Qualitative changes in proteins contained in outer membrane vesicles produced by Rhizobium etli grown in the presence of

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ORIGINAL PAPER

Qualitative changes in proteins contained in outer membrane vesicles produced by Rhizobium etli grown in the presence of the nod gene inducer naringenin Hermenegildo Taboada1 · Michael F. Dunn1 · Niurka Meneses1,2,3 · Carmen Vargas‑Lagunas1 · Natasha Buchs2 · Andrés Andrade‑Domínguez1,4 · Sergio Encarnación1  Received: 25 January 2019 / Revised: 22 April 2019 / Accepted: 21 May 2019 © Springer-Verlag GmbH Germany, part of Springer Nature 2019

Abstract In this work, we compared the proteomic profiles of outer membrane vesicles (OMVs) isolated from Rhizobium etli CE3 grown in minimal medium (MM) with and without exogenous naringenin. One-hundred and seven proteins were present only in OMVs from naringenin-containing cultures (N-OMVs), 57 proteins were unique to OMVs from control cultures lacking naringenin (C-OMVs) and 303 proteins were present in OMVs from both culture conditions (S-OMVs). Although we found no absolute predominance of specific types of proteins in the N-, C- or S-OMV classes, there were categories of proteins that were significantly less or more common in the different OMV categories. Proteins for energy production, translation and membrane and cell wall biogenesis were overrepresented in C-OMVs relative to N-OMVs. Proteins for carbohydrate metabolism and transport and those classified as either general function prediction only, function unknown, or without functional prediction were more common in N-OMVs than C-OMVs. This indicates that naringenin increased the proportion of these proteins in the OMVs, although NodD binding sites were only slightly more common in the promoters of genes for proteins found in the N-OMVs. In addition, OMVs from naringenin-containing cultures contained nodulation factor. Keywords  Protein secretion · Exoproteome · Naringenin · Nodulation factors · Outer membrane vesicles · Rhizobiumlegume symbiosis Communicated by Erko Stackebrandt. Hermenegildo Taboada and Michael F. Dunn contributed equally to this work. Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s0020​3-019-01682​-4) contains supplementary material, which is available to authorized users. * Sergio Encarnación [email protected] 1



Programa de Genómica Funcional de Procariotes, Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México, C. P. 62210 Cuernavaca, Morelos, México

2



Mass Spectrometry and Proteomics Laboratory, Department of Clinical Research, University of Bern, 3010 Bern, Switzerland

3

Faculty of Science, Department of Chemistry and Biochemistry, University of Bern, 3010 Bern, Switzerland

4

Noxgen Biotech, Centro Novatec, Palmas No. 1, Fracc. Lomas de Cocoyoc, C.P. 62847 Atlatlahucan, Morelos, México





Introduction Several genera of alpha- and beta-proteobacteria establish endosymbioses with compatible (principally leguminous) plants. These bacteria are collectively referred to as rhizobia. Rhizobia that reside within plant cells of nodules formed on the roots of the host plant are called bacteroids. The b