. Bacteriol, 160, pp. 510-516
  • Johnston, A.W., Beringer, J.E., Identification of the Rhizobium strains in pea root nodules using genetic markers (1975) J. Gen. Microbiol, 87, pp. 343-350
  • Kovach, M.E., Elzer, P.H., Hill, D.S., Robertson, G.T., Farris, M.A., Roop, R.M., II, Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes (1995) Gene, 166, pp. 175-176
  • Krehenbrink, M., Downie, J.A., Identification of protein secretion systems and novel secreted proteins in Rhizobium leguminosarum bv. viciae (2008) BMC Genomics, 9, p. 55
  • Laus, M.C., Logman, T.J., Lamers, G.E., Van Brussel, A.A., Carlson, R.W., Kijne, J.W., A novel polar surface polysaccharide from Rhizobium leguminosarum binds host plant lectin (2006) Mol. Microbiol, 59, pp. 1704-1713
  • Laus, M.C., Logman, T.J., Van Brussel, A.A., Carlson, R.W., Azadi, P., Gao, M.Y., Involvement of exo5 in production of surface polysaccharides in Rhizobium leguminosarum and its role in nodulation of Vicia sativa subsp. nigra (2004) J. Bacteriol, 186, pp. 6617-6625
  • Loewus, F.A., Improvement in anthrone method for determination of carbohydrates (1952) Anal. Chem, 24, p. 219
  • Mongiardini, E.J., Ausmees, N., Perez-Gimenez, J., Julia Althabegoiti, M., Ignacio Quelas, J., Lopez-Garcia, S.L., The rhizobial adhesion protein RapA1 is involved in adsorption of rhizobia to plant roots but not in nodulation (2008) FEMS Microbiol. Ecol, 65, pp. 279-288
  • Omori, K., Idei, A., Gram-negative bacterial ATP-binding cassette protein exporter family and diverse secretory proteins (2003) J. Biosci. Bioeng, 95, pp. 1-12
  • O'Toole, G.A., Pratt, L.A., Watnick, P.I., Newman, D.K., Weaver, V.B., Kolter, R., Genetic approaches to study of biofilms (1999) Methods Enzymol, 310, pp. 91-109
  • Park, J.H., Jo, Y., Jang, S.Y., Kwon, H., Irie, Y., Parsek, M.R., The cabABC operon essential for biofilm and rugose colony development in Vibrio vulnificus (2015) PLoS Pathog, 11
  • Rinaudi, L.V., Sorroche, F., Zorreguieta, A., Giordano, W., Analysis of the mucR gene regulating biosynthesis of exopolysaccharides: implications for biofilm formation in Sinorhizobium meliloti Rm1021 (2010) FEMS Microbiol. Lett, 302, pp. 15-21
  • Rodriguez-Navarro, D.N., Dardanelli, M.S., Ruiz-Sainz, J.E., Attachment of bacteria to the roots of higher plants (2007) FEMS Microbiol. Lett, 272, pp. 127-136
  • Russo, D.M., Abdian, P.L., Posadas, D.M., Williams, A., Vozza, N., Giordano, W., Lipopolysaccharide O-chain core region required for cellular cohesion and compaction of in vitro and root biofilms developed by Rhizobium leguminosarum (2015) Appl. Environ. Microbiol, 81, pp. 1013-1023
  • Russo, D.M., Williams, A., Edwards, A., Posadas, D.M., Finnie, C., Dankert, M., Proteins exported via the PrsD-PrsE type I secretion system and the acidic exopolysaccharide are involved in biofilm formation by Rhizobium leguminosarum (2006) J. Bacteriol, 188, pp. 4474-4486
  • Schafer, A., Tauch, A., Jager, W., Kalinowski, J., Thierbach, G., Puhler, A., Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum (1994) Gene, 145, pp. 69-73
  • Sherwood, M.T., Improved synthetic medium for the growth of Rhizobium (1970) J. Appl. Bacteriol, 33, pp. 708-713
  • Simon, R., Priefer, U., Pûhler, A., "Vector plasmids for in vivo and in vitro manipulations of gram-negative bacteria," (1983) Molecular Genetics of the Bacteria-Plant Interactions, pp. 98-106. , ed. A. Pûhler (Berlin: Springer-Verlag KG)
  • Skorupska, A., Janczarek, M., Marczak, M., Mazur, A., Krol, J., Rhizobial exopolysaccharides: genetic control and symbiotic functions (2006) Microb. Cell Fact, 5, p. 7
  • Staskawicz, B., Dahlbeck, D., Keen, N., Napoli, C., Molecular characterization of cloned avirulence genes from race 0 and race 1 of Pseudomonas syringae pv. glycinea (1987) J. Bacteriol, 169, pp. 5789-5794
  • Wang, R., Neoh, T.L., Kobayashi, T., Miyake, Y., Hosoda, A., Taniguchi, H., Degradation kinetics of glucuronic acid in subcritical water (2010) Biosci. Biotechnol. Biochem, 74, pp. 601-605
  • Williams, A., Wilkinson, A., Krehenbrink, M., Russo, D.M., Zorreguieta, A., Downie, J.A., Glucomannan-mediated attachment of Rhizobium leguminosarum to pea root hairs is required for competitive nodule infection (2008) J. Bacteriol, 190, pp. 4706-4715
  • Young, J.P., Crossman, L.C., Johnston, A.W., Thomson, N.R., Ghazoui, Z.F., Hull, K.H., The genome of Rhizobium leguminosarum has recognizable core and accessory components (2006) Genome Biol, 7
  • Zorreguieta, A., Finnie, C., Downie, J.A., Extracellular glycanases of Rhizobium leguminosarum are activated on the cell surface by an exopolysaccharide-related component (2000) J. Bacteriol, 182, pp. 1304-1312

Citas:

---------- APA ----------
Vozza, N.F., Abdian, P.L., Russo, D.M., Mongiardini, E.J., Lodeiro, A.R., Molin, S. & Zorreguieta, A. (2016) . A Rhizobium leguminosarum CHDL- (cadherin-Like-) lectin participates in assembly and remodeling of the biofilm matrix. Frontiers in Microbiology, 7(OCT).
http://dx.doi.org/10.3389/fmicb.2016.01608
---------- CHICAGO ----------
Vozza, N.F., Abdian, P.L., Russo, D.M., Mongiardini, E.J., Lodeiro, A.R., Molin, S., et al. "A Rhizobium leguminosarum CHDL- (cadherin-Like-) lectin participates in assembly and remodeling of the biofilm matrix" . Frontiers in Microbiology 7, no. OCT (2016).
http://dx.doi.org/10.3389/fmicb.2016.01608
---------- MLA ----------
Vozza, N.F., Abdian, P.L., Russo, D.M., Mongiardini, E.J., Lodeiro, A.R., Molin, S., et al. "A Rhizobium leguminosarum CHDL- (cadherin-Like-) lectin participates in assembly and remodeling of the biofilm matrix" . Frontiers in Microbiology, vol. 7, no. OCT, 2016.
http://dx.doi.org/10.3389/fmicb.2016.01608
---------- VANCOUVER ----------
Vozza, N.F., Abdian, P.L., Russo, D.M., Mongiardini, E.J., Lodeiro, A.R., Molin, S., et al. A Rhizobium leguminosarum CHDL- (cadherin-Like-) lectin participates in assembly and remodeling of the biofilm matrix. Front. Microbiol. 2016;7(OCT).
http://dx.doi.org/10.3389/fmicb.2016.01608