Abstract
Endophytic bacteria refer to bacteria which promote plant growth via direct and indirect mechanisms. Three endophytic bacteria isolated from Jerusalem artichoke exhibited plant growth induction and inulin production. These bacteria had functions of fructan degradation and synthesis from inulinase and levansucrase, respectively. Rossellomorea aquimaris 3.13 and Priestia megaterium 3.5 obtained inulinase/levanase enzyme with inulin and levan as substrates; enzyme production showed the optimum conditions in 1% inulin medium of 35 °C, pH 7.0. Bacillus velezensis 5.18 and Priestia megaterium 3.5 had inulosucrase/levansucrase enzyme with sucrose as a major carbon source; the enzyme had optimum temperature and pH conditions of 30 °C and pH 7.0, respectively. A combination of carbon sources had effect on decreasing enzyme activity; in addition, co-inoculation of bacteria showed a slight difference in enzyme production compared with single inoculation. The inulosucrase/levansucrase was produced earlier in co-culture containing bacteria with inulinase activity. Plant fructan synthesis was involved in 1-SST and 1-FFT, while 1-FEH encoded inulin degradation; these genes were evaluated in Jerusalem artichoke inoculated with the endophytic bacteria to quantify gene expression level using qPCR. All genes expressed in low levels at early stage of growth, responding to all endophytic bacteria. Significantly, Bacillus velezensis 5.18 induced all genes of the plant at 65 days of inoculation; Rossellomorea aquimaris 3.13 induced 1-FFT while Priestia megaterium 3.5 induced 1-SST.
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References
Anwar MA, Kralj S, van der Maarel MJEC, 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. https://doi.org/10.1128/AEM.00377-08
Ayyachamy M, Khelawan K, Pillay D, Permaul K, Singh S (2007) Production of inulinase by Xanthomonas campestris pv phaseoli using onion (Allium cepa) and garlic (Allium sativum) peels in solid state cultivation. Lett Appl Microbiol 45:439–444. https://doi.org/10.1111/j.1472-765X.2007.02222.x
Beck RHF (2017) Statistic thermodynamic analysis of fructans—Part 4: modeling inulin biosynthesis as anon-equilibrium thermodynamic process. Sugar Ind 142:206–211. https://doi.org/10.36961/si18245
Das D, Bhat MR, Selvaraj R (2019) Review of inulinase production using solid-state fermentation. Ann Microbiol 69:201–209. https://doi.org/10.1007/s13213-019-1436-5
Derycke DG, Vandamme EJ (1984) Production and properties of Aspergillus niger inulinase. Chem Technol Biotechnol 34:45–51. https://doi.org/10.1002/jctb.280340108
Elyachioui M, Horeiz JP, Taillez R (1992) General properties of extracellular bacterial inulinase. J Appl Bacteriol 73:514–519. https://doi.org/10.1111/j.1365-2672.1992.tb05014.x
Fang G, Tong Z, Zhenming C, Jun S, Jing L, Xianghong W (2008) Purification and characterization of extracellular inulinase from a marine yeast Pichia guilliermondii and inulin hydrolysis by the purified inulinase. Biotechnol Bioproc E 13:533–539. https://doi.org/10.1007/s12257-007-0177-7
Flavio T, Vanessa FO, Maria AMC, Marilia G (2015) Effects of different carbohydrate sources on fructan metabolism in plants of Chrysolaena obovata grown in vitro. Front Plant Sci 6:1–13. https://doi.org/10.3389/fpls.2015.00681
Han YW (1990) Microbial levan. Adv Appl Microbiol 35:171–194. https://doi.org/10.1016/s0065-2164(08)70244-2
Hardoim PR, van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A et al (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320. https://doi.org/10.1128/MMBR.00050-14
Hellemans J, Mortier G, Paepe AD, Speleman F, Vandesompele J (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8:R19. https://doi.org/10.1186/gb-2007-8-2-r19
Man S, Taohua L, Yuan Y, Yingying L, Long M, Fuping L (2021) The roles of inulin-type fructans. Carbohyd Polym 252:117–155. https://doi.org/10.1016/j.carbpol.2020.117155
Namwongsa J, Jogloy S, Vorasoot N, Boonlue S, Riddech N, Mongkolthanaruk W (2019) Endophytic bacteria improve root traits, biomass and yield of Helianthus tuberosus L. under normal and deficit water conditions. J Microbiol Biotechnol 29:1777–1789. https://doi.org/10.4014/jmb.1903.03062
Olivares-Illana V, Wacher-Rodarte C, Le Borgne S (2002) Characterization of a cell-associated inulosucrase from a novel source: A Leuconostoc citreum strain isolated from Pozol, a fermented corn beverage of Mayan origin. J Ind Microbiol Biot 28:112–117. https://doi.org/10.1038/sj/jim/7000224
Öner ET, Hernández L, Combie J (2016) Review of levan polysaccharide: from a century of past experiences to future prospects. Biotechnol Adv 34:827–844. https://doi.org/10.1016/j.biotechadv.2016.05.002
Pandey A, Soccol CR, Selvakumar P, Soccol VT, Krieger N, Jose D (1999) Recent developments in microbial inulinases, its production, properties and Industrial applications. Appl Biochem Biotech 81:35–52. https://doi.org/10.1385/abab:81:1:35
Peña-Cardeña A, Rodríguez-Alegría ME, Olvera C, Munguía AL (2015) Synthesis of fructooligosaccharides by IslA4, a truncated inulosucrase from Leuconostoc citreum. BMC Biotechnol 15:2. https://doi.org/10.1186/s12896-015-0116-1
Phengnoi P, Charoenwongpaiboon T, Wangpaiboon K, Klaewkla M, Nakapong S, Visessanguan W, Ito K, Pichyangkura R, Kuttiyawong K (2020) Levansucrase from Bacillus amyloliquefaciens KK9 and Its Y237S variant producing the high bioactive levan-type fructooligosaccharides. Biomolecules 29:692. https://doi.org/10.3390/biom10050692
Porras-Domínguez JR, Ávila-Fernández A, Miranda-Molina A, Rodríguez-Alegría ME, Munguía AL (2015) Bacillus subtilis 168 levansucrase (SacB) activity affects average levan molecular weight. Carbohyd Polym 132:338–344. https://doi.org/10.1016/j.carbpol.2015.06.056
Prabhjot KG, Arun DS, Rajesh KH, Prabhjeet S (2003) Effect of media supplements and culture conditions on inulinase production by an actinomycete strain. Bioresour Technol 87:359–362. https://doi.org/10.1016/S0960-8524(02)00262-6
Prangviset K, Songpim M, Yodsuwan N, Wannawilai S, Dejsungkranont M, Changlek P, Sirisansaneeyakul S (2018) Fructose production from Jerusalem artichoke using mixed inulinases. Agric Nat Resour 52:132–139. https://doi.org/10.1016/j.anres.2018.08.001
Roy KL, Vergauwen R, Cammaer V, Yoshida M, Kawakami A et al (2007) Fructan 1-exohydrolase is associated with flower opening in Campanula rapunculoides. Funct Plant Biol 34:972–983. https://doi.org/10.1071/FP07125
Saengkanuk A, Nuchadomrong S, Jogloy S, Patanothai A, Srijaranai S (2011) A simplified spectrophotometric method for the determination of inulin in Jerusalem artichoke (Helianthus tuberosus L.) tubers. Eur Food Res Technol 233:609–616. https://doi.org/10.1007/s00217-011-1552-3
Shen J, Zhang R, Li J, Tang X, Li R, Wang M et al (2015) Characterization of an exo-inulinase from Arthrobacter: a novel NaCl-tolerant exo-inulinase with high molecular mass. Bioengineered 6:99–105. https://doi.org/10.1080/21655979.2015.1019686
Shi Q, Hou Y, Xu Y, Mørkeberg Krogh KBR, Tenkanen M (2019) Enzymatic analysis of levan produced by lactic acid bacteria in fermented doughs. Carbohyd Polym 208:285–293. https://doi.org/10.1016/j.carbpol.2018.12.044
Valcheva R, Koleva P, Martinez I, Walter J, Ganzle 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. https://doi.org/10.1080/19490976.2018.1526583
Van den Ende W, De Coninck B, Van LA (2004) Plant fructan exohydrolases: a role in signaling and defense? Trends Plant Sci 9:523–528. https://doi.org/10.1016/j.tplants.2004.09.008
Waterhouse AL, Chatterton NJ (1993) Glossary of fructan terms. In: Suzuki M, Chatterton JN (eds) Science and technology of fructans. CRC Press, Boca Raton, pp 1–7
Xu M, Zhang L, Zhao F, Wang J, Zhao B, Zhou Z, Han Y (2021) Cloning and expression of levansucrase gene of Bacillus velezensis BM-2 and enzymatic synthesis of levan. Processes 9(2):317. https://doi.org/10.3390/pr9020317
Yokota A, Yamauchi O, Tomita F (1995) Production of inulotriose from inulin by inulin degrading enzyme from Streptomyces rochei. Lett Appl Microbiol 21:330–333. https://doi.org/10.1111/j.1472-765X.1995.tb01072.x
Yoshida M (2021) Fructan structure and metabolism in overwintering plants. Plants 10:933. https://doi.org/10.3390/plants10050933
Zhang T, Chi Z, Zhao CH, Chi ZM, Gong F (2010) Bioethanol production from hydrolysates of inulin and the tuber meal of Jerusalem artichoke by Saccharomyces sp. Bioresource Technol 101:8166–8170. https://doi.org/10.1016/j.biortech.2010.06.013
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This work was supported by Office of National Higher Education Science Research and Innovation Policy Council under Program Management Unit-B (Project B05F630053); and also, was supported by Salt-tolerant Rice Research Group, Khon Kaen University, Thailand.
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Khamwan, S., Boonlue, S. & Mongkolthanaruk, W. Production of fructan synthesis/hydrolysis of endophytic bacteria involved in inulin production in Jerusalem artichoke. 3 Biotech 12, 296 (2022). https://doi.org/10.1007/s13205-022-03374-1
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DOI: https://doi.org/10.1007/s13205-022-03374-1