The naringenin-induced exoproteome of Rhizobium etli CE3
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Flavonoids excreted by legume roots induce the expression of symbiotically essential nodulation (nod) genes in rhizobia, as well as that of specific protein export systems. In the bean microsymbiont Rhizobium etli CE3, nod genes are induced by the flavonoid naringenin. In this study, we identified 693 proteins in the exoproteome of strain CE3 grown in minimal medium with or without naringenin, with 101 and 100 exoproteins being exclusive to these conditions, respectively. Four hundred ninety-two (71%) of the extracellular proteins were found in both cultures. Of the total exoproteins identified, nearly 35% were also present in the intracellular proteome of R. etli bacteroids, 27% had N-terminal signal sequences and a significant number had previously demonstrated or possible novel roles in symbiosis, including bacterial cell surface modification, adhesins, proteins classified as MAMPs (microbe-associated molecular patterns), such as flagellin and EF-Tu, and several normally cytoplasmic proteins as Ndk and glycolytic enzymes, which are known to have extracellular “moonlighting” roles in bacteria that interact with eukaryotic cells. It is noteworthy that the transmembrane ß (1,2) glucan biosynthesis protein NdvB, an essential symbiotic protein in rhizobia, was found in the R. etli naringenin-induced exoproteome. In addition, potential binding sites for two nod-gene transcriptional regulators (NodD) occurred somewhat more frequently in the promoters of genes encoding naringenin-induced exoproteins in comparison to those ofexoproteins found in the control condition.
KeywordsRhizobium Nitrogen Fixation Proteomics Naringenin
Part of this work was supported by CONACyT Grant 220790 and DGAPA-PAPIIT Grant IN213216. Thanks to Jaime A. Castro Mondragón for contributing to the Dyad analysis and Omar Alejandro Aguilar for bioinformatics assistance. The authors would like to thank the anonymous reviewers for their valuable comments and suggestions to improve the quality of the review.
- Chagnot C, Zorgani MA, Astruc T, Desvaux M (2013) Proteinaceous determinants of surface colonization in bacteria: bacterial adhesion and biofilm formation from a protein secretion perspective. Front Microbiol 4:303. doi: 10.3389/fmicb.2013.00303
- Dunn MF, Araíza G, Encarnación S et al (2002) Effect of aniA (Carbon Flux Regulator) and and phaC (poly-beta-hydroxybutirate synthase) mutations on Pyruvate Metabolism in Rhizobium etli 1–5. doi: 10.1128/JB.184.8.2296-2299.2002.
- Foreman DL, Vanderlinde EM, Bay DC, Yost CK (2010) Characterization of a gene family of outer membrane proteins (ropB) in Rhizobium leguminosarum bv. viciae VF39SM and the role of the sensor kinase ChvG in their regulation. J Bacteriol 192:975–983. doi: 10.1128/JB.01140-09 CrossRefPubMedGoogle Scholar
- Gay-Fraret J, Ardissone S, Kambara K et al (2012) Cyclic-β-glucans of Rhizobium (Sinorhizobium) sp. strain NGR234 are required for hypo-osmotic adaptation, motility, and efficient symbiosis with host plants. FEMS Microbiol Lett 333:28–36. doi: 10.1111/j.1574-6968.2012.02595.x CrossRefPubMedGoogle Scholar
- Gazi AD, Sarris PF, Fadouloglou VE et al (2012) Phylogenetic analysis of a gene cluster encoding an additional, rhizobial-like type III secretion system that is narrowly distributed among Pseudomonas syringae strains. BMC Microbiol 12:188. doi: 10.1186/1471-2180-12-188 CrossRefPubMedPubMedCentralGoogle Scholar
- Jain S, Kumar S, Dohre S et al (2014) Identification of a protective protein from stationary-phase exoproteome of Brucella abortus. Pathog Dis 70:75–83. doi: 10.1111/2049-632X.12079
- Jiang G, Krishnan AH, Kim YW et al (2001) A functional myo-inositol dehydrogenase gene is required for efficient nitrogen fixation and competitiveness of Sinorhizobium fredii USDA191 to nodulate soybean (Glycine max [L.] Merr.). J Bacteriol 183:2595–2604. doi: 10.1128/JB.183.8.2595-2604.2001 CrossRefPubMedPubMedCentralGoogle Scholar
- Krishnan HB, Lorio J, Kim WS et al (2003) Extracellular proteins involved in soybean cultivar-specific nodulation are associated with pilus-like surface appendages and exported by a type III protein secretion system in Sinorhizobium fredii USDA257. Mol Plant Microbe Interact 16:617–625. doi: 10.1094/MPMI.2003.16.7.617 CrossRefPubMedGoogle Scholar
- Król JE, Mazur A, Marczak M, Skorupska A (2006) Syntenic arrangements of the surface polysaccharide biosynthesis genes in Rhizobium leguminosarum. doi: 10.1016/j.ygeno.2006.08.015
- Pappas KM, Cevallos MA (2011) Plasmids of the Rhizobiaceae and Their Role in Interbacterial and Transkingdom Interactions. In: Witzany G (ed) Biocommunication in soil microorganisms, soil biology 23. Berlin Heidelberg, pp 295–338Google Scholar
- Pérez-Montaño F, del Cerro P, Jiménez-Guerrero I et al (2016a) RNA-seq analysis of the Rhizobium tropici CIAT 899 transcriptome shows similarities in the activation patterns of symbiotic genes in the presence of apigenin and salt. BMC Genomics 17:1–11. doi: 10.1186/s12864-016-2543-3 CrossRefGoogle Scholar
- Pérez-Montaño F, Jiménez-Guerrero I, Acosta-Jurado S, et al (2016b) A transcriptomic analysis of the effect of genistein on Sinorhizobium fredii HH103 reveals novel rhizobial genes putatively involved in symbiosis. Sci Rep 6:31592. doi: 10.1038/srep31592
- Sadovskaya I, Vinogradov E, Li J et al (2010) High-level antibiotic resistance in Pseudomonas aeruginosa biofilm: the ndvB gene is involved in the production of highly glycerol-phosphorylated—(1→3)-glucans, which bind aminoglycosides. Glycobiology 20:895–904. doi: 10.1093/glycob/cwq047 CrossRefPubMedGoogle Scholar
- Silva WM, Seyffert N, Santos A V et al (2013) Identification of 11 new exoproteins in Corynebacterium pseudotuberculosis by comparative analysis of the exoproteome. doi: 10.1016/j.micpath.2013.05.004
- von Tils D, Blädel I, Schmidt MA, Heusipp G (2012) Type II secretion in Yersinia-a secretion system for pathogenicity and environmental fitness. Front Cell Infect Microbiol 2:160. doi: 10.3389/fcimb.2012.00160
- Ye Zhang MS (2013) The roles of malic ensymes in Rhizobium carbon metabolism. McMaster University, Hamilton, OntarioGoogle Scholar