Archives of Microbiology

, Volume 199, Issue 5, pp 737–755 | Cite as

The naringenin-induced exoproteome of Rhizobium etli CE3

  • Niurka Meneses
  • Hermenegildo Taboada
  • Michael F. Dunn
  • María del Carmen Vargas
  • Natasha Buchs
  • Manfred Heller
  • Sergio Encarnación
Original Paper


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.


Rhizobium 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.

Supplementary material

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Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Programa de Genómica Funcional de Procariotes, Centro de Ciencias GenómicasUniversidad Nacional Autónoma de MéxicoCuernavacaMexico
  2. 2.Mass Spectrometry and Proteomics Laboratory, Department of Clinical ResearchUniversity of BernBernSwitzerland
  3. 3.Faculty of Science, Department of Chemistry and BiochemistryUniversity of BernBernSwitzerland

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