Artículo

Bonomi, H.R.; Posadas, D.M.; Paris, G.; Del Carmen Carrica, M.; Frederickson, M.; Pietrasanta, L.I.; Bogomolni, R.A.; Zorreguieta, A.; Goldbaum, F.A. "Light regulates attachment, exopolysaccharide production, and nodulation in Rhizobium leguminosarum through a LOV-histidine kinase photoreceptor" (2012) Proceedings of the National Academy of Sciences of the United States of America. 109(30):12135-12140
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Abstract:

Rhizobium leguminosarum is a soil bacterium that infects root hairs and induces the formation of nitrogen-fixing nodules on leguminous plants. Light, oxygen, and voltage (LOV)-domain proteins are bluelight receptors found in higher plants and many algae, fungi, and bacteria. The genome of R. leguminosarum bv. viciae 3841, a peanodulating endosymbiont, encodes a sensor histidine kinase containing a LOV domain at the N-terminal end (R-LOV-HK). R-LOV-HK has a typical LOV domain absorption spectrum with broad bands in the blue and UV-A regions and shows a truncated photocycle. Here we show that the R-LOV-HK protein regulates attachment to an abiotic surface and production of flagellar proteins and exopolysaccharide in response to light. Also, illumination of bacterial cultures before inoculation of pea roots increases the number of nodules per plant and the number of intranodular bacteroids. The effects of light on nodulation are dependent on a functional lov gene. The results presented in this work suggest that light, sensed by R-LOV-HK, is an important environmental factor that controls adaptive responses and the symbiotic efficiency of R. leguminosarum.

Registro:

Documento: Artículo
Título:Light regulates attachment, exopolysaccharide production, and nodulation in Rhizobium leguminosarum through a LOV-histidine kinase photoreceptor
Autor:Bonomi, H.R.; Posadas, D.M.; Paris, G.; Del Carmen Carrica, M.; Frederickson, M.; Pietrasanta, L.I.; Bogomolni, R.A.; Zorreguieta, A.; Goldbaum, F.A.
Filiación:Fundación Instituto Leloir, IIBBA, Consejo Nacional de Investigaciones Científicas Y Técnicas de Argentina, C1405BWE, Buenos Aires, Argentina
Department of Chemistry, University of California, Santa Cruz, CA 95064, United States
Centro de Microscopías Avanzadas, Facultad de Ciencias Exactas Y Naturales (FCEyN), Universidad de Buenos Aires, C1428EHA, Buenos Aires, Argentina
Consejo Nacional de Investigaciones Científicas Y Técnicas de Argentina, C1033AAJ, Buenos Aires, Argentina
Departamento de Química Biológica, FCEyN, Universidad de Buenos Aires, C1428EHA, Buenos Aires, Argentina
Palabras clave:bacterial polysaccharide; bacterial protein; exopolysaccharide; light oxygen and voltage histidine kinase; unclassified drug; adaptation; amino terminal sequence; article; bacterial gene; bacterium culture; biofilm; blue light; environmental factor; illumination; light; lov gene; nodulation; nonhuman; pea; plant root; priority journal; protein synthesis; real time polymerase chain reaction; reverse transcription polymerase chain reaction; Rhizobium leguminosarum; symbiosis; Amino Acid Sequence; Bacterial Adhesion; Base Sequence; Biofilms; Blotting, Western; Flagella; Gentian Violet; Light; Microscopy, Electron, Scanning; Molecular Sequence Data; Peas; Photoreceptors, Microbial; Plant Root Nodulation; Polysaccharides, Bacterial; Protein Kinases; Protein Structure, Tertiary; Real-Time Polymerase Chain Reaction; Rhizobium leguminosarum; Sequence Alignment; Sequence Analysis, DNA; Statistics, Nonparametric; Symbiosis; algae; Bacteria (microorganisms); Embryophyta; Fabaceae; Fungi; Pisum sativum; Rhizobium leguminosarum
Año:2012
Volumen:109
Número:30
Página de inicio:12135
Página de fin:12140
DOI: http://dx.doi.org/10.1073/pnas.1121292109
Título revista:Proceedings of the National Academy of Sciences of the United States of America
Título revista abreviado:Proc. Natl. Acad. Sci. U. S. A.
ISSN:00278424
CODEN:PNASA
CAS:EPSI polysaccharide; Gentian Violet, 548-62-9; Photoreceptors, Microbial; Polysaccharides, Bacterial; Protein Kinases, 2.7.-; protein-histidine kinase, 2.7.3.-
PDF:https://bibliotecadigital.exactas.uba.ar/download/paper/paper_00278424_v109_n30_p12135_Bonomi.pdf
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00278424_v109_n30_p12135_Bonomi

Referencias:

  • Purcell, E.B., Crosson, S., Photoregulation in prokaryotes (2008) Curr Opin Microbiol, 11, pp. 168-178
  • Van Der Horst, M.A., Key, J., Hellingwerf, K.J., Photosensing in chemotrophic, non-phototrophic bacteria: let there be light sensing too (2007) Trends in Microbiology, 15 (12), pp. 554-562. , DOI 10.1016/j.tim.2007.09.009, PII S0966842X07002041
  • Taylor, B.L., Zhulin, I.B., PAS domains: Internal sensors of oxygen, redox potential, and light (1999) Microbiology and Molecular Biology Reviews, 63 (2), pp. 479-506
  • Christie, J.M., Phototropin blue-light receptors (2007) Annu Rev Plant Biol, 58, pp. 21-45
  • Krauss, U., Distribution and phylogeny of light-oxygen-voltage-blue-light-signaling proteins in the three kingdoms of life (2009) J Bacteriol, 191, pp. 7234-7242
  • Swartz, T.E., Tseng, T.-S., Frederickson, M.A., Paris, G., Comerci, D.J., Rajashekara, G., Kim, J.-G., Bogomolni, R.A., Blue-light-activated histidine kinases: Two-component sensors in bacteria (2007) Science, 317 (5841), pp. 1090-1093. , DOI 10.1126/science.1144306
  • Ettema, T.J., Andersson, S.G., The alpha-proteobacteria: The Darwin finches of the bacterial world (2009) Biol Lett, 5, pp. 429-432
  • 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
  • Long, S.R., Genes and signals in the rhizobium-legume symbiosis (2001) Plant Physiol, 125, pp. 69-72
  • Hirsch, A.M., Lum, M.R., Downie, J.A., What makes the Rhizobia-legume symbiosis so special? (2001) Plant Physiology, 127 (4), pp. 1484-1492. , DOI 10.1104/pp.127.4.1484
  • Miller, L.D., Yost, C.K., Hynes, M.F., Alexandre, G., The major chemotaxis gene cluster of Rhizobium leguminosarum bv. viciae is essential for competitive nodulation (2007) Molecular Microbiology, 63 (2), pp. 348-362. , DOI 10.1111/j.1365-2958.2006.05515.x
  • Albareda, M., Factors affecting the attachment of rhizospheric bacteria to bean and soybean roots (2006) FEMS Microbiol Lett, 259, pp. 67-73
  • Skorupska, A., Janczarek, M., Marczak, M., Mazur, A., Król, J., Rhizobial exopolysaccharides: Genetic control and symbiotic functions (2006) Microb Cell Fact, 16, pp. 5-7
  • Russo, D.M., Williams, A., Edwards, A., Posadas, D.M., Finnie, C., Dankert, M., Downie, J.A., Zorreguieta, A., Proteins exported via the PrsD-PrsE type I secretion system and the acidic exopolysaccharide are involved in biofilm formation by Rhizobium leguminosarum (2006) Journal of Bacteriology, 188 (12), pp. 4474-4486. , DOI 10.1128/JB.00246-06
  • 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) Journal of Bacteriology, 190 (13), pp. 4706-4715. , DOI 10.1128/JB.01694-07
  • Karniol, B., Vierstra, R.D., The HWE Histidine Kinases, a New Family of Bacterial Two-Component Sensor Kinases with Potentially Diverse Roles in Environmental Signaling (2004) Journal of Bacteriology, 186 (2), pp. 445-453. , DOI 10.1128/JB.186.2.445-453.2004
  • Harper, S.M., Neil, L.C., Gardner, K.H., Structural basis of a phototropin light switch (2003) Science, 301 (5639), pp. 1541-1544. , DOI 10.1126/science.1086810
  • Grebe, T.W., Stock, J.B., The histidine protein kinase superfamily (1999) Advances in Microbial Physiology, 41, pp. 139-227
  • Swartz, T.E., The photocycle of a flavin-binding domain of the blue light photoreceptor phototropin (2001) J Biol Chem, 276, pp. 36493-36500
  • Losi, A., Gärtner, W., Bacterial bilin- and flavin-binding photoreceptors (2008) Photochem Photobiol Sci, 7, pp. 1168-1178
  • Imaizumi, T., Tran, H.G., Swartz, T.E., Briggs, W.R., Kay, S.A., FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis (2003) Nature, 426 (6964), pp. 302-306. , DOI 10.1038/nature02090
  • Kottke, T., Heberle, J., Hehn, D., Dick, B., Hegemannt, P., Phot-LOV1: Photocycle of a blue-light receptor domain from the green alga Chlamydomonas reinhardtii (2003) Biophysical Journal, 84 (2 I), pp. 1192-1201
  • Alexandre, M.T.A., Arents, J.C., Van Grondelle, R., Hellingwerf, K.J., Kennis, J.T.M., A base-catalyzed mechanism for dark state recovery in the Avena sativa phototropin-1 LOV2 domain (2007) Biochemistry, 46 (11), pp. 3129-3137. , DOI 10.1021/bi062074e
  • Karatan, E., Watnick, P., Signals, regulatory networks, and materials that build and break bacterial biofilms (2009) Microbiol Mol Biol Rev, 73, pp. 310-347
  • Purcell, E.B., Siegal-Gaskins, D., Rawling, D.C., Fiebig, A., Crosson, S., A photosensory two-component system regulates bacterial cell attachment (2007) Proceedings of the National Academy of Sciences of the United States of America, 104 (46), pp. 18241-18246. , http://www.pnas.org/cgi/reprint/104/46/18241, DOI 10.1073/pnas.0705887104
  • Klausen, M., Heydorn, A., Ragas, P., Lambertsen, L., Aaes-Jorgensen, A., Molin, S., Tolker-Nielsen, T., Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants (2003) Molecular Microbiology, 48 (6), pp. 1511-1524. , DOI 10.1046/j.1365-2958.2003.03525.x
  • O'Toole, G.A., Kolter, R., Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development (1998) Molecular Microbiology, 30 (2), pp. 295-304. , DOI 10.1046/j.1365-2958.1998.01062.x
  • Miller, L.D., Russell, M.H., Alexandre, G., Diversity in bacterial chemotactic responses and niche adaptation (2009) Adv Appl Microbiol, 66, pp. 53-75
  • 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
  • Tambalo, D.D., Characterization and functional analysis of seven flagellin genes in Rhizobium leguminosarum bv. viciae. Characterization of R. leguminosarum flagellins (2010) BMC Microbiol, 10, p. 219
  • Oberpichler, I., Light affects motility and infectivity of Agrobacterium tumefaciens (2008) Environ Microbiol, 10, pp. 2020-2029
  • 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
  • Belas, R., Simon, M., Silverman, M., Regulation of lateral flagella gene transcription in Vibrio parahaemolyticus (1986) Journal of Bacteriology, 167 (1), pp. 210-218
  • McCarter, L.L., Dual flagellar systems enable motility under different circumstances (2004) J Mol Microbiol Biotechnol, 7, pp. 18-29
  • Kanbe, M., Yagasaki, J., Zehner, S., Gottfert, M., Aizawa, S.-I., Characterization of two sets of subpolar flagella in Bradyrhizobium japonicum (2007) Journal of Bacteriology, 189 (3), pp. 1083-1089. , DOI 10.1128/JB.01405-06
  • Armitage, J.P., Gallagher, A., Johnston, A.W., Comparison of the chemotactic behaviour of Rhizobium leguminosarum with and without the nodulation plasmid (1988) Mol Microbiol, 2, pp. 743-748
  • Barbour, W.M., Hattermann, D.R., Stacey, G., Chemotaxis of Bradyrhizobium japonicum to soybean exudates (1991) Appl Environ Microbiol, 57, pp. 2635-2639
  • Crespi, M., Gálvez, S., Molecular mechanisms in root nodule development (2000) J Plant Growth Regul, 19, pp. 155-166
  • Rinaudi, L., Fujishige, N.A., Hirsch, A.M., Banchio, E., Zorreguieta, A., Giordano, W., Effects of nutritional and environmental conditions on Sinorhizobium meliloti biofilm formation (2006) Research in Microbiology, 157 (9), pp. 867-875. , DOI 10.1016/j.resmic.2006.06.002, PII S0923250806001264
  • Borthakur, D., Johnston, A.W.B., Sequence of psi, a gene on the symbiotic plasmid of Rhizobium phaseoli which inhibits exopolysaccharide synthesis and nodulation and demonstration that its transcription is inhibited by psr, another gene on the symbiotic plasmid (1987) Molecular and General Genetics, 207 (1), pp. 149-154. , DOI 10.1007/BF00331502
  • Latchford, J.W., Borthakur, D., Johnston, A.W.B., The products of Rhizobium genes, psi and pss, which affect exopolysaccharide production, are associated with the bacterial cell surface (1991) Molecular Microbiology, 5 (9), pp. 2107-2114
  • Bittinger, M.A., Handelsman, J., Identification of genes in the RosR regulon of Rhizobium etli (2000) Journal of Bacteriology, 182 (6), pp. 1706-1713. , DOI 10.1128/JB.182.6.1706-1713.2000
  • Gage, D.J., Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes (2004) Microbiol Mol Biol Rev, 68, pp. 280-300
  • Chandra-Shekara, A.C., Gupte, M., Navarre, D., Raina, S., Raina, R., Klessig, D., Kachroo, P., Light-dependent hypersensitive response and resistance signaling against Turnip Crinkle Virus in Arabidopsis (2006) Plant Journal, 45 (3), pp. 320-334. , DOI 10.1111/j.1365-313X.2005.02618.x
  • Fraysse, N., Couderc, F., Poinsot, V., Surface polysaccharide involvement in establishing the rhizobium-legume symbiosis (2003) European Journal of Biochemistry, 270 (7), pp. 1365-1380. , DOI 10.1046/j.1432-1033.2003.03492.x
  • Gibson, K.E., Kobayashi, H., Walker, G.C., Molecular determinants of a symbiotic chronic infection (2008) Annu Rev Genet, 42, pp. 413-441

Citas:

---------- APA ----------
Bonomi, H.R., Posadas, D.M., Paris, G., Del Carmen Carrica, M., Frederickson, M., Pietrasanta, L.I., Bogomolni, R.A.,..., Goldbaum, F.A. (2012) . Light regulates attachment, exopolysaccharide production, and nodulation in Rhizobium leguminosarum through a LOV-histidine kinase photoreceptor. Proceedings of the National Academy of Sciences of the United States of America, 109(30), 12135-12140.
http://dx.doi.org/10.1073/pnas.1121292109
---------- CHICAGO ----------
Bonomi, H.R., Posadas, D.M., Paris, G., Del Carmen Carrica, M., Frederickson, M., Pietrasanta, L.I., et al. "Light regulates attachment, exopolysaccharide production, and nodulation in Rhizobium leguminosarum through a LOV-histidine kinase photoreceptor" . Proceedings of the National Academy of Sciences of the United States of America 109, no. 30 (2012) : 12135-12140.
http://dx.doi.org/10.1073/pnas.1121292109
---------- MLA ----------
Bonomi, H.R., Posadas, D.M., Paris, G., Del Carmen Carrica, M., Frederickson, M., Pietrasanta, L.I., et al. "Light regulates attachment, exopolysaccharide production, and nodulation in Rhizobium leguminosarum through a LOV-histidine kinase photoreceptor" . Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 30, 2012, pp. 12135-12140.
http://dx.doi.org/10.1073/pnas.1121292109
---------- VANCOUVER ----------
Bonomi, H.R., Posadas, D.M., Paris, G., Del Carmen Carrica, M., Frederickson, M., Pietrasanta, L.I., et al. Light regulates attachment, exopolysaccharide production, and nodulation in Rhizobium leguminosarum through a LOV-histidine kinase photoreceptor. Proc. Natl. Acad. Sci. U. S. A. 2012;109(30):12135-12140.
http://dx.doi.org/10.1073/pnas.1121292109