Investigation of impact of siderophore and process variables on production of iron enriched Saccharomyces boulardii by Plackett-Burman design.
Pseudomonas aeruginosa
Saccharomyces boulardii
Bioaccumulation
Design of experiments
Enrichment
Fe
FeY
Iron enriched yeast
Plackett–Burman
Probiotic yeast
Process variable
Siderophore
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
01 Oct 2024
01 Oct 2024
Historique:
received:
25
02
2024
accepted:
16
08
2024
medline:
2
10
2024
pubmed:
2
10
2024
entrez:
1
10
2024
Statut:
epublish
Résumé
The primary cause of anemia worldwide is due to poor diet and iron deficiency. Iron (Fe) enriched yeast can be the most effective way to manage anemia because of the capability for biotransformation of mineral to organic and bioavailable iron. To overcome the low richness of yeast, the use of siderophore as cellular iron carriers is a new approach. In this research, for the first time the potential of siderophore in increasing the Fe enrichment of Saccharomyces boulardii (S. boulardii), which is important because of its probiotic properties and resistance to different stresses, has been investigated to produce of potential iron supplements. For this purpose, siderophore was produced by Pseudomonas aeruginosa (P. aeruginosa). Siderophore impact, along with ten other independent process variables, has been studied on the efficiency of iron biotransformation by the Plackett-Burman design (PBD). The results showed that the highest biotransformation yield was 17.77 mg Fe/g dry cell weight (DCW) in the highest biomass weight of 9 g/l. Iron concentration is the most important variable, with contributions of 46% and 70.79% for biomass weight and biotransformation, respectively, followed by fermentation time, agitation speed, and KH
Identifiants
pubmed: 39353969
doi: 10.1038/s41598-024-70467-7
pii: 10.1038/s41598-024-70467-7
doi:
Substances chimiques
Siderophores
0
Iron
E1UOL152H7
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
22813Informations de copyright
© 2024. The Author(s).
Références
Ramos-Alonso, L. et al. Molecular strategies to increase yeast iron accumulation and resistance. Metallomics 10, 1245–1256. https://doi.org/10.1039/c8mt00124c (2018).
doi: 10.1039/c8mt00124c
pubmed: 30137082
Gafter-Gvili, A., Schechter, A. & Rozen-Zvi, B. Iron deficiency anemia in chronic kidney disease. Acta Haematol. 142, 44–50. https://doi.org/10.1159/000496492 (2019).
doi: 10.1159/000496492
pubmed: 30970355
Halterman, J. S., Kaczorowski, J. M., Aligne, C. A., Auinger, P. & Szilagyi, P. G. Iron deficiency and cognitive achievement among school-aged children and adolescents in the United States. Pediatrics. 107, 1381–1386. https://doi.org/10.1542/peds.107.6.1381 (2001).
doi: 10.1542/peds.107.6.1381
pubmed: 11389261
World Health Organization. Anaemia in women and children [Internet]. https://www.who.int/data/gho/data/themes/topics/anaemia_in_women_and_children (2023).
World Health Organization. The Global Prevalence of Anaemia in 2011 43 (World Health Organization, 2015).
Amils, R. C. Encyclopedia of Astrobiology 293 (Springer, 2011). https://doi.org/10.1007/978-3-642-11274-4 .
doi: 10.1007/978-3-642-11274-4
Zhang, X. G. et al. Preparation of S-iron-enriched yeast using siderophores and its effect on iron deficiency anemia in rats. Food Chem. 365, 130508. https://doi.org/10.1016/j.foodchem.2021.130508 (2021).
doi: 10.1016/j.foodchem.2021.130508
pubmed: 34247046
Yuan, Y., Guo, X., He, X., Zhang, B. & Liu, S. Construction of a high-biomass, iron-enriched yeast strain and study on distribution of iron in the cells of Saccharomyces cerevisiae. Biotechnol. Lett. 26, 311–315. https://doi.org/10.1023/b:bile.0000015449.30186.90 (2004).
doi: 10.1023/b:bile.0000015449.30186.90
pubmed: 15055767
Gaudreau, H., Tompkins, T. A. & Champagne, C. P. The distribution of iron in iron-enriched cells of Saccharomyces cerevisiae. Acta Aliment. 30, 355–356. https://doi.org/10.1556/AAlim.30.2001.4.4 (2001).
doi: 10.1556/AAlim.30.2001.4.4
Paš, M., Piškur, B., Šuštarič, M. & Raspor, P. Iron enriched yeast biomass—a promising mineral feed supplement. Bioresour. Technol. 98, 1622–1628. https://doi.org/10.1016/j.biortech.2006.06.002 (2007).
doi: 10.1016/j.biortech.2006.06.002
pubmed: 16935492
Pirman, T. & Orešnik, A. Fe bioavailability from Fe-enriched yeast biomass in growing rats. Animal 6, 221–226. https://doi.org/10.1017/S1751731111001546 (2012).
doi: 10.1017/S1751731111001546
pubmed: 22436179
McFarland, L. V. Systematic review and meta-analysis of Saccharomyces boulardii in adult patients. World J. Gastroenterol. 16, 2202–2222. https://doi.org/10.3748/wjg.v16.i18.2202 (2010).
doi: 10.3748/wjg.v16.i18.2202
pubmed: 20458757
pmcid: 2868213
Hudson, L. E. et al. Characterization of the probiotic yeast Saccharomyces boulardii in the healthy mucosal immune system. PLoS One. 11, e0153351. https://doi.org/10.1371/journal.pone.0153351 (2016).
doi: 10.1371/journal.pone.0153351
pubmed: 27064405
pmcid: 4827847
Ramírez-Cota, G. Y., López-Villegas, E. O., Jiménez-Aparicio, A. R. & Hernández-Sánchez, H. Modeling the ethanol tolerance of the probiotic yeast Saccharomyces cerevisiae var. boulardii CNCM I-745 for its possible use in a functional beer. Probiot. Antimicrob. 13, 187–194. https://doi.org/10.1007/s12602-020-09680-5 (2021).
doi: 10.1007/s12602-020-09680-5
Graff, S., Chaumeil, J. C., Boy, P., Lai-Kuen, R. & Charrueau, C. Formulations for protecting the probiotic Saccharomyces boulardii from degradation in acidic condition. Biol. Pharm. Bull. 31, 266–272. https://doi.org/10.1248/bpb.31.266 (2008).
doi: 10.1248/bpb.31.266
pubmed: 18239285
Martínez-Garay, C. A., De Llanos, R., Romero, A. M., Martínez-Pastor, M. T. & Puig, S. Responses of Saccharomyces cerevisiae strains from different origins to elevated iron concentrations. Appl. Environ. Microbiol. 82, 1906–1916. https://doi.org/10.1128/AEM.03464-15 (2016).
doi: 10.1128/AEM.03464-15
pubmed: 26773083
pmcid: 4784042
Nowosad, K., Sujka, M., Pankiewicz, U., Miklavčič, D. & Arczewska, M. Pulsed electric field (Pef) enhances iron uptake by the yeast Saccharomyces cerevisiae. Biomolecules. 11, 850. https://doi.org/10.3390/biom11060850 (2021).
doi: 10.3390/biom11060850
pubmed: 34200319
pmcid: 8227778
Nowosad, K. & Sujka, M. The use of iron-enriched yeast for the production of flatbread. Molecules 26, 5204. https://doi.org/10.3390/molecules26175204 (2021).
doi: 10.3390/molecules26175204
pubmed: 34500637
pmcid: 8434235
De Serrano, L. O. Biotechnology of siderophores in high-impact scientific fields. Biomol. Concepts 8, 169–178. https://doi.org/10.1515/bmc-2017-0016 (2017).
doi: 10.1515/bmc-2017-0016
pubmed: 28889118
Soares, E. V. Perspective on the biotechnological production of bacterial siderophores and their use. Appl. Microbiol. Biotechnol. 106, 3985–4004. https://doi.org/10.1007/s00253-022-11995-y (2022).
doi: 10.1007/s00253-022-11995-y
pubmed: 35672469
Miethke, M. & Marahiel, M. A. Siderophore-based iron acquisition and pathogen control. Microbiol. Mol. Biol. Rev. 71, 453–551. https://doi.org/10.1128/MMBR.00012-07 (2007).
doi: 10.1128/MMBR.00012-07
Yun, C. W., Tiedeman, J. S., Moore, R. E. & Philpott, C. C. Siderophore-iron uptake in Saccharomyces cerevisiae: Identification of ferrichrome and fusarinine transporters. J. Biol. Chem. 275, 16354–16359. https://doi.org/10.1074/jbc.M001456200 (2000).
doi: 10.1074/jbc.M001456200
pubmed: 10748025
Jalal, M. A. F., Love, S. K. & Van Der Helm, D. Siderophore mediated iron(III) uptake in Gliocladium virens 2. Role of ferric mono- and dihydroxamates as iron transport agents. J. Inorg. Biochem. 29, 259–267. https://doi.org/10.1016/0162-0134(87)80033-8 (1987).
doi: 10.1016/0162-0134(87)80033-8
pubmed: 2953864
Gaensly, F., Wille, G. M. F. C., Brand, D. & Bonfim, T. M. B. Iron enriched Saccharomyces cerevisiae maintains its fermenting power and bakery properties. Food Sci. Technol. 31, 980–983 (2011).
doi: 10.1590/S0101-20612011000400025
Kyyaly, M. A., Powell, C. & Ramadan, E. Preparation of iron-enriched baker’s yeast and its efficiency in recovery of rats from dietary iron deficiency. Nutrition. 31, 1155–1164. https://doi.org/10.1016/j.nut.2015.04.017 (2015).
doi: 10.1016/j.nut.2015.04.017
pubmed: 26233875
Strobel, R. J. & Sullivan, G. R. Experimental design for improvement of fermentations. In Manual of Industrial Microbiology and Biotechnology (eds. Demain, A. L. and Davies, J. E.) 80–93 (ASM, 1999).
Schwyn, B. & Neilands, J. B. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160, 47–56. https://doi.org/10.1016/0003-2697(87)90612-9 (1987).
doi: 10.1016/0003-2697(87)90612-9
pubmed: 2952030
Lakshmanan, V. A natural rice rhizospheric bacterium abates arsenic accumulation in rice (Oryza sativa L.). Planta. 242, 1037–1050. https://doi.org/10.1007/s00425-015-2340-2 (2015).
doi: 10.1007/s00425-015-2340-2
pubmed: 26059607
Arnow, L. E. Colorimetric determination of the components of 3,4-dihydroxyphenylalanine-tyrosine mixtures. J. Biol. Chem. 118, 531–537. https://doi.org/10.1016/S0021-9258(18)74509-2 (1937).
doi: 10.1016/S0021-9258(18)74509-2
Payne, S. M. Detection, isolation, and characterization of siderophores. Meth. Enzymol. 235, 329–344. https://doi.org/10.1016/0076-6879(94)35151-1 (1994).
doi: 10.1016/0076-6879(94)35151-1
Malairuang, K., Krajang, M., Sukna, J., Rattanapradit, K. & Chamsart, S. High cell density cultivation of Saccharomyces cerevisiae with intensive multiple sequential batches together with a novel technique of fed-batch at cell level (FBC). Processes. 8, 1–26. https://doi.org/10.3390/pr8101321 (2020).
doi: 10.3390/pr8101321
Tafazzoli, K., Ghavami, M. & Khosravi-Darani, K. Production of iron enrisched Saccharomyces boulardii: Impact of process variables. Sci. Rep. 14, 4844. https://doi.org/10.1038/s41598-024-55433-7 (2024).
doi: 10.1038/s41598-024-55433-7
pubmed: 38418660
pmcid: 10902395
Wang, R., Lorantfy, B., Fusco, S., Olsson, L. & Franzén, C. J. Analysis of methods for quantifying yeast cell concentration in complex lignocellulosic fermentation processes. Sci. Rep. 11, 11293. https://doi.org/10.1038/s41598-021-90703-8 (2021).
doi: 10.1038/s41598-021-90703-8
pubmed: 34050249
pmcid: 8163860
Olivares-Marin, I. K., González-Hernández, J. C., Regalado-Gonzalez, C. & Madrigal-Perez, L. A. Saccharomyces cerevisiae exponential growth kinetics in batch culture to analyze respiratory and fermentative metabolism. J. Vis. Exp. 2018, 58192. https://doi.org/10.3791/58192 (2018).
doi: 10.3791/58192
Zhang, X. G. et al. Effects of Fe-YM1504 on iron deficiency anemia in rats. Food Funct. 7, 3184–3192. https://doi.org/10.1039/C6FO00423G (2016).
doi: 10.1039/C6FO00423G
pubmed: 27326788
Zhang, X. G., Peng, Y. N., Li, X. R., Ma, G. D. & Chen, X. Q. Screening of iron-enriched fungus from natural environment and evaluation of organically bound iron bioavailability in rats. Food Sci. Technol. Int. 35, 58–66. https://doi.org/10.1590/1678-457X.6454 (2015).
doi: 10.1590/1678-457X.6454
Sabatier, M. et al. Iron bioavailability from fresh cheese fortified with iron-enriched yeast. Eur. J. Nutr. 56, 1551–1560. https://doi.org/10.1007/s00394-016-1200-6 (2017).
doi: 10.1007/s00394-016-1200-6
pubmed: 27029918
Gaensly, F., Picheth, G., Brand, D. & Bonfim, T. M. B. The uptake of different iron salts by the yeast Saccharomyces cerevisiae. Braz. J. Microbiol. 45, 491–494. https://doi.org/10.1590/s1517-83822014000200016 (2014).
doi: 10.1590/s1517-83822014000200016
pubmed: 25242932
pmcid: 4166273
Esmaeili, S., Khosravi-Darani, K., Pourahmad, R. & Komeili, R. An experimental design for production of selenium-enriched yeast. World Appl. Sci. J. 19, 31–37. https://doi.org/10.5829/idosi.wasj.2012.19.01.2634 (2012).
doi: 10.5829/idosi.wasj.2012.19.01.2634
Nie, X. et al. ARTP mutagenesis promotes selenium accumulation in Saccharomyces boulardii. LWT. 168, 113916. https://doi.org/10.1016/j.lwt.2022.113916 (2022).
doi: 10.1016/j.lwt.2022.113916
Kitamura, D. H. et al. Selenium-enriched probiotic Saccharomyces boulardii CCT 4308 biomass production using low-cost sugarcane molasses medium. Braz. Arch. Biol. Technol. 64, e21200658. https://doi.org/10.1590/1678-4324-75years-2021200658 (2021).
doi: 10.1590/1678-4324-75years-2021200658
González-Salitre, L. et al. Physicochemical and microbiological parameters during the manufacturing of a beer-type fermented beverage using selenized Saccharomycesboulardii. Heliyon. 9, e21190. https://doi.org/10.1016/j.heliyon.2023.e21190 (2023).
doi: 10.1016/j.heliyon.2023.e21190
pubmed: 37928392
pmcid: 10622692
Hyrslova, I. et al. In vitro digestion and characterization of selenized Saccharomyces cerevisiae, Pichia fermentans and probiotic Saccharomyces boulardii. J. Trace Elem. Med. Biol. 83, 127402. https://doi.org/10.1016/j.jtemb.2024.127402 (2024).
doi: 10.1016/j.jtemb.2024.127402
pubmed: 38310829
Kwak, S. et al. Dissection and enhancement of prebiotic properties of yeast cell wall oligosaccharides through metabolic engineering. Biomaterials 282, 121379. https://doi.org/10.1016/j.biomaterials.2022.121379 (2022).
doi: 10.1016/j.biomaterials.2022.121379
pubmed: 35078005
Graus, M. S. et al. Mannan molecular substructures control nanoscale glucan exposure in Candida. Cell Rep. 24, 2432–2442. https://doi.org/10.1016/j.celrep.2018.07.088 (2018).
doi: 10.1016/j.celrep.2018.07.088
pubmed: 30157435
pmcid: 6204226
Gow, N. A. R. & Hube, B. Importance of the Candida albicans cell wall during commensalism and infection. Curr. Opin. Microbiol. 15, 406–412. https://doi.org/10.1016/j.mib.2012.04.005 (2012).
doi: 10.1016/j.mib.2012.04.005
pubmed: 22609181
Kodoi, R., Takahashi, T., Oka, O. & Urasaki, H. Inventors; Oriental Yeast Co Ltd, assignee. Method for producing high-zinc-content yeast extract, high-zinc-content yeast extract, foods, and agent for maintaining and restoring green color of vegetables. United States patent US20140212571A1. https://patents.google.com/patent/US20140212571A1/en (2014).
Choi, Y. Inventor; Barrick Gold Corp, assignee. Production of zinc sulphate concentrates from a dilute zinc sulphate solution. United States patent US20110165059A1. https://patents.google.com/patent/US20110165059A1/en (2011).
Polson, C., Sarkar, P., Incledon, B., Raguvaran, V. & Grant, R. Optimization of protein precipitation based upon effectiveness of protein removal and ionization effect in liquid chromatography-tandem mass spectrometry. Chromatogr. B Ana Technol. Biomed. Life Sci. 785, 263–275. https://doi.org/10.1016/s1570-0232(02)00914-5 (2003).
doi: 10.1016/s1570-0232(02)00914-5
El-Neggar, N. E. et al. Process development for scale-up production of a therapeutic L-asparaginase by Streptomyces brollosae NEAE-115 from shake flasks to bioreactor. Sci. Rep. 9, 13571. https://doi.org/10.1038/s41598-019-49709-6 (2019).
doi: 10.1038/s41598-019-49709-6
The oxygen-transferring ferment of respiration. Nobel Lecture. https://www.nobelprize.org/uploads/2018/06/warburg-lecture.pdf (1931).
Hazra, A. et al. Coenzyme and prosthetic group biosynthesis. Encycl. Microbiol. 79–88, 2009. https://doi.org/10.1016/B978-012373944-5.00069-9 (2009).
doi: 10.1016/B978-012373944-5.00069-9
Coote, N. & Kirsop, B. H. Factors responsible for the decrease in ph during beer fermentations. J. Inst. Brew. 82, 149–153. https://doi.org/10.1002/j.2050-0416.1976.tb03739.x (1976).
doi: 10.1002/j.2050-0416.1976.tb03739.x
Cox, C. D. & Adams, P. Siderophore activity of pyoverdin for Pseudomonas aeruginosa. Infect. Immun. 48, 130–138. https://doi.org/10.1128/iai.48.1.130-138.1985 (1985).
doi: 10.1128/iai.48.1.130-138.1985
pubmed: 3156815
pmcid: 261925
Sheykhi, F., Ahmadifard, N., Samadi, N. & Nematzadeh, K. The effect of different concentrations of organic and inorganic zinc on the growth and zinc content in yeast (Saccharomyces Cerevisiae). BJM 7, 103–109 (2019).
Shet, A. R., Patil, L., Hombalimath, V. S., Yaraguppi, D. & Udapudi, B. B. Enrichment of Saccharomyces cerevisiae with zinc and their impact on cell growth. Biotechnol. Bioinf. Bioeng. 1, 523–527 (2011).
Liu, X. F., Supek, F., Nelson, N. & Culotta, V. C. Negative control of heavy metal uptake by the Saccharomyces cerevisiae BSD2 gene. J. Biol. Chem. 272, 11763–11769. https://doi.org/10.1074/jbc.272.18.11763 (1997).
doi: 10.1074/jbc.272.18.11763
pubmed: 9115231
Zhang, B. B. & Cheung, P. C. K. A mechanistic study of the enhancing effect of Tween 80 on the mycelial growth and exopolysaccharide production by Pleurotus tuber-regium. Bioresour. Technol. 102, 8323–8326. https://doi.org/10.1016/j.biortech.2011.06.021 (2011).
doi: 10.1016/j.biortech.2011.06.021
pubmed: 21708463
Zhang, B. B., Chen, L. & Cheung, P. C. K. Two-dimensional gel electrophoresis analysis of mycelial cells treated with tween 80: Differentially expressed protein related to enhanced metabolite production. J. Agric. Food. Chem. 60, 10585–10591. https://doi.org/10.1021/jf303570d (2012).
doi: 10.1021/jf303570d
pubmed: 23013510
Liang, Y. et al. Influence of Tween-80 on the production and structure of water-insoluble curdlan from Agrobacterium sp.. Int. J. Biol Macromol. 106, 611–619. https://doi.org/10.1016/j.ijbiomac.2017.08.052 (2018).
doi: 10.1016/j.ijbiomac.2017.08.052
pubmed: 28807687
Li, Q., Lei, Y., Hu, G., Lei, Y. & Dan, D. Effects of Tween 80 on the liquid fermentation of Lentinus edodes. Food Sci. Biotechnol. 27, 1103–1109. https://doi.org/10.1007/s10068-018-0339-8 (2018).
doi: 10.1007/s10068-018-0339-8
pubmed: 30263840
pmcid: 6085267
Sheng, L., Zhu, G. & Tong, Q. Mechanism study of Tween 80 enhancing the pullulan production by Aureobasidium pullulans. Carbohydr. Polym. 97, 121–123. https://doi.org/10.1016/j.carbpol.2013.04.058 (2013).
doi: 10.1016/j.carbpol.2013.04.058
pubmed: 23769526
Tu, G., Wang, Y., Ji, Y. & Zou, X. The effect of Tween 80 on the polymalic acid and pullulan production by Aureobasidium pullulans CCTCC M2012223. World J. Microbiol. Biotechnol. 31, 219–226. https://doi.org/10.1007/s11274-014-1779-9 (2015).
doi: 10.1007/s11274-014-1779-9
pubmed: 25413862
Yin, H. et al. Evaluation of surfactant effect on β-poly (L-malic acid) production by Aureobasidium pullulans. Biotechnol. Biotechnol. Equip. 33, 954–966. https://doi.org/10.1080/13102818.2019.1631718 (2019).
doi: 10.1080/13102818.2019.1631718
Cui, J. et al. Tween 80 micelles loaded with Fe3O4 nanoparticles and artemisinin for combined oxygen-independent ferroptosis therapy of cancer. Pharmaceutics. 16, 639. https://doi.org/10.3390/pharmaceutics16050639 (2024).
doi: 10.3390/pharmaceutics16050639
pubmed: 38794301
pmcid: 11124998
Xu, H. X. et al. Degradation of fluoranthene by a newly isolated strain of Herbaspirillum chlorophenolicum from activated sludge. Biodegradation 22, 335–345. https://doi.org/10.1007/s10532-010-9403-7 (2011).
doi: 10.1007/s10532-010-9403-7
pubmed: 20711747
Jin, D., Jiang, X., Jing, X. & Ou, Z. Effects of concentration, head group, and structure of surfactants on the degradation of phenanthrene. J. Hazard Mater. 144, 215–221. https://doi.org/10.1016/j.jhazmat.2006.10.012 (2007).
doi: 10.1016/j.jhazmat.2006.10.012
pubmed: 17113708
Li, J. L. & Chen, B. H. Effect of nonionic surfactants on biodegradation of phenanthrene by a marine bacteria of Neptunomonas naphthovorans. J. Hazard Mater. 162, 66–73. https://doi.org/10.1016/j.jhazmat.2008.05.019 (2009).
doi: 10.1016/j.jhazmat.2008.05.019
pubmed: 18554784
Akhnazarova, S., Kafarov, V., Repyev, A. P. & Matskovsky, V. M. Experiment Optimization in Chemistry and Chemical Engineering (Mir, 1982).
Stowe, R. A. & Mayer, R. P. Efficient screening of process variables. J. Ind. Eng. Chem. 58, 36–40. https://doi.org/10.1021/IE50674A007 (1966).
doi: 10.1021/IE50674A007
El-Naggar, N. E., Haroun, S. A., El-Weshy, E. M., Metwally, E. A. & Sherief, A. A. Mathematical modeling for bioprocess optimization of a protein drug, uricase, production by Aspergillus welwitschiae strain 1–4. Sci. Rep. 9, 12971. https://doi.org/10.1038/s41598-019-49201-1 (2019).
doi: 10.1038/s41598-019-49201-1
pubmed: 31506445
pmcid: 6736946
Montgomery, D. C. Design and Analysis of Experiments 3rd edn. (Wiley, Uk, 1991).