Improving the activity of an inulosucrase by rational engineering for the efficient biosynthesis of low-molecular-weight inulin.
Inulosucrase
Low-molecular-weight inulin
Molecular dynamics simulations
Non-processive mechanism
Rational design
Journal
Archives of microbiology
ISSN: 1432-072X
Titre abrégé: Arch Microbiol
Pays: Germany
ID NLM: 0410427
Informations de publication
Date de publication:
03 Oct 2024
03 Oct 2024
Historique:
received:
07
08
2024
accepted:
29
09
2024
revised:
23
09
2024
medline:
3
10
2024
pubmed:
3
10
2024
entrez:
3
10
2024
Statut:
epublish
Résumé
Inulin, a widely recognized prebiotic, has diverse applications across various industrial sectors. Although inulin is primarily produced through plant extraction, there is growing interest in enzymatic synthesis as an alternative. The enzymatic production of inulin from sucrose, which yields polymers with degrees of polymerization similar to those of plant-derived inulin, shows potential as a viable replacement for traditional extraction methods. In this study, an inulosucrase from Neobacillus bataviensis was identified, demonstrating a non-processive mechanism specifically tailored for synthesizing inulin with polymerization degrees ranging from 3 to approximately 40. The enzyme exhibited optimal activity at pH 6.5 and 55 °C, efficiently producing inulin with a yield of 50.6%. Ca
Identifiants
pubmed: 39361031
doi: 10.1007/s00203-024-04153-7
pii: 10.1007/s00203-024-04153-7
doi:
Substances chimiques
Inulin
9005-80-5
Hexosyltransferases
EC 2.4.1.-
inulosucrase
EC 2.4.1.9
Sucrose
57-50-1
Bacterial Proteins
0
Calcium
SY7Q814VUP
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
424Subventions
Organisme : National Natural Science Foundation of China
ID : No. 22308118
Organisme : National Natural Science Foundation of China
ID : No. 22278183
Organisme : Natural Science Foundation of Jiangsu Province
ID : No. BK20231045
Organisme : the R&D Program of Beijing Municipal Education Commission
ID : No. KM202312448003
Organisme : Natural Science Foundation of Shandong Province
ID : No. ZR2023QC040
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Abaramak G, Porras-Domínguez JR, van Janse HC, Lescrinier E, Toksoy Öner E, Kırtel O, van den Ende W (2021) Functional and molecular characterization of the Halomicrobium Sp. IBSBa Inulosucrase Microorganisms 9:749
doi: 10.3390/microorganisms9040749
pubmed: 33918392
Abraham MJ, Murtola T, Schulz R, Páll S, Smith JC, Hess B, Lindahl E (2015) GROMACS: high performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX 1:19–25
doi: 10.1016/j.softx.2015.06.001
Anwar MA, Kralj S, van der Maarel MJ, Dijkhuizen L (2008) The probiotic Lactobacillus johnsonii NCC 533 produces high-molecular-mass inulin from sucrose by using an inulosucrase enzyme. Appl Environ Microbiol 74:3426–3433
doi: 10.1128/AEM.00377-08
pubmed: 18408060
pmcid: 2423029
Anwar MA, Kralj S, Pique AV, Leemhuis H, van der Maarel MJ, Dijkhuizen L (2010) Inulin and levan synthesis by probiotic Lactobacillus gasseri strains: characterization of three novel fructansucrase enzymes and their fructan products. Microbiology 156:1264–1274
doi: 10.1099/mic.0.036616-0
pubmed: 20075040
Aragón-León A, Moreno-Vilet L, González-Ávila M, Mondragón-Cortez PM, Sassaki GL, Martínez-Pérez RB, Camacho-Ruíz RM (2023) Inulin from halophilic archaeon Haloarcula: production, chemical characterization, biological, and technological properties. Carbohydr Polym 321:121333
doi: 10.1016/j.carbpol.2023.121333
pubmed: 37739546
Charoenwongpaiboon T, Sitthiyotha T, Ayutthaya PPN, Wangpaiboon K, Chunsrivirot S, Prousoontorn MH, Pichyangkura R (2019) Modulation of fructooligosaccharide chain length and insight into the product binding motif of Lactobacillus reuteri 121 inulosucrase. Carbohydr Polym 209:111–121
doi: 10.1016/j.carbpol.2018.12.078
pubmed: 30732790
Charoenwongpaiboon T, Wangpaiboon K, Puangpathanachai M, Pongsawasdi P, Pichyangkura R (2023) Energy-and evolution-based design of inulosucrase for enhanced thermostability and inulin production. Appl Microbiol Biotechnol 107:6831–6843
doi: 10.1007/s00253-023-12759-y
pubmed: 37688600
Dewulf EM, Cani PD, Claus SP, Fuentes S, Puylaert PG, Neyrinck AM, Bindels LB, de Vos WM, Gibson GR, Thissen J-P, Delzenne NM (2013) Insight into the prebiotic concept: lessons from an exploratory, double blind intervention study with inulin-type fructans in obese women. Gut 62:1112–1121
doi: 10.1136/gutjnl-2012-303304
pubmed: 23135760
Frasch HJ, Leeuwen SS, Dijkhuizen L (2017) Molecular and biochemical characteristics of the inulosucrase HugO from Streptomyces viridochromogenes DSM40736 (Tü494). Microbiology 163:1030–1041
doi: 10.1099/mic.0.000493
pubmed: 28714842
Ghauri K, Pijning T, Munawar N, Ali H, Ghauri MA, Anwar MA, Wallis R (2021) Crystal structure of an inulosucrase from Halalkalicoccus jeotgali B3T, a halophilic archaeal strain. FEBS J 288:5723–5736
doi: 10.1111/febs.15843
pubmed: 33783128
Goldenzweig A, Goldsmith M, Hill SE, Gertman O, Laurino P, Ashani Y, Prilusky J (2016) Automated structure-and sequence-based design of proteins for high bacterial expression and stability. Mol Cell 63:337–346
doi: 10.1016/j.molcel.2016.06.012
pubmed: 27425410
pmcid: 4961223
Illippangama AU, Jayasena DD, Jo C, Mudannayake DC (2022) Inulin as a functional ingredient and their applications in meat products. Carbohydr Polym 275:118706
doi: 10.1016/j.carbpol.2021.118706
pubmed: 34742431
Ishak SNH, Kamarudin NHA, Ali MSM, Leow ATC, Shariff FM, Rahman RNZRA (2021) Structure elucidation and docking analysis of 5 M mutant of T1 lipase Geobacillus zalihae. PLoS ONE 16:e0251751
doi: 10.1371/journal.pone.0251751
pubmed: 34061877
pmcid: 8168862
Kalantari H, Asadmasjedi N, reza Abyaz M, Mahdavinia M, Mohammadtaghvaei N (2019) Protective effect of inulin on methotrexate-induced liver toxicity in mice. Biomed Pharmacother 110:943–950
doi: 10.1016/j.biopha.2018.11.144
pubmed: 30625516
Kido Y, Saburi W, Nagura T, Mori H (2023) Hydrolysis-transglycosylation of sucrose and production of β-(2→1)-fructan by inulosucrase from Neobacillus drentensis 57 N. Biosci Biotechnol Biochem 87:1169–1182
doi: 10.1093/bbb/zbad100
pubmed: 37491698
Kralj S, Leeflang C, Sierra EI, Kempiński B, Alkan V, Kolkman M (2018) Synthesis of fructooligosaccharides (FosA) and inulin (InuO) by GH68 fructosyltransferases from Bacillus agaradhaerens strain WDG185. Carbohydr Polym 179:350–359
doi: 10.1016/j.carbpol.2017.09.069
pubmed: 29111061
Li J, Cui H, Xu X, Li J, Lu M, Guan X, Zhu D, Liu H (2022) Effect of fat replacement by inulin on the physicochemical properties and sensory attributes of low-fat margarine. Food Hydrocolloids 133:107868
doi: 10.1016/j.foodhyd.2022.107868
Moradali MF, Rehm BH (2020) Bacterial biopolymers: from pathogenesis to advanced materials. Nat Rev Microbiol 18:195–210
doi: 10.1038/s41579-019-0313-3
pubmed: 31992873
pmcid: 7223192
Ni D, Zhu Y, Xu W, Pang X, Lv J, Mu W (2020a) Production and physicochemical properties of food-grade high-molecular-weight Lactobacillus inulin. J Agric Food Chem 68:5854–5862
doi: 10.1021/acs.jafc.9b07894
pubmed: 32366099
Ni D, Chen Z, Xu W, Zhang W, Mu W (2020b) Efficient production of inulin and oligosaccharides using thermostable inulosucrase from Lactobacillus jensenii. Int J Biol Macromol 165:1250–1257
doi: 10.1016/j.ijbiomac.2020.10.003
pubmed: 33038393
Ni D, Kırtel O, Yin D, Xu W, Chen Q, Öner ET, Mu W (2021a) Improving the catalytic behaviors of Lactobacillus-derived fructansucrases by truncation strategies. Enzyme Microb Technol 149:109857
doi: 10.1016/j.enzmictec.2021.109857
pubmed: 34311894
Ni D, Zhang S, Kırtel O, Xu W, Chen Q, Öner ET, Mu W (2021b) Improving the thermostability and catalytic activity of an inulosucrase by rational engineering for the biosynthesis of microbial inulin. J Agric Food Chem 69:13125–13134
doi: 10.1021/acs.jafc.1c04852
pubmed: 34618455
Ni D, Zhang S, Liu X, Zhu Y, Xu W, Zhang W, Mu W (2024) Production, effects, and applications of fructans with various molecular weights. Food Chem 437:137895
doi: 10.1016/j.foodchem.2023.137895
pubmed: 37924765
Ozimek LK, Kralj S, van der Maarel MJ, Dijkhuizen L (2006) The levansucrase and inulosucrase enzymes of Lactobacillus reuteri 121 catalyse processive and non-processive transglycosylation reactions. Microbiology 152:1187–1196
doi: 10.1099/mic.0.28484-0
pubmed: 16549681
Pijning T, Anwar MA, Böger M, Dobruchowska JM, Leemhuis H, Kralj S, Dijkstra BW (2011) Crystal structure of inulosucrase from Lactobacillus: insights into the substrate specificity and product specificity of GH68 fructansucrases. J Mol Biol 412:80–93
doi: 10.1016/j.jmb.2011.07.031
pubmed: 21801732
Raga-Carbajal E, Carrillo-Nava E, Costas M, Porras-Dominguez J, López-Munguía A, Olvera C (2016) Size product modulation by enzyme concentration reveals two distinct levan elongation mechanisms in Bacillus subtilis levansucrase. Glycobiology 26:377–385
doi: 10.1093/glycob/cwv112
pubmed: 26646447
Rehm BH (2010) Bacterial polymers: biosynthesis, modifications and applications. Nat Rev Microbiol 8:578–592
doi: 10.1038/nrmicro2354
pubmed: 20581859
Sheng W, Ji G, Zhang L (2023) Immunomodulatory effects of inulin and its intestinal metabolites. Front Immunol 14:1224092
doi: 10.3389/fimmu.2023.1224092
pubmed: 37638034
pmcid: 10449545
Sürmeli Y, Durmuş N, Şanlı-Mohamed G (2024) Exploring the structural insights of thermostable Geobacillus esterases by computational characterization. ACS Omega 9:32931–32941
pubmed: 39100300
pmcid: 11292637
Tütüncü HE, Durmuş N, Sürmeli Y (2024) Unraveling the potential of uninvestigated thermoalkaliphilic lipases by molecular docking and molecular dynamic simulation: an in silico characterization study. 3 Biotech 14:179
doi: 10.1007/s13205-024-04023-5
pubmed: 38882640
Valcheva R, Koleva P, Martínez I, Walter J, Gänzle MG, Dieleman LA (2019) Inulin-type fructans improve active ulcerative colitis associated with microbiota changes and increased short-chain fatty acids levels. Gut Microbes 10:334–357
doi: 10.1080/19490976.2018.1526583
pubmed: 30395776
van Hijum S, van Geel-Schutten G, Rahaoui H, van der Maarel M, Dijkhuizen L (2002) Characterization of a novel fructosyltransferase from Lactobacillus reuteri that synthesizes high-molecular-weight inulin and inulin oligosaccharides. Appl Environ Microbiol 68:4390–4398
doi: 10.1128/AEM.68.9.4390-4398.2002
pubmed: 12200292
pmcid: 124061
Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R, Heer FT, de Beer TA, Rempfer C, Bordoli L, Lepore R, Schwede T (2018) SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res 46:W296–W303
doi: 10.1093/nar/gky427
pubmed: 29788355
pmcid: 6030848
Xu W, Ni D, Hou X, Pijning T, Guskov A, Rao Y, Mu W (2022) Crystal structure of levansucrase from the gram-negative bacterium Brenneria provides insights into its product size specificity. J Agric Food Chem 70:5095–5105
doi: 10.1021/acs.jafc.2c01225
pubmed: 35388691
Yokoi K-j, Tsutsui S, Arakawa G-y, Takaba M, Fujii K, Kaneko S (2021) Molecular and biochemical characteristics of inulosucrase InuBK from Alkalihalobacillus krulwichiae JCM 11691. Biosci Biotechnol Biochem 85:1830–1838
doi: 10.1093/bbb/zbab094
pubmed: 34021568
Zhang J, Li L, Gu S, Teng K, Ren J, Liu G, Zhong J (2022) Characterization of a novel fructosyltransferase from Lactobacillus crispatus, InuCA, that attaches to the cell surface by electrostatic interaction. Appl Environ Microbiol 88:e02399–e02321
doi: 10.1128/aem.02399-21
pubmed: 34910558
pmcid: 8863051
Zhang S, Ni D, Xu W, Zhang W, Mu W (2023) Characterization of a processive inulosucrase from Lactobacillus mulieris for efficient biosynthesis of high-molecular-weight inulin. Enzyme Microb Technol 164:110186
doi: 10.1016/j.enzmictec.2022.110186
pubmed: 36529060
Zou J, Reddivari L, Shi Z, Li S, Wang Y, Bretin A, Ngo VL, Flythe M, Pellizzon M, Chassaing B, Gewirtz AT (2021) Inulin fermentable fiber ameliorates type I diabetes via IL22 and short-chain fatty acids in experimental models. Cell Mol Gastroenterol Hepatol 12:983–1000
doi: 10.1016/j.jcmgh.2021.04.014
pubmed: 33940221
pmcid: 8346662