Abstract
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.
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Acosta-Jurado SS, Navarro-Gómez P, Murdoch PDS et al (2016) Exopolysaccharide production by Sinorhizobium fredii HH103 is repressed by genistein in a NodD1-dependent manner. PLoS One 11:1–16. doi:10.1371/journal.pone.0160499
Afroz A, Zahur M, Zeeshan N, Komatsu S (2013) Plant-bacterium interactions analyzed by proteomics. Front Plant Sci 4:21. doi:10.3389/fpls.2013.00021
Ardissone S, Noel KD, Klement M et al (2011) Synthesis of the flavonoid-induced lipopolysaccharide of Rhizobium Sp. strain NGR234 requires rhamnosyl transferases encoded by genes rgpF and wbgA. Mol Plant Microbe Interact 24:1513–1521. doi:10.1094/MPMI-05-11-0143
Arrigoni G, Tolin S, Moscatiello R et al (2013) Calcium-dependent regulation of genes for plant nodulation in Rhizobium leguminosarum detected by iTRAQ quantitative proteomic analysis. J Proteome Res 12:5323–5330. doi:10.1021/pr400656g
Aslam SN, Erbs G, Morrissey KL et al (2009) Microbe-associated molecular pattern (MAMP) signatures, synergy, size and charge: Influences on perception or mobility and host defence responses. Mol Plant Pathol 10:375–387. doi:10.1111/j.1364-3703.2009.00537.x
Bittinger M a., Handelsman J (2000) Identification of genes in the RosR regulon of Rhizobium etli. J Bacteriol 182:1706–1713. doi:10.1128/JB.182.6.1706-1713.2000
Breedveld MW, Miller KJ (1994) Cyclic beta-glucans of members of the family Rhizobiaceae. Microbiol Rev 58:145–161
Broughton WJ, Hanin M, Relic B et al (2006) Flavonoid-inducible modifications to rhamnan O antigens are necessary for Rhizobium sp. strain NGR234-legume symbioses. J Bacteriol 188:3654–3663. doi:10.1128/JB.188.10.3654-3663.2006
Cafardi V, Biagini M, Martinelli M et al (2013) Identification of a novel zinc metalloprotease through a global analysis of Clostridium difficile extracellular proteins. PLoS One 8:1–14. doi:10.1371/journal.pone.0081306
Campbell GRO, Sharypova LA, Scheidle H et al (2003) Striking complexity of lipopolysaccharide defects in a collection of Sinorhizobium meliloti mutants. J Bacteriol 185:3853–3862
Cao Y, Tanaka K, Nguyen CT, Stacey G (2014) Extracellular ATP is a central signaling molecule in plant stress responses. Curr Opin Plant Biol 20:82–87. doi:10.1016/j.pbi.2014.04.009
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
Cosme AM, Becker A, Santos MR et al (2008) The outer membrane protein TolC from Sinorhizobium meliloti affects protein secretion, polysaccharide biosynthesis, antimicrobial resistance, and symbiosis. Mol Plant Microbe Interact 21:947–957. doi:10.1094/MPMI-21-7-0947
Crespo-Rivas JC, Margaret I, Hidalgo A et al (2009) Sinorhizobium fredii HH103 cgs mutants are unable to nodulate determinate- and indeterminate nodule-forming legumes and overproduce an altered EPS. Mol Plant Microbe Interact 22:575–588. doi:10.1094/MPMI-22-5-0575
Dar HH, Prasad D, Varshney GC, Chakraborti PK (2011) Secretory nucleoside diphosphate kinases from both intra- and extracellular pathogenic bacteria are functionally indistinguishable. Microbiology 157:3024–3035. doi:10.1099/mic.0.049221-0
Deakin WJ, Broughton WJ (2009) Symbiotic use of pathogenic strategies: rhizobial protein secretion systems. Nat Rev Microbiol 7:312–320. doi:10.1038/nrmicro2091
Defeu Soufo HJ, Reimold C, Linne U et al (2010) Bacterial translation elongation factor EF-Tu interacts and colocalizes with actin-like MreB protein. Proc Natl Acad Sci U S A 107:3163–3168. doi:10.1073/pnas.0911979107
Dou D, Zhou J-MM (2012) Phytopathogen effectors subverting host immunity: Different foes, similar battleground. Cell Host Microbe 12:484–495. doi:10.1016/j.chom.2012.09.003
Downie JA (2010) The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots. FEMS Microbiol Rev 34:150–170. doi:10.1111/j.1574-6976.2009.00205.x
Driscoll BT, Finan TM (1996) NADP+-dependent malic enzyme of Rhizobium meliloti. J Bacteriol 178:2224–2231
Dunn MF (1998) Tricarboxylic acid cycle and anaplerotic enzymes in rhizobia. FEMS Microbiol Rev 22:105–123
Dunn MF (2015) Key roles of microsymbiont amino acid metabolism in rhizobia-legume interactions. Crit Rev Microbiol 41:411–451. doi:10.3109/1040841X.2013.856854
Dunn MF, Pueppke SG, Krishnan HB (1992) The nod gene inducer genistein alters the composition and molecular mass distribution of extracellular polysaccharides produced by Rhizobium fredii USDA193. FEMS Microbiol Lett 97:107–112. doi:10.1016/0378-1097(92)90372-U
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.
Emerich DW, Krishnan HB (2014) Symbiosomes: temporary moonlighting organelles. Biochem J 460:1–11. doi:10.1042/BJ20130271
Encarnación S, Dunn M, Willms K et al (1995) Fermentative and aerobic metabolism in Rhizobium etli. J Bacteriol 177:3058–3066
Encarnación S, Del Carmen Vargas M, Dunn MF et al (2002) Ania regulates reserve polymer accumulation and global protein expression in Rhizobium etli. J Bacteriol 184:2287–2295. doi:10.1128/JB.184.8.2287-2295.2002
Encarnación S, Guzmán Y, Dunn MF et al (2003) Proteome analysis of aerobic and fermentative metabolism in Rhizobium etli CE3. Proteomics 3:1077–1085. doi:10.1002/pmic.200300427
Fauvart M, Michiels J (2008) Rhizobial secreted proteins as determinants of host specificity in the rhizobium-legume symbiosis. FEMS Microbiol Lett 285:1–9. doi:10.1111/j.1574-6968.2008.01254.x
Feng J, Li Q, Hu HL et al (2003) Inactivation of the nod box distal half-site allows tetrameric NodD to activate nodA transcription in an inducer-independent manner. Nucleic Acids Res 31:3143–3156. doi:10.1093/nar/gkg411
Fiebig A, Herrou J, Willett J, Crosson S (2015) General stress signaling in the alphaproteobacteria. Annu Rev Genet 49:603–625. doi:10.1146/annurev-genet-112414-054813
Finnie C, Hartley NM, Findlay KC, Downie J a (1997) The Rhizobium leguminosarum prsDE genes are required for secretion of several proteins, some of which influence nodulation, symbiotic nitrogen fixation and exopolysaccharide modification. Mol Microbiol 25:135–146
Finnie C, Zorreguieta A, Hartley NM, Downie JA (1998) Characterization of Rhizobium leguminosarum exopolysaccharide glycanases that are secreted via a type I exporter and have a novel heptapeptide repeat motif. J Bacteriol 180:1691–1699
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
Fry J, Wood M, Poole PS (2001) Investigation of myo-inositol catabolism in Rhizobium leguminosarum bv. viciae and its effect on nodulation competitiveness. Mol Plant Microbe Interact 14:1016–1025. doi:10.1094/MPMI.2001.14.8.1016
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
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
Gohar M, Gilois N, Graveline R et al (2005) A comparative study of Bacillus cereus, Bacillus thuringiensis and Bacillus anthracis extracellular proteomes. Proteomics 5:3696–3711. doi:10.1002/pmic.200401225
Gómez-Gómez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5:1003–1011
González V, Santamaría RI, Bustos P et al (2006) The partitioned Rhizobium etli genome: genetic and metabolic redundancy in seven interacting replicons. Proc Natl Acad Sci USA 103:3834–3839. doi:10.1073/pnas.0508502103
González-Pasayo R, Martínez-Romero E (2000) Multiresistance genes of Rhizobium etli CFN42. Mol Plant Microbe Interact 13:572–577. doi:10.1094/MPMI.2000.13.5.572
Guerreiro N, Redmond JW, Rolfe BG, Djordjevic M a (1997) New Rhizobium leguminosarum flavonoid-induced proteins revealed by proteome analysis of differentially displayed proteins. Mol Plant Microbe Interact 10:506–516. doi:10.1094/MPMI.1997.10.4.506
Gunasekera K, Wüthrich D, Braga-Lagache S et al (2012) Proteome remodelling during development from blood to insect-form Trypanosoma brucei quantified by SILAC and mass spectrometry. BMC Genomics 13:556. doi:10.1186/1471-2164-13-556
Hansmeier N, Chao TC, Kalinowski J et al (2006) Mapping and comprehensive analysis of the extracellular and cell surface proteome of the human pathogen Corynebacterium diphtheriae. Proteomics 6:2465–2476. doi:10.1002/pmic.200500360
Hempel J, Zehner S, Göttfert M, Patschkowski T (2009) Analysis of the secretome of the soybean symbiont Bradyrhizobium japonicum. J Biotechnol 140:51–58. doi:10.1016/j.jbiotec.2008.11.002
Henderson B, Martin A (2011) Bacterial Virulence in the Moonlight: Multitasking Bacterial Moonlighting Proteins Are Virulence Determinants in Infectious Disease. Infect Immun 79:3476–3491. doi:10.1128/IAI.00179-11
Horváth I, Multhoff G, Sonnleitner A, Vígh L (2008) Membrane-associated stress proteins: more than simply chaperones. Biochim Biophys Acta 1778:1653–1664. doi:10.1016/j.bbamem.2008.02.012
Ingram-Smith C, Miller KJ (1998) Effects of ionic and osmotic strength on the glucosyltransferase of Rhizobium meliloti responsible for cyclic beta-(1,2)-glucan biosynthesis. Appl Environ Microbiol 64:1290–1297
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
Janczarek M (2011) Environmental signals and regulatory pathways that influence exopolysaccharide production in rhizobia. Int J Mol Sci 12:7898–7933. doi:10.3390/ijms12117898
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
Johnsen HR, Krause K (2014) Cellulase activity screening using pure carboxymethylcellulose: application to soluble cellulolytic samples and to plant tissue prints. Int J Mol Sci 15:830–838. doi:10.3390/ijms15010830
Kamath S, Chen ML, Chakrabarty AM (2000) Secretion of nucleoside diphosphate kinase by mucoid Pseudomonas aeruginosa 8821: involvement of a carboxy-terminal motif in secretion. J Bacteriol 182:3826–3831
Kazemi-Pour N, Condemine G, Hugouvieux-Cotte-Pattat N (2004) The secretome of the plant pathogenic bacterium Erwinia chrysanthemi. Proteomics 4:3177–3186. doi:10.1002/pmic.200300814
Krehenbrink M, Downie JA (2008) Identification of protein secretion systems and novel secreted proteins in Rhizobium leguminosarum bv. viciae. BMC Genomics 9:55. doi:10.1186/1471-2164-9-55
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
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
López-Baena FJ, Ruiz-Sainz JE, Rodríguez-Carvajal MA, Vinardell JM (2016) Bacterial Molecular Signals in the Sinorhizobium fredii-Soybean Symbiosis. Int J Mol Sci 17:755. doi:10.3390/ijms17050755
Mastronunzio JE, Huang Y, Benson DR (2009) Diminished exoproteome of Frankia spp. in culture and symbiosis. Appl Environ Microbiol 75:6721–6728. doi:10.1128/AEM.01559-09
Mateos PF, Jimenez-Zurdo JI, Chen J et al (1992) Cell-associated pectinolytic and cellulolytic enzymes in Rhizobium leguminosarum biovar trifolii. Appl Environ Microbiol 58:1816–1822
Mawuenyega KG, Forst CV, Dobos KM et al (2005) Mycobacterium tuberculosis functional network analysis by global subcellular protein profiling. Mol Biol Cell 16:396–404. doi:10.1091/mbc.E04-04-0329
McBroom AJ, Kuehn MJ (2007) Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response. Mol Microbiol 63:545–558. doi:10.1111/j.1365-2958.2006.05522.x
Medina-Rivera A, Abreu-Goodger C, Thomas-Chollier M et al (2011) Theoretical and empirical quality assessment of transcription factor-binding motifs. Nucleic Acids Res 39:808–824. doi:10.1093/nar/gkq710
Meneses N, Mendoza-Hernández G, Encarnación S (2010) The extracellular proteome of Rhizobium etli CE3 in exponential and stationary growth phase. Proteome Sci 8:51. doi:10.1186/1477-5956-8-51
Mongiardini EJ, Ausmees N, Pérez-Giménez J et al (2008) The rhizobial adhesion protein RapA1 is involved in adsorption of rhizobia to plant roots but not in nodulation. FEMS Microbiol Ecol 65:279–288. doi:10.1111/j.1574-6941.2008.00467.x
Morales VM, Martinez-Molina E, Hubbell DH (1984) Cellulase production by Rhizobium. Plant Soil 80:407–415
Pacheco LGC, Slade SE, Seyffert N et al (2011) A combined approach for comparative exoproteome analysis of Corynebacterium pseudotuberculosis. BMC Microbiol 11:12. doi:10.1186/1471-2180-11-12
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 295–338
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
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
Peterson JB, LaRue TA (1982) Soluble aldehyde dehydrogenase and metabolism of aldehydes by soybean bacteroids. J Bacteriol 151:1473–1484
Pickering BS, Yudistira H, Oresnik IJ (2012) Characterization of the twin-arginine transport secretome in Sinorhizobium meliloti and evidence for host-dependent phenotypes. Appl Environ Microbiol 78:7141–7144. doi:10.1128/AEM.01458-12
Poupot R, Martinez-Romero E, Gautier N, Promé JC (1995) Wild type Rhizobium etli, a bean symbiont, produces acetylfucosylated, N-methylated, and carbamoylated nodulation factors. J Biol Chem 270:6050–6055
Prell J, White JP, Bourdes A et al (2009) Legumes regulate Rhizobium bacteroid development and persistence by the supply of branched-chain amino acids. Proc Natl Acad Sci USA 106:12477–12482. doi:10.1073/pnas.0903653106
Rath P, Huang C, Wang TT et al (2013) Genetic regulation of vesiculogenesis and immunomodulation in Mycobacterium tuberculosis. Proc Natl Acad Sci USA 110:E4790–E4797. doi:10.1073/pnas.1320118110
Resendis-Antonio O, Hernández M, Salazar E et al (2011) Systems biology of bacterial nitrogen fixation: high-throughput technology and its integrative description with constraint-based modeling. BMC Syst Biol 5:120. doi:10.1186/1752-0509-5-120
Rogel MA, Ormeño-Orrillo E, Martinez Romero E (2011) Symbiovars in rhizobia reflect bacterial adaptation to legumes. Syst Appl Microbiol 34:96–104. doi:10.1016/j.syapm.2010.11.015
Russo DM, Williams A, Edwards A et al (2006) Proteins exported via the PrsD-PrsE type I secretion system and the acidic exopolysaccharide are involved in biofilm formation by Rhizobium leguminosarum. J Bacteriol 188:4474–4486. doi:10.1128/JB.00246-06
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
Sánchez B, Urdaci MC, Margolles A (2010) Extracellular proteins secreted by probiotic bacteria as mediators of effects that promote mucosa-bacteria interactions. Microbiology 156:3232–3242. doi:10.1099/mic.0.044057-0
Sarma AD, Emerich DW (2006) A comparative proteomic evaluation of culture grown vs nodule isolated Bradyrhizobium japonicum. Proteomics 6:3008–3028. doi:10.1002/pmic.200500783
Silipo A, Molinaro A, Sturiale L et al (2005) The elicitation of plant innate immunity by lipooligosaccharide of Xanthomonas campestris. J Biol Chem 280:33660–33668. doi:10.1074/jbc.M506254200
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
Da Silva Batista JS, Hungria M (2012) Proteomics reveals differential expression of proteins related to a variety of metabolic pathways by genistein-induced Bradyrhizobium japonicum strains. J Proteomics 75:1211–1219. doi:10.1016/j.jprot.2011.10.032
Simsek S, Ojanen-Reuhs T, Marie C, Reuhs BL (2009) An apigenin-induced decrease in K-antigen production by Sinorhizobium sp. NGR234 is 4gM- and nodD1-dependent. Carbohydr Res 344:1947–1950. doi:10.1016/j.carres.2009.07.006
Song YC, Jin S, Louie H et al (2004) FlaC, a protein of Campylobacter jejuni TGH9011 (ATCC43431) secreted through the flagellar apparatus, binds epithelial cells and influences cell invasion. Mol Microbiol 53:541–553. doi:10.1111/j.1365-2958.2004.04175.x
Soto MJ, Sanjuán J, Olivares J (2006) Rhizobia and plant-pathogenic bacteria: common infection weapons. Microbiology 152:3167–3174. doi:10.1099/mic.0.29112-00
Soto MJ, Domínguez-Ferreras A, Pérez-Mendoza D et al (2009) Mutualism versus pathogenesis: the give-and-take in plant-bacteria interactions. Cell Microbiol 11:381–388. doi:10.1111/j.1462-5822.2008.01282.x
Süss C, Hempel J, Zehner S et al (2006) Identification of genistein-inducible and type III-secreted proteins of Bradyrhizobium japonicum. J Biotechnol 126:69–77. doi:10.1016/j.jbiotec.2006.03.037
Tadra-Sfeir MZ, Souza EM, Faoro H et al (2011) Naringenin regulates expression of genes involved in cell wall synthesis in Herbaspirillum seropedicae. Appl Environ Microbiol 77:2180–2183. doi:10.1128/AEM.02071-10
Tan C, Fu S, Liu M et al (2008) Cloning, expression and characterization of a cell wall surface protein, 6-phosphogluconate-dehydrogenase, of Streptococcus suis serotype 2. Vet Microbiol 130:363–370. doi:10.1016/j.vetmic.2008.02.025
Tanaka K, Gilroy S, Jones AM, Stacey G (2010) Extracellular ATP signaling in plants. Trends Cell Biol 20:601–608. doi:10.1016/j.tcb.2010.07.005
Thomas-Chollier M, Defrance M, Medina-Rivera A et al (2011) RSAT 2011: Regulatory sequence analysis tools. Nucleic Acids Res 39:86–91. doi:10.1093/nar/gkr377
Tolin S, Arrigoni G, Moscatiello R et al (2013) Quantitative analysis of the naringenin-inducible proteome in Rhizobium leguminosarum by isobaric tagging and mass spectrometry. Proteomics 13:1961–1972. doi:10.1002/pmic.201200472
Tóth K, Stacey G (2015) Does plant immunity play a critical role during initiation of the legume-rhizobium symbiosis? Front Plant Sci 6:401. doi:10.3389/fpls.2015.00401
Udvardi M, Poole PS (2013) Transport and metabolism in legume-rhizobia symbioses. Annu Rev Plant Biol 64:781–805. doi:10.1146/annurev-arplant-050312-120235
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
Wang G, Xia Y, Song X, Ai L (2016) Common non-classically secreted bacterial proteins with experimental evidence. Curr Microbiol 72:102–111. doi:10.1007/s00284-015-0915-6
Watt SA, Wilke A, Patschkowski T, Niehaus K (2005) Comprehensive analysis of the extracellular proteins from Xanthomonas campestris pv. campestris B100. Proteomics 5:153–167. doi:10.1002/pmic.200400905
Yang C-K, Ewis HE, Zhang X et al (2011) Nonclassical protein secretion by Bacillus subtilis in the stationary phase is not due to cell lysis. J Bacteriol 193:5607–5615. doi:10.1128/JB.05897-11
Ye Zhang MS (2013) The roles of malic ensymes in Rhizobium carbon metabolism. McMaster University, Hamilton, Ontario
York GM, Walker GC (1998) The succinyl and acetyl modifications of succinoglycan influence susceptibility of succinoglycan to cleavage by the Rhizobium meliloti glycanases ExoK and ExsH. J Bacteriol 180:4184–4191
Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989
Zanotti G, Cendron L (2014) Structural and functional aspects of the Helicobacter pylori secretome. World J Gastroenterol 20:1402–1423. doi:10.3748/wjg.v20.i6.1402
Zipfel C, Kunze G, Chinchilla D et al (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749–760. doi:10.1016/j.cell.2006.03.037
Zorreguieta A, Finnie C, Downie JA (2000) Extracellular glycanases of Rhizobium leguminosarum are activated on the cell surface by an exopolysaccharide-related component. J Bacteriol 182:1304–1312
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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.
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Communicated by Jorge Membrillo-Hernández.
Niurka Meneses and Hermenegildo Taboada contributed equally to this work.
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Meneses, N., Taboada, H., Dunn, M.F. et al. The naringenin-induced exoproteome of Rhizobium etli CE3. Arch Microbiol 199, 737–755 (2017). https://doi.org/10.1007/s00203-017-1351-8
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DOI: https://doi.org/10.1007/s00203-017-1351-8