Halotolerant aminopeptidase M29 from Mesorhizobium SEMIA 3007 with biotechnological potential and its impact on biofilm synthesis

dc.contributor.authorMachado Sierra, Elwi
dc.contributor.authorRangel Pereira, Mariana
dc.contributor.authorCarvalho Maester, Thaís
dc.contributor.authorSoares Gomes-Pepe, Elisangela
dc.contributor.authorRodas Mendoza, Elkin
dc.contributor.authorMacedo Lemos, Elkin
dc.date.accessioned2018-02-05T14:41:30Z
dc.date.available2018-02-05T14:41:30Z
dc.date.issued2017-09-06
dc.description.abstractThe aminopeptidase gene from Mesorhizobium SEMIA3007 was cloned and overexpressed in Escherichia coli. The enzyme called MesoAmp exhibited optimum activity at pH 8.5 and 45 °C and was strongly activated by Co2+ and Mn2+. Under these reaction conditions, the enzyme displayed Km and kcat values of 0.2364 ± 0.018 mM and 712.1 ± 88.12 s−1, respectively. Additionally, the enzyme showed remarkable stability in organic solvents and was active at high concentrations of NaCl, suggesting that the enzyme might be suitable for use in biotechnology. MesoAmp is responsible for 40% of the organism’s aminopeptidase activity. However, the enzyme’s absence does not affect bacterial growth in synthetic broth, although it interfered with biofilm synthesis and osmoregulation. To the best of our knowledge, this report describes the first detailed characterization of aminopeptidase from Mesorhizobium and suggests its importance in biofilm formation and osmotic stress tolerance. In summary, this work lays the foundation for potential biotechnological applications and/or the development of environmentally friendly technologies and describes the first solvent- and halo-tolerant aminopeptidases identified from the Mesorhizobium genus and its importance in bacterial metabolism.eng
dc.identifier.issn20452322
dc.identifier.urihttp://hdl.handle.net/20.500.12442/1585
dc.language.isoengspa
dc.publisherSpringerspa
dc.rights.accessrightsinfo:eu-repo/semantics/openAccess
dc.rights.licenselicencia de Creative Commons Reconocimiento-NoComercial-CompartirIgual 4.0 Internacionalspa
dc.sourceScientific Reportseng
dc.sourceVol. 7, No. 10684 (2017)
dc.source.uriDOI:10.1038/s41598-017-10932-8eng
dc.subjectMesorhizobiumeng
dc.subjectAminopeptidaseeng
dc.subjectMicrobial Biofilmseng
dc.subjectSodium Chlorideeng
dc.subjectOsmosiseng
dc.subjectBiotechnologyeng
dc.subjectWater-Electrolyte Balanceeng
dc.subjectOrganic solvent producteng
dc.titleHalotolerant aminopeptidase M29 from Mesorhizobium SEMIA 3007 with biotechnological potential and its impact on biofilm synthesiseng
dc.typearticlespa
dcterms.referencesGhobakhlou, A.-F., Johnston, A., Harris, L., Antoun, H. & Laberge, S. Microarray transcriptional profiling of Arctic Mesorhizobium strain N33 at low temperature provides insights into cold adaption strategies. BMC Genomics 16, 383 (2015).eng
dcterms.referencesKrick, A. et al. A Marine Mesorhizobium sp. Produces Structurally Novel Long-Chain N-Acyl-L-Homoserine Lactones. Appl. Environ. Microbiol. 73, 3587–3594 (2007).eng
dcterms.referencesDiouf, F. et al. Genetic and Genomic Diversity Studies of Acacia Symbionts in Senegal Reveal New Species of Mesorhizobium with a Putative Geographical Pattern. PLoS One 10, e0117667 (2015).eng
dcterms.referencesTeng, Y. et al. Isolation of the PCB-degrading bacteria Mesorhizobium sp. ZY1 and its combined remediation with Astragalus sinicus L. for contaminated soil. Int. J. Phytoremediation 20 (2015).eng
dcterms.referencesVenkatachalam, G., Nandakumar, V., Suresh, G. & Doble, M. Characterization and applications of cyclic β-(1,2)-glucan produced from R. meliloti. RSC Adv. 4, 11393 (2014).eng
dcterms.referencesUechi, K., Takata, G., Fukai, Y., Yoshihara, A. & Morimoto, K. Gene Cloning and Characterization of L-Ribulose 3-epimerase from Mesorhizobium loti and its Application to Rare Sugar Production. Biosci. Biotechnol. Biochem. 77, 511–515 (2013).eng
dcterms.referencesKim, J. et al. Cloning and characterization of a novel β-transaminase from Mesorhizobium sp. strain LUK: A new biocatalyst for the synthesis of enantiomerically pure??-amino acids. Appl. Environ. Microbiol. 73, 1772–1782 (2007).eng
dcterms.referencesPrasad, M. P. & Sethi, R. Optimization of cellulase production from a novel bacterial isolate Mesorhizobium sp. from marine source. J. Enzym. Res. 4, 39–45 (2013).eng
dcterms.referencesTakata, G. et al. Characterization of Mesorhizobium loti L -Rhamnose Isomerase and Its Application to L -Talose Production. Biosci. Biotechnol. Biochem. 75, 1006–1009 (2011).eng
dcterms.referencesMugo, A. N. et al. Crystal structure of pyridoxine 4-oxidase from Mesorhizobium loti. Biochim. Biophys. Acta 1834, 953–63 (2013).eng
dcterms.referencesHuang, W. et al. The Structure and Enzyme Characteristics of a Recombinant Leucine Aminopeptidase rLap1 from Aspergillus sojae and Its Application in Debittering. Appl. Biochem. Biotechnol. 177, 190–206 (2015).eng
dcterms.referencesThomas, S., Besset, C., Courtin, P. & Rul, F. The role of aminopeptidase PepS in the growth of Streptococcus thermophilus is not restricted to nitrogen nutrition. J. Appl. Microbiol. 108, 148–157 (2010).eng
dcterms.referencesCheng, C. et al. Aminopeptidase T of M29 Family Acts as A Novel Intracellular Virulence Factor for Listeria monocytogenes Infection. Sci. Rep. 5, 17370 (2015).eng
dcterms.referencesHernández-Moreno, A. V. et al. Kinetics and conformational stability studies of recombinant leucine aminopeptidase. Int. J. Biol. Macromol. 64, 306–312 (2014).eng
dcterms.referencesRamírez-Zavala, B., Mercado-Flores, Y., Hernández-Rodríguez, C. & Villa-Tanaca, L. Purification and characterization of a lysine aminopeptidase from Kluyveromyces marxianus. FEMS Microbiol. Lett. 235, 369–375 (2004).eng
dcterms.referencesDing, G., Zhou, N. & Tian, Y. Over-Expression of a Proline Specific Aminopeptidase from Aspergillus oryzae JN-412 and Its Application in Collagen Degradation. Appl. Biochem. Biotechnol. 173, 1765–1777 (2014).eng
dcterms.referencesRawlings, N. D., Waller, M., Barrett, A. J. & Bateman, A. MEROPS: The database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res. 42, 343–350 (2014).eng
dcterms.referencesRawlings, N. D. & Barrett, A. J. Evolutionary families of metallopeptidases. Methods Enzymol. 248, 183–228 (1995).eng
dcterms.referencesBailey, S., Ward, D., Middleton, R., Grossmann, J. G. & Zambryski, P. C. Agrobacterium tumefaciens VirB8 structure reveals potential protein-protein interaction sites. Proc. Natl. Acad. Sci. 103, 2582–2587 (2006).eng
dcterms.referencesWang, T.-F., Lin, M.-G., Lo, H.-F., Chi, M.-C. & Lin, L.-L. Biophysical characterization of a recombinant aminopeptidase II from the thermophilic bacterium Bacillus stearothermophilus. J. Biol. Phys. 40, 25–40 (2014).eng
dcterms.referencesZhuo, S. & Dixon, J. E. Effects of sulfhydryl regents on the activity of lambda Ser/Thr phosphoprotein phosphatase and inhibition of the enzyme by zinc ion. Protein Eng. 10, 1445–52 (1997).eng
dcterms.referencesMukhopadhyay, A. Tolerance engineering in bacteria for the production of advanced biofuels and chemicals. Trends Microbiol. 23, 498–508 (2015).eng
dcterms.referencesSardessai, Y. & Bhosle, S. Tolerance of bacteria to organic solvents. Res. Microbiol. 153, 263–268 (2002).eng
dcterms.referencesBertin, P. B. et al. The thermophilic, homohexameric aminopeptidase of Borrelia burgdorferi is a member of the M29 family of metallopeptidases. Infect. Immun. 73, 2253–2261 (2005).eng
dcterms.referencesFernandez-Espla, M. D. & Rul, F. PepS from Streptococcus thermophilus: A new member of the aminopeptidase T family of thermophilic bacteria. Eur. J. Biochem. 263, 502–510 (1999).eng
dcterms.referencesMitchell, A. et al. The InterPro protein families database: the classification resource after 15 years. Nucleic Acids Res. 43, D213–D221 (2015).eng
dcterms.referencesTa, H. M. et al. Structure-based elucidation of the regulatory mechanism for aminopeptidase activity. Acta Crystallogr. Sect. D Biol. Crystallogr. 69, 1738–1747 (2013).eng
dcterms.referencesRul, F. In Handbook of Proteolytic Enzymes (eds Rawlings, N. D. & Salvesen, G.) 1677–1678 (Academic Press publications - Elsevier). doi:10.1016/B978-0-12-382219-2.00380-X (2013).eng
dcterms.referencesPlotka, M. et al. Novel Highly Thermostable Endolysin from Thermus scotoductus MAT2119 Bacteriophage Ph2119 with Amino Acid Sequence Similarity to Eukaryotic Peptidoglycan Recognition Proteins. Appl. Environ. Microbiol. 80, 886–895 (2014).eng
dcterms.referencesVieille, C., Zeikus, G. J. & Vieille, C. Thermostability Hyperthermophilic Enzymes: Sources, Uses, and Molecular Mechanisms for Thermostability. Microbiol. Mol. Biol. Rev. 65, 1–43 (2001).eng
dcterms.referencesMerheb-Dini, C. et al. Biochemical and functional characterization of a metalloprotease from the thermophilic fungus thermoascus aurantiacus. J. Agric. Food Chem. 57, 9210–9217 (2009).eng
dcterms.referencesHandbook of Proteolytic Enzymes. Protein Science 8, (Academic Press, 2013).eng
dcterms.referencesKuo, L.-Y., Hwang, G.-Y., Lai, Y.-J., Yang, S.-L. & Lin, L.-L. Overexpression, purification, and characterization of the recombinant leucine aminopeptidase II of Bacillus stearothermophilus. Curr. Microbiol. 47, 40–45 (2003).eng
dcterms.referencesDong, L. et al. The leucyl aminopeptidase from Helicobacter pylori is an allosteric enzyme. Microbiology 151, 2017–2023 (2005).eng
dcterms.referencesWang, F. et al. Biochemical Properties of Recombinant Leucine Aminopeptidase II from Bacillus stearothermophilus and Potential Applications in the Hydrolysis of Chinese Anchovy (Engraulis japonicus) Proteins. J. Agric. Food Chem. 60, 165–172 (2012).eng
dcterms.referencesZhu, X. et al. Mechanism of peptide hydrolysis by co-catalytic metal centers containing leucine aminopeptidase enzyme: A DFT approach. J. Biol. Inorg. Chem. 17, 209–222 (2012).eng
dcterms.referencesDoukyu, N. & Ogino, H. Organic solvent-tolerant enzymes. Biochem. Eng. J. 48, 270–282 (2010).eng
dcterms.referencesGaur, R., Grover, T., Sharma, R., Kapoor, S. & Khare, S. K. Purification and characterization of a solvent stable aminopeptidase from Pseudomonas aeruginosa: Cloning and analysis of aminopeptidase gene conferring solvent stability. Process Biochem. 45, 757–764 (2010).eng
dcterms.referencesChang, A. et al. BRENDA in 2015: exciting developments in its 25th year of existence. Nucleic Acids Res. 43, D439–46 (2015).eng
dcterms.referencesCarroll, R. K. et al. Identification of an intracellular M17 family leucine aminopeptidase that is required for virulence in Staphylococcus aureus. Microbes Infect. 14, 989–999 (2012).eng
dcterms.referencesCarroll, R. K. et al. The Staphylococcus aureus leucine aminopeptidase is localized to the bacterial cytosol and demonstrates a broad substrate range that extends beyond leucine. Biol. Chem. 394, 1199–1216 (2013).eng
dcterms.referencesSingh, A. K., Singh, R., Tomar, D., Pandya, C. D. & Singh, R. The leucine aminopeptidase of Staphylococcus aureus is secreted and contributes to biofilm formation. Int. J. Infect. Dis. 16, e375–e381 (2012).eng
dcterms.referencesMiller, C. G. & Green, L. Degradation of abnormal proteins in peptidase-deficient mutants of Salmonella typhimurium. J. Bacteriol. 147, 925–30 (1981).eng
dcterms.referencesCharlier, D. et al. Mutational analysis of Escherichia coli PepA, a multifunctional DNA-binding aminopeptidase 1 1 Edited by M. Yaniv. J. Mol. Biol. 302, 409–424 (2000).eng
dcterms.referencesKleine, L. L., Monnet, V., Pechoux, C. & Trubuil, A. Role of bacterial peptidase F inferred by statistical analysis and further experimental validation. HFSP J. 2, 29–41 (2008).eng
dcterms.referencesBeenken, K. E., Blevins, J. S. & Smeltzer, M. S. Mutation of sarA in Staphylococcus aureus Limits Biofilm Formation. Infect. Immun. 71, 4206–4211 (2003).eng
dcterms.referencesDíaz-Pérez, A. L., Díaz-Pérez, C. & Campos-García, J. Bacterial l-leucine catabolism as a source of secondary metabolites. Rev. Environ. Sci. Biotechnol. 15, 1–29 (2015).eng
dcterms.referencesMeasures, J. Role of amino acids in osmoregulation of non-halophilic bacteria. Nature 257, 398–400 (1975).eng
dcterms.referencesBharti, N., Yadav, D., Barnawal, D., Maji, D. & Kalra, A. Exiguobacterium oxidotolerans, a halotolerant plant growth promoting rhizobacteria, improves yield and content of secondary metabolites in Bacopa monnieri (L.) Pennell under primary and secondary salt stress. World J. Microbiol. Biotechnol. 29, 379–387 (2013).eng
dcterms.referencesLi, W., Zhou, R. & Mu, Y. Salting effects on protein components in aqueous NaCl and urea solutions: Toward understanding of ureainduced protein denaturation. J. Phys. Chem. B 116, 1446–1451 (2012).eng
dcterms.referencesGong, J.-S. et al. Metagenomic technology and genome mining: emerging areas for exploring novel nitrilases. Appl. Microbiol. Biotechnol. 97, 6603–6611 (2013).Gong, J.-S. et al. Metagenomic technology and genome mining: emerging areas for exploring novel nitrilases. Appl. Microbiol. Biotechnol. 97, 6603–6611 (2013).eng
dcterms.referencesXi, H., Tian, Y., Zhou, N., Zhou, Z. & Shen, W. Characterization of an N -glycosylated Bacillus subtilis leucine aminopeptidase expressed in Pichia pastoris. J. Basic Microbiol. 55, 236–246 (2015).eng
dcterms.referencesSetyorini, E., Kim, Y.-J., Takenaka, S., Murakami, S. & Aoki, K. Purification and characterization of a halotolerant intracellular protease fromBacillus subtilis strain FP-133. J. Basic Microbiol. 46, 294–304 (2006).eng
dcterms.referencesAziz, R. K. et al. The RAST Server: Rapid Annotations using Subsystems Technology. BMC Genomics 9, 75 (2008).eng
dcterms.referencesKishi, L. T., Fernandes, C. C., Omori, W. P., Campanharo, J. C. & Macedo Lemos, E. Reclassification of the taxonomic status of SEMIA3007 isolated in Mexico B-11A Mex as Rhizobium leguminosarum bv. viceae by bioinformatic tools. BMC Microbiol. 16, 1–8 (2016).eng
dcterms.referencesOverbeek, R. et al. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res. 42, D206–D214 (2014).eng
dcterms.referencesThompson, J. D., Higgins, D. G. & Gibson, T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–80 (1994).eng
dcterms.referencesAshkenazy, H., Erez, E., Martz, E. & Pupko, T. & Ben-Tal, N. ConSurf 2010: Calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res. 38, 529–533 (2010).eng
dcterms.referencesPetersen, T. N., Brunak, S., von Heijne, G. & Nielsen, H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8, 785–786 (2011).eng
dcterms.referencesFiser, A., Sali, A. & Šali, A. MODELLER: Generation and Refinement of Homology-Based Protein Structure Models. Methods Enzymol. 374, 461–491 (2003).eng
dcterms.referencesOdintsov, S. G., Sabała, I., Bourenkov, G., Rybin, V. & Bochtler, M. Substrate access to the active sites in aminopeptidase T, a representative of a new metallopeptidase clan. J. Mol. Biol. 354, 403–412 (2005).eng
dcterms.referencesSabała, G. E., Bourenkov, I. G., Rybin, V. & Bochtler, M. Staphylococcus aureus aminopeptidase S is a founding member of a new peptidase clan. J. Biol. Chem. 280, 27792–27799 (2005).eng
dcterms.referencesMcGuffin, L. J., Buenavista, M. T. & Roche, D. B. The ModFOLD4 server for the quality assessment of 3D protein models. Nucleic Acids Res. 41, W368–W372 (2013).eng
dcterms.referencesPierce, B. G. et al. Structural bioinformatics ZDOCK server: interactive docking prediction of protein – protein complexes and symmetric multimers. Bioinformatics 30, 1771–1773 (2014).eng
dcterms.referencesOliveira, S. H. P. et al. KVFinder: steered identification of protein cavities as a PyMOL plugin. BMC Bioinformatics 15, 197 (2014).eng
dcterms.referencesDeLano, W. L. The PyMOL Molecular Graphics System, Version 1.7.4 Schrödinger, LLC (2004).eng
dcterms.referencesPereira, M. R., Mercaldi, G. F., Maester, T. C., Balan, A. & De Macedo Lemos, E. G. Est16, a new esterase isolated from a metagenomic library of a microbial consortium specializing in diesel oil degradation. PLoS One 10, 1–16 (2015).eng
dcterms.referencesMaester, T. C., Pereira, M. R., Machado Sierra, E. G., Balan, A. & de Macedo Lemos, E. G. Characterization of EST3: a metagenomederived esterase with suitable properties for biotechnological applications. Appl. Microbiol. Biotechnol. 100, 5815–5827 (2016).eng
dcterms.referencesBradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254 (1976).eng
dcterms.referencesLaemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–5 (1970).eng
dcterms.referencesGreenfield, N. J. Using circular dichroism collected as a funcion of temperature to determine the thermodynamics of protein unfolding and binding interactions. Nat. Protoc. 1, 2527–2535 (2009).eng
dcterms.referencesWest, L., Yang, D. & Stephens, C. Use of the Caulobacter crescentus Genome Sequence To Develop a Method for Systematic Genetic Mapping. J. Bacteriol. 184, 2155–2166 (2002).eng
dcterms.referencesLiu, Z. et al. Efficient Construction of Large Genomic Deletion in Agrobacterium tumefaciens by Combination of Cre/loxP System and Triple Recombineering. Curr. Microbiol. 72, 465–472 (2016).eng
dcterms.referencesBeringer, J. E. R factor transfer in Rhizobium leguminosarum. J. Gen. Microbiol. 84, 188–98 (1974).eng
dcterms.referencesOliveira, N. M. et al. Correction: Biofilm Formation As a Response to Ecological Competition. PloS Biol. 13, e1002232 (2015).eng
dcterms.referencesHwang, G. Y., Kuo, L. Y., Tsai, M. R., Yang, S. L. & Lin, L. L. Histidines 345 and 378 of Bacillus stearotheromophilus leucine aminopeptidase II are essential for the catalytic activity of the enzyme. Antonie van Leeuwenhoek, Int. J. Gen. Mol. Microbiol. 87, 355–359 (2005).eng
dcterms.referencesJankiewicz, U. & Wnuk, a An activated by cobalt alkaline aminopeptidase from Bacillus mycoides. Appl. Biochem. Microbiol. 47, 136–143 (2011).eng
dcterms.referencesKhan, A. R., Nirasawa, S., Kaneko, S., Shimonishi, T. & Hayashi, K. Characterization of a solvent resistant and thermostable aminopeptidase from the hyperthermophillic bacterium, Aquifex aeolicus. Enzyme Microb. Technol. 27, 83–88 (2000).eng
dcterms.referencesChung, D.-M., Lee, G., Chun, S.-S., Chung, Y. & Chun, H. Effect of NaCl on Hydrolytic Activity of Leucine Aminopeptidase from Bacillus sp. N2. J. Life Sci. 21, 761–765 (2011).eng
dcterms.referencesLee, G., Chun, S., Kho, Y. & Chun, H. Purification and properties of an extracellular leucine aminopeptidase from the Bacillus sp. N2. J. Appl. Microbiol. 85, 561–566 (1998).eng

Archivos

Bloque original
Mostrando 1 - 1 de 1
Cargando...
Miniatura
Nombre:
2017_Halotolerant (1).pdf
Tamaño:
1.68 MB
Formato:
Adobe Portable Document Format
Descripción:
Formato Pdf texto completo
Bloque de licencias
Mostrando 1 - 1 de 1
No hay miniatura disponible
Nombre:
license.txt
Tamaño:
1.71 KB
Formato:
Item-specific license agreed upon to submission
Descripción:

Colecciones