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Abstract:

Sinorhizobium meliloti is a symbiotic nitrogen-fixing bacterium that elicits nodule formation on roots of alfalfa plants. S. meliloti produces two exopolysaccharides (EPSs), termed EPS I and EPS II, that are both able to promote symbiosis. EPS I and EPS II are secreted in two major fractions that reflect differing degrees of subunit polymerization, designated high- and low-molecularweight fractions. We reported previously that EPSs are crucial for autoaggregation and biofilm formation in S. meliloti reference strains and isogenic mutants. However, the previous observations were obtained by use of "domesticated" laboratory strains, with mutations resulting from successive passages under unnatural conditions, as has been documented for reference strain Rm1021. In the present study, we analyzed the autoaggregation and biofilm formation abilities of native S. meliloti strains isolated from root nodules of alfalfa plants grown in four regions of Argentina. 16S rRNA gene analysis of all the native isolates revealed a high degree of identity with reference S. meliloti strains. PCR analysis of the expR gene of all the isolates showed that, as in the case of reference strain Rm8530, this gene is not interrupted by an insertion sequence (IS) element. A positive correlation was found between autoaggregation and biofilm formation abilities in these rhizobia, indicating that both processes depend on the same physical adhesive forces. Extracellular complementation experiments using mutants of the native strains showed that autoaggregation was dependent on EPS II production. Our results indicate that a functional EPS II synthetic pathway and its proper regulation are essential for cell-cell interactions and surface attachment of S. meliloti. © 2012, American Society for Microbiology.

Registro:

Documento: Artículo
Título:A positive correlation between bacterial autoaggregation and biofilm formation in native Sinorhizobium meliloti isolates from Argentina
Autor:Sorroche, F.G.; Spesia, M.B.; Zorreguieta, Á.; Giordano, W.
Filiación:Departamento de Biología Molecular, Universidad Nacional de Río Cuarto, Río Cuarto, Córdoba, Argentina
Fundación Instituto Leloir, IIBBA, CONICET and FCEyN, Universidad de Buenos Aires, Buenos Aires, Argentina
Palabras clave:16S rRNA gene; Adhesive force; Argentina; Biofilm formation; Cell-cell interaction; Complementation; Exopolysaccharides; Extracellular; Insertion sequences; Nitrogen fixing bacteria; PCR analysis; Positive correlations; Reference strains; Root nodules; Sinorhizobium meliloti; Surface attachment; Synthetic pathways; Bacteria; Genes; Nitrogen fixation; RNA; Biofilms; bacterial DNA; bacterial polysaccharide; ribosome DNA; RNA 16S; aggregation; alfalfa; bacterium; biofilm; genetic analysis; mutation; nitrogen fixation; nodulation; polymerase chain reaction; polymerization; symbiont; symbiosis; alfalfa; Argentina; article; bacterium adherence; biofilm; chemistry; classification; cluster analysis; DNA sequence; genetics; growth, development and aging; isolation and purification; metabolism; microbiology; molecular genetics; nucleotide sequence; phylogeny; physiology; plant root; Sinorhizobium meliloti; Argentina; Bacterial Adhesion; Biofilms; Cluster Analysis; DNA, Bacterial; DNA, Ribosomal; Medicago sativa; Molecular Sequence Data; Phylogeny; Plant Roots; Polysaccharides, Bacterial; RNA, Ribosomal, 16S; Sequence Analysis, DNA; Sinorhizobium meliloti; Argentina; Bacteria (microorganisms); Medicago sativa; Sinorhizobium meliloti
Año:2012
Volumen:78
Número:12
Página de inicio:4092
Página de fin:4101
DOI: http://dx.doi.org/10.1128/AEM.07826-11
Título revista:Applied and Environmental Microbiology
Título revista abreviado:Appl. Environ. Microbiol.
ISSN:00992240
CODEN:AEMID
CAS:DNA, Bacterial; DNA, Ribosomal; Polysaccharides, Bacterial; RNA, Ribosomal, 16S
PDF:https://bibliotecadigital.exactas.uba.ar/download/paper/paper_00992240_v78_n12_p4092_Sorroche.pdf
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00992240_v78_n12_p4092_Sorroche

Referencias:

  • Altschul, S.F., Gapped BLAST and PSI-BLAST, a new generation of protein database search programs (1997) Nucleic Acids Res, 25, pp. 3389-3402
  • Bogino, P., Banchio, E., Bonfiglio, C., Giordano, W., Competitiveness of a Bradyrhizobium sp. strain in soils containing indigenous rhizobia (2008) Curr. Microbiol., 56, pp. 66-72
  • Brosius, J., Palmer, J.L., Kennedy, H.P., Noller, H.F., Complete nucleotide sequence of a 16S ribosomal RNA gene from Escherichia coli (1978) Proc. Natl. Acad. Sci. U. S. A., 75, pp. 4801-4805
  • Caetano-Anollés, G., Favelukes, G., Quantitation of adsorption of rhizobia in low numbers to small legume roots (1986) Appl. Environ. Microbiol., 52, pp. 371-376
  • Campbell, G.R., Reuhs, B.L., Walker, G.C., Chronic intracellular infection of alfalfa nodules by Sinorhizobium meliloti requires correct lipopolysaccharide core (2002) Proc. Natl. Acad. Sci. U. S. A., 99, pp. 3938-3943
  • Cepeda, C., Santos, Y., Rapid and low-level toxic PCR-based method for routine identification of Flavobacterium psychrophilum (2000) Int. Microbiol., 3, pp. 235-238
  • Costerton, J.W., Lewandowski, Z., Caldwell, D.E., Korber, D.R., Lappin-Scott, H.M., Microbial biofilms (1995) Annu. Rev. Microbiol., 49, pp. 711-745
  • Denarié, J., Debellé, F., Promé, J.C., Rhizobium lipo-chitooligosaccharide nodulation factors, signaling molecules mediating recognition and morphogenesis (1996) Annu. Rev. Biochem., 65, pp. 503-535
  • Ferguson, G.P., Roop, R.M., Walker, G.C., Deficiency of a Sinorhizobium meliloti bacA mutant in alfalfa symbiosis correlates with alteration of the cell envelope (2002) J. Bacteriol., 184, pp. 5625-5632
  • Finan, T.M., General transduction in Rhizobium meliloti (1984) J. Bacteriol., 159, pp. 120-124
  • Fisher, R.F., Long, S.R., Rhizobium-plant signal exchange (1992) Nature, 357, pp. 655-660
  • Fraysse, N., Couderc, F., Poinsot, V., Surface polysaccharide involvement in establishing the Rhizobium-legume symbiosis (2003) Eur. J. Biochem., 270, pp. 1365-1380
  • 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
  • Fujishige, N.A., Kapadia, N.N., Hirsch, A.M., A feeling for the microorganism, structure on a small scale (2006) Biofilms on plant roots. Bot. J. Linn. Soc., 150, pp. 79-88
  • Fujishige, N.A., Rhizobium common nod genes are required for biofilm formation (2008) Mol. Microbiol., 67, pp. 504-515
  • Galibert, F., The composite genome of the legume symbiont Sinorhizobium meliloti (2001) Science, 293, pp. 668-672
  • Glazebrook, J., Walker, G.C., A novel exopolysaccharide can function in place of the calcofluor-binding exopolysaccharide in nodulation of alfalfa by Rhizobium meliloti (1989) Cell, 56, pp. 661-672
  • Hirsch, A.M., Role of lectins (and rhizobial exopolysaccharides) in legume nodulation (1999) Curr. Opin. Plant Biol., 2, pp. 320-326
  • Hirsch, A.M., Lum, M.R., Fujishige, N.A., Microbial encounters of a symbiotic kind-attaching to roots and other surfaces (2009) Root hairs. Plant cell monographs, 12, pp. 295-314. , In Emons AMC, Ketelaar T (ed). Springer-Verlag, Berlin, Germany
  • Hotter, G.S., Scott, B., Exopolysaccharide mutants of Rhizobium loti are fully effective on a determinate nodulating host but are ineffective on an indeterminate nodulating host (1991) J. Bacteriol., 173, pp. 851-859
  • Jacobs, A., Chenia, H.Y., Biofilm-forming capacity, surface hydrophobicity and aggregation characteristics of Myroides odoratus isolated from South African Oreochromis mossambicus fish (2010) J. Appl. Microbiol., 107, pp. 1957-1966
  • Janczarek, M., Environmental signals and regulatory pathways that influence exopolysaccharide production in rhizobia (2011) Int. J. Mol. Sci., 12, pp. 7898-7933
  • Keller, M., Molecular analysis of the Rhizobium meliloti mucR gene regulating the biosynthesis of the exopolysaccharides succinoglycan and galactoglucan (1995) Mol. Plant Microbe Interact., 8, pp. 267-277
  • Krol, E., Becker, A., Global transcriptional analysis of the phosphate starvation response in Sinorhizobium meliloti strains 1021 and 2011 (2004) Mol. Genet. Genomics, 272, pp. 1-17
  • Lane, D.J., (1991) 16S/23S rRNA sequencing, pp. 115-175. , Stackebrant E, GoodfellowM(ed), Nucleic acid techniques in bacterial systematics John Wiley & Sons, New York, NY
  • Leigh, J.A., Signer, E.R., Walker, G.C., Exopolysaccharide-deficient mutants of Rhizobium meliloti that form ineffective nodules (1985) Proc. Natl. Acad. Sci. U. S. A., 82, pp. 6231-6235
  • Lindström, K., Murwira, M., Willems, A., Altier, N., The biodiversity of beneficial microbe-host mutualism, the case of rhizobia (2010) Res. Microbiol., 161, pp. 453-463
  • Löbler, M., Hirsch, A.M., A gene that encodes a proline-rich nodulin with limited homology to PsENOD12 is expressed in the invasion zone of Rhizobium meliloti-induced alfalfa nodules (1993) Plant Physiol, 103, pp. 21-30
  • McInnes, A., Thies, J.E., Abbott, L.K., Howieson, J.G., Structure and diversity among rhizobial strains, populations and communities-a review (2004) Soil Biol. Biochem., 36, pp. 1295-1308
  • Meade, H., Long, S., Ruvkun, G., Brown, S., Ausubel, F., Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposon Tn5 mutagenesis (1982) J. Bacteriol., 149, pp. 114-122
  • Morris, C.E., Monier, J.M., The ecological significance of biofilm formation by plant-associated bacteria (2003) Annu. Rev. Phytopathol., 41, pp. 429-453
  • Nievas, F., Bogino, P., Nocelli, N., Giordano, W., Genotypic analysis of isolated peanut-nodulating rhizobial strains reveals differences among populations obtained from soils with different cropping histories (2012) Appl. Soil Ecol., 53, pp. 74-82
  • Nikitina, V.E., Ponomareva, E.G., Alen'kina, S.A., Konnova, S.A., The role of cell-surface lectins in the aggregation of Azospirilla (2001) Microbiology, 70, pp. 471-476
  • O'Toole, G.A., Kolter, R., Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways, a genetic analysis (1998) Mol. Microbiol., 28, pp. 449-461
  • Pellock, B.J., Teplitski, M., Boinay, R.P., Bauer, W.D., Walker, G.C., A LuxR homolog controls production of symbiotically active extracellular polysaccharide II by Sinorhizobium meliloti (2002) J. Bacteriol., 184, pp. 5067-5076
  • Reuber, T.L., Walker, G.C., Biosynthesis of succinoglycan, a symbiotically important exopolysaccharide of Rhizobium meliloti (1993) Cell, 74, pp. 269-280
  • Rinaudi, L., Effects of nutritional and environmental conditions on Sinorhizobium meliloti biofilm formation (2006) Res. Microbiol., 157, pp. 867-875
  • Rinaudi, L., Sorroche, F., Zorreguieta, A., Giordano, W., Analysis of mucR gene regulating biosynthesis of exopolysaccharides, implications for biofilm formation in Sinorhizobium meliloti Rm1021 (2010) FEMS Microbiol. Lett., 302, pp. 15-21
  • Rinaudi, L.V., Giordano, W., An integrated view of biofilm formation in rhizobia (2010) FEMS Microbiol. Lett., 304, pp. 1-11
  • Rinaudi, L.V., Gonzalez, J.E., The low-molecular-weight fraction of exopolysaccharide II from Sinorhizobium meliloti is a crucial determinant of biofilm formation (2009) J. Bacteriol., 191, pp. 7216-7224
  • Russo, D.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
  • Saitou, N., Nei, M., The neighbor-joining method, a new method for reconstructing phylogenetic trees (1987) Mol. Biol. Evol., 4, pp. 406-425
  • Santaella, C., Schue, M., Berge, O., Heulin, T., Achouak, W., The exopolysaccharide of Rhizobium sp (2008) YAS34 is not necessary for biofilm formation on Arabidopsis thaliana and Brassica napus roots but contributes to root colonization. Environ. Microbiol., 10, pp. 2150-2163
  • Simon, R., Hötte, B., Klauke, B., Kosier, B., Isolation and characterization of insertion sequence elements from gram-negative bacteria by using new broad-host-range, positive selection vectors (1991) J. Bacteriol., 173, pp. 1502-1508
  • Skorupska, A., Janczarek, M., Marczak, M., Mazur, A., Król, J., Rhizobial exopolysaccharides, genetic control and symbiotic functions (2006) Microb. Cell Fact., 5, p. 7
  • Sorroche, F., Rinaudi, L., Zorreguieta, A., Giordano, W., EPS IIdependent autoaggregation of Sinorhizobium meliloti planktonic cells (2010) Curr. Microbiol., 61, pp. 465-470
  • Spaink, H.P., Root nodulation and infection factors produced by rhizobial bacteria (2000) Annu. Rev. Microbiol., 54, pp. 257-288
  • Stackebrandt, E., Goebel, B.M., Taxonomic note, a place for DNADNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology (1994) Int. J. Syst. Bacteriol., 44, pp. 846-849
  • Streeter, J.G., (1994) Plant-environment interactions symbiotic nitrogen fixation, pp. 245-262. , Wilkinson RE (ed), Marcel Dekker Inc, New York, NY
  • Vincent, J.M., (1970) A manual for the practical study of root-nodule bacteria, , Blackwell Scientific Publications, Oxford, England
  • Wells, D.H., Chen, E.J., Fisher, R.F., Long, S.R., ExoR is genetically coupled to the ExoS-ChvI two-component system and located in the periplasm of Sinorhizobium meliloti (2007) Mol. Microbiol., 64, pp. 647-664
  • Williams, A., Glucomannan-mediated attachment of Rhizobium leguminosarum to pea root hairs is required for competitive nodule infection (2008) J. Bacteriol., 190, pp. 4706-4715
  • Williams, V., Fletcher, M., Pseudomonas fluorescens adhesion and transport through porous media are affected by lipopolysaccharide composition (1996) Appl. Environ. Microbiol., 62, pp. 100-104
  • Zhan, H.J., Lee, C.C., Leigh, J.A., Induction of the second exopolysaccharide (EPSb) in Rhizobium meliloti SU47 by low phosphate concentrations (1991) J. Bacteriol., 173, pp. 7391-7394

Citas:

---------- APA ----------
Sorroche, F.G., Spesia, M.B., Zorreguieta, Á. & Giordano, W. (2012) . A positive correlation between bacterial autoaggregation and biofilm formation in native Sinorhizobium meliloti isolates from Argentina. Applied and Environmental Microbiology, 78(12), 4092-4101.
http://dx.doi.org/10.1128/AEM.07826-11
---------- CHICAGO ----------
Sorroche, F.G., Spesia, M.B., Zorreguieta, Á., Giordano, W. "A positive correlation between bacterial autoaggregation and biofilm formation in native Sinorhizobium meliloti isolates from Argentina" . Applied and Environmental Microbiology 78, no. 12 (2012) : 4092-4101.
http://dx.doi.org/10.1128/AEM.07826-11
---------- MLA ----------
Sorroche, F.G., Spesia, M.B., Zorreguieta, Á., Giordano, W. "A positive correlation between bacterial autoaggregation and biofilm formation in native Sinorhizobium meliloti isolates from Argentina" . Applied and Environmental Microbiology, vol. 78, no. 12, 2012, pp. 4092-4101.
http://dx.doi.org/10.1128/AEM.07826-11
---------- VANCOUVER ----------
Sorroche, F.G., Spesia, M.B., Zorreguieta, Á., Giordano, W. A positive correlation between bacterial autoaggregation and biofilm formation in native Sinorhizobium meliloti isolates from Argentina. Appl. Environ. Microbiol. 2012;78(12):4092-4101.
http://dx.doi.org/10.1128/AEM.07826-11