Effect of linear and branched fructans on growth and probiotic characteristics of seven Lactobacillus spp. isolated from an autochthonous beverage from Chiapas, Mexico.
Antibiotic resistance
Fructans
Growth kinetic parameters
Lactic acid bacteria
Simulated gastrointestinal conditions
Journal
Archives of microbiology
ISSN: 1432-072X
Titre abrégé: Arch Microbiol
Pays: Germany
ID NLM: 0410427
Informations de publication
Date de publication:
04 Jun 2022
04 Jun 2022
Historique:
received:
02
10
2021
accepted:
12
05
2022
revised:
11
05
2022
entrez:
6
6
2022
pubmed:
7
6
2022
medline:
9
6
2022
Statut:
epublish
Résumé
The effect that the fructans of Cichorium intybus and Agave salmiana have on health, as well as on the growth of some Lactobacillus species, has been demonstrated. The aim of this work was to evaluate the effect of linear and branched fructans on the growth of seven strains and some probiotic characteristics. The molecular identification of seven strains was performed. Moreover, the growth, resistance to antibiotics and simulated gastrointestinal conditions were also evaluated when these microorganisms were grown in a culture medium containing agave and chicory fructans. The strains were identified as Lactiplantibacillus plantarum, Lactiplantibacillus pentosus, Lactiplantibacillus fabifermentans and Lactiplantibacillus paraplantarum. The results suggest that the seven Lactobacillus strains were able to grow using agave (branched) and chicory (linear) fructans. The linear and branched fructans statistically influenced the kinetic parameters. The specific growth rate varied between 0.270 and 0.573 h
Identifiants
pubmed: 35661269
doi: 10.1007/s00203-022-02984-w
pii: 10.1007/s00203-022-02984-w
doi:
Substances chimiques
Culture Media
0
Fructans
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
364Subventions
Organisme : Consejo Nacional de Ciencia y Tecnología
ID : 817440
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Alcántara Hernández RJ, Rodríguez Álvarez JA, Valenzuela Encinas C, Gutiérrez Miceli FA, Castañón González H, Marsch R, Ayora Talavera T, Dendooven L (2010) The bacterial community in ‘taberna’ a traditional beverage of Southern Mexico. Lett Appl Microb 51(5):558–563. https://doi.org/10.1111/j.1472-765X.2010.02934.x
doi: 10.1111/j.1472-765X.2010.02934.x
Ayala Montero MA, Hernández Sánchez D, Pinto Ruiz R, González Muñoz SS, Bárcena Gama JR, Hernández Mendo O, Torres Salado N (2018) Prebiotic effect of two sources of inulin on in vitro growth of Lactobacillus salivarius and Enterococcus faecium. Rev Mex de Cienc Pecuarias 9(2):346–361. https://doi.org/10.22319/rmcp.v9i2.4488
doi: 10.22319/rmcp.v9i2.4488
Barbera E, Grandi A, Borella L, Bertucco A, Sforza E (2019) Continuous cultivation as a method to assess the maximum specific growth rate of photosynthetic organisms. Front Bioeng Biotechnol 7(274):1–12. https://doi.org/10.3389/fbioe.2019.00274
doi: 10.3389/fbioe.2019.00274
Begley M, Hill C, Gahan CG (2006) Bile salt hydrolase activity in probiotics. Appl Environ Microb 72(3):1729–1738. https://doi.org/10.1128/AEM.72.3.1729-1738.2006
doi: 10.1128/AEM.72.3.1729-1738.2006
Bindu A, Lakshmidevi N (2020) Identification and in vitro evaluation of probiotic attributes of lactic acid bacteria isolated from fermented food sources. Arch Microb 203:579–595. https://doi.org/10.1007/s00203-020-02037-0
doi: 10.1007/s00203-020-02037-0
Brenner DJ, Krieg NR, Staley JT, Garrity GM, Bergey DH (2005) Bergey’s manual of systematic bacteriology, 2nd edn. Springer, New York
doi: 10.1007/0-387-28021-9
Buntin N, Hongpattarakere T, Ritari J, Douillard FP, Paulin L, Boeren S, de Vos WM (2016) An inducible Operon is involved in inulin utilization in Lactobacillus plantarum strains, as revealed by comparative proteogenomics and metabolic profiling. Appl Environ Microb 83(2):2402–2416. https://doi.org/10.1128/aem.02402-16
doi: 10.1128/aem.02402-16
Byrne CS, Chambers ES, Morrison DJ, Frost G (2015) The role of short chain fatty acids in appetite regulation and energy homeostasis. Int J Obes 39(9):1331–1338. https://doi.org/10.1038/ijo.2015.84
doi: 10.1038/ijo.2015.84
Castillo Andrade AI, Rivera Bautista C, Ruiz Cabrera MA, Soria Guerra RE, Fuentes Ahumada C, García Chávez E, Grajales Lagunes A (2019) Agave salmiana fructans as gut health promoters: prebiotic activity and inflammatory response in Wistar healthy rats. Int J Biol Macromol 1(136):785–795. https://doi.org/10.1016/j.ijbiomac.2019.06.045
doi: 10.1016/j.ijbiomac.2019.06.045
Chowdhury R, Banerjee D, Bhattacharya P. (2016) The prebiotic influence of inulin on growth rate and antibiotic sensitivity of Lactobacillus casei. Int J Pharm Pharm Sci 8(4):181–184. https://innovareacademics.in/journals/index.php/ijpps/article/view/10199/4160 Accessed 26 Aug 2021
da Silva SS, Converti A, Dimitrov Todorov S, Dominguez J, de Souza Oliveira RP (2015) Effect of inulin on growth and bacteriocin production by Lactobacillus plantarum in stationary and shaken cultures. Int J of Food Sci Technol 50(4):864–870. https://doi.org/10.1111/ijfs.12711
doi: 10.1111/ijfs.12711
De Bruyne K, Camu N, De Vuyst L, Vandamme P (2009) Lactobacillus fabifermentans sp. nov. and Lactobacillus cacaonum sp. nov., isolated from Ghanaian cocoa fermentations. Int J Syst Evol Microb 59(1):7–12. https://doi.org/10.1099/ijs.0.001172-0
doi: 10.1099/ijs.0.001172-0
Escobar Ramírez MC, Jaimez Ordaz J, Escorza Iglesias VA, Rodríguez Serrano GM, Contreras López E, Ramírez Godínez J, Castañeda Ovando A, Morales Estrada AI, Felix Reyes N, González Olivares LG (2020) Lactobacillus pentosus ABHEAU-05: an in vitro digestion resistant lactic acid bacterium isolated from a traditional fermented Mexican beverage. Rev Argent Microb 52(4):305–314. https://doi.org/10.1016/j.ram.2019.10.005
doi: 10.1016/j.ram.2019.10.005
Falony G, Vlachou A, Verbrugghe K, De Vuyst L (2006) Cross-feeding between Bifidobacterium longum BB536 and acetate-converting, butyrate-producing colon bacteria during growth on oligofructose. Appl Environ Microb 72:7835–7841. https://doi.org/10.1128/AEM.01296-06
doi: 10.1128/AEM.01296-06
Farinha RL, Sabo SV, Porto MC, Souza EC, Oliveira MN, Oliveira RPS (2015) Influence of prebiotic ingredients on the growth kinetics and bacteriocin production by Lactococcus lactis. Chem Eng Trans 43:313–318. https://doi.org/10.3303/CET1543053
doi: 10.3303/CET1543053
Godínez Hernández CI, Aguirre Rivera JR, Juárez Flores BI, Ortiz Pérez MD, Becerra Jiménez J. (2016) Extraction and characterization of Agave salmiana Otto ex Salm-Dyck fructans. Rev Chap Ser Cien For Amb 22(1):59–72. https://www.redalyc.org/articulo.oa?id=62943324004 Accessed 12 Sep 2021
Guerra Giacon T, Goise Cunha GC, Pontes Eliodório K, de Souza Oliveira RP, Olitta Basso T (2021) Homo-and heterofermentative lactobacilli are differently affected by lignocellulosic inhibitory compounds. bioRxiv. https://doi.org/10.1101/2021.01.18.427060
doi: 10.1101/2021.01.18.427060
Hardy H, Harris J, Lyon E, Beal J, Foey AD (2013) Probiotics, prebiotics and immunomodulation of gut mucosal defenses: homeostasis and Immunopathology. Nutrients 5:1869–1912. https://doi.org/10.3390/nu5061869
doi: 10.3390/nu5061869
pubmed: 23760057
pmcid: 3725482
Hernández Rosas F, Castilla Marroquín JD, Loeza Corte J, Lizardi Jimenez M, Hernández Martínez R (2021) The importance of carbon and nitrogen sources on exopolysaccharide synthesis by lactic acid bacteria and their industrial importance. Rev Mex De Ing Quím 20(3):1–21. https://doi.org/10.24275/rmiq/Bio2429
doi: 10.24275/rmiq/Bio2429
James M, Velastegui E, Cruz MA (2017) Evaluation of culture conditions of Lactobacillus acidophilus y Lactobacillus casei on laboratory scale, with inulin as carbon source. Bionatura 2(1):235–240. https://doi.org/10.21931/RB/2017.02.01.4
doi: 10.21931/RB/2017.02.01.4
Jasso Padilla I, Juárez Flores B, Alvarez Fuentes G, De la Cruz MA, González Ramírez J, Moscosa Santillán M, Martinez Gutierrez F (2016) Effect of prebiotics of Agave salmiana fed to healthy wistar rats. J Sci Food Agric 97(2):556–563. https://doi.org/10.1002/jsfa.7764
doi: 10.1002/jsfa.7764
pubmed: 27097820
Jurado Gámez H, Calpa Yamá F, Chaspuengal Tulcán A (2014) Determinación de parámetros cinéticos de Lactobacillus casei en dos medios probióticos. Veterinaria y Zootecnía 8(2):15–35. https://doi.org/10.17151/vetzo.2014.8.2.2
doi: 10.17151/vetzo.2014.8.2.2
Kaplan H, Hutkins R (2003) Metabolism of fructooligosaccharides by Lactobacillus paracasei 1195. Appl Environ Microb 69:2217–2222. https://doi.org/10.1128/AEM.69.4.2217-2222.2003
doi: 10.1128/AEM.69.4.2217-2222.2003
Kapoor G, Saigal S, Elongavan A (2017) Action and resistance mechanisms of antibiotics: a guide for clinicians. J Anaesthesiol Clin Pharm 33(3):300–305. https://doi.org/10.4103/joacp.JOACP_349_15
doi: 10.4103/joacp.JOACP_349_15
Kechagia M, Basoulis D, Konstantopoulou S, Dimitriadi D, Gyftopoulou K, Skarmoutsou N, Fakiri EM (2013) Health benefits of probiotics: a review. ISRN Nut 2:481–651. https://doi.org/10.5402/2013/481651
doi: 10.5402/2013/481651
Kleerebezem M, Boekhorst J, van Kranenburg R, Molenaar D, Kuipers OP, Leer R, Tarchini R, Peters SA, Sandbrink HM, Fiers MW, Stiekema W, Lankhorst RM, Bron PA, Hoffer SM, Groot MN, Kerkhoven R, de Vries M, Ursing B, de Vos WM, Siezen RJ (2003) Complete genome sequence of Lactobacillus plantarum WCFS1. Proc Natl Acad Sci USA 100:1990–1995. https://doi.org/10.1073/pnas.0337704100
doi: 10.1073/pnas.0337704100
pubmed: 12566566
pmcid: 149946
Liu Y, Tang H, Lin Z, Xu P (2015) Mechanisms of acid tolerance in bacteria and prospects in biotechnology and bioremediation. Biotechnol Adv 33:1484–1492. https://doi.org/10.1016/j.biotechadv.2015.06.001
doi: 10.1016/j.biotechadv.2015.06.001
pubmed: 26057689
Mahboubi M, Kazempour N. (2016) The effects of inulin on characteristics of Lactobacillus paracasei TD3 (IBRC-M 10784) as probiotic bacteria in vitro. Arch Iran Med 19(2):92–95. https://pubmed.ncbi.nlm.nih.gov/26838078/ Accessed 18 Sep 2021
Makras L, Van Acker G, De Vuyst L (2005) Lactobacillus paracasei subsp. paracasei 8700: 2 degrades inulin-type fructans exhibiting different degrees of polymerization. Appl Environ Microb 71(11):6531–6537. https://doi.org/10.1128/AEM.71.11.6531-6537.2005
doi: 10.1128/AEM.71.11.6531-6537.2005
Martínez Gutierrez F, Ratering S, Juárez Flores B, Godínez Hernandez C, Geissler Plaum R, Prell F, Zorn H, Czermak P, Schnell S (2017) Potential use of Agave salmiana as a prebiotic that stimulates the growth of probiotic bacteria. Int J of Food Sci Technol 84:151–159. https://doi.org/10.1016/j.lwt.2017.05.044
doi: 10.1016/j.lwt.2017.05.044
Mendoza Avendaño C, Meza Gordillo R, Ovando Chacón SL, Luján-Hidalgo MC, Ruiz Cabrera MA, Grajales Lagunes A, Ruiz Valdiviezo VM, Gutiérrez Miceli FA, Abud-Archila M (2019) Evaluation of bioactive and anti-nutritional compounds during soy milk fermentation with Lactobacillus plantarum BAL-03-ITTG and Lactobacillus fermentum BAL-21-ITTG. Rev Mex Ing Quím 18:967–978. https://doi.org/10.24275/uam/izt/dcbi/revmexingquim/2019v18n3/Mendoza
doi: 10.24275/uam/izt/dcbi/revmexingquim/2019v18n3/Mendoza
Mora-López JL, Reyes Agüero JA, Flores Flores JL, Peña Valdivia CB, Aguirre Rivera JR (2011) Variación morfológica y humanización de la sección Salmiana del género Agave. Agrociencia 45:465–477. http://www.scielo.org.mx/scielo.php?script=sci_arttext&pid=S1405-31952011000400006
Moreno Vilet L, García Hernández MH, Delgado Portales RE, Corral Fernández NM, Cortez Espinoza N, Ruiz Cabrera MA, Portales Pérez DP (2014) In vitro assessment of agave fructans (Agave salmiana) as prebiotics and immune system activators. Int J Biol Macromol 63:181–187. https://doi.org/10.1016/j.ijbiomac.2013.10.039
doi: 10.1016/j.ijbiomac.2013.10.039
pubmed: 24211431
Mykytczuk NCS, Trevors JT, Leduc LG, Ferroni GD (2007) Fluorescence polarization in studies of bacterial cytoplasmic membrane fluidity under environmental stress. Prog Biophys Mol Biol 95(3):60–82. https://doi.org/10.1016/j.pbiomolbio.2007.05.001
doi: 10.1016/j.pbiomolbio.2007.05.001
pubmed: 17628643
Nishimura M, Ohkawara T, Kanayama T, Kitagawa K, Nishimura H, Nishihira J (2015) Effects of the extract from roasted chicory (Cichorium intybus L.) root containing inulin-type fructans on blood glucose, lipid metabolism, and fecal properties. J Tradit Complement Med 5(3):161–167. https://doi.org/10.1016/j.jtcme.2014.11.016
doi: 10.1016/j.jtcme.2014.11.016
pubmed: 26151029
pmcid: 4488567
Ouoba LI, Kando C, Parkouda C, Sawadogo Lingani H, Diawara B, Sutherland JP (2012) The microbiology of Bandji, palm wine of Borassus akeassii from Burkina Faso: identification and genotypic diversity of yeast, lactic acid and acetic acid bacteria. J Appl Microb 113:1428–1441. https://doi.org/10.1111/jam.12014
doi: 10.1111/jam.12014
Özcelik S, Kuley E, Özogul F (2016) Formation of lactic, acetic, succinic, propionic, formic and butyric acid by lactic acid bacteria. LWT-Food Sci Technol 73:536–542. https://doi.org/10.1016/j.lwt.2016.06.066
doi: 10.1016/j.lwt.2016.06.066
Paludan Müller C, Madsen M, Sophanodora P, Gram L, Moller PL (2002) Fermentation and microflora of plaa-som, a thai fermented fish product prepared with different salt concentrations. Int J Food Microb 73:61–70. https://doi.org/10.1016/s0168-1605(01)00688-2
doi: 10.1016/s0168-1605(01)00688-2
Petkova N, Vrancheva R, Denev P, Ivanov I, Pavlov A. (2014) HPLC-RID method for determination of inulin and fructooligosaccharides. Acta Sci Nat 1:107. https://www.researchgate.net/publication/262456529_HPLC_-_RID_method_for_determination_of_inulin_and_fructooligosaccharides Accessed 18 Sep 2021
Picot A, Lacroix C (2004) Encapsulation of bifidobacteria in whey protein-based microcapsules and survival in simulated gastrointestinal conditions and in yoghurt. Int Dairy J 14:505–515. https://doi.org/10.1016/j.idairyj.2003.10.008
doi: 10.1016/j.idairyj.2003.10.008
Prangthip P, Surasiang R, Charoensiri R, Leardkamolkarn V, Komindr S, Yamborisut U, Vanavichit A, Kongkachuichai R (2013) Amelioration of hyperglycemia hyperlipidemia, oxidative stress and inflammation in streptozotocin-induced diabetic rats fed a high fat diet by riceberry supplement. J Funct Foods 5:195–203. https://doi.org/10.1016/j.jff.2012.10.005
doi: 10.1016/j.jff.2012.10.005
Rusznyák A, Vladár P, Szabó G, Márialigeti K, Borsodi AK (2008) Phylogenetic and metabolic bacterial diversity of Phragmites australis periphyton communities in two hungarian soda ponds. Extremophiles 12:763–773. https://doi.org/10.1007/s00792-008-0183-5
doi: 10.1007/s00792-008-0183-5
pubmed: 18679563
Saarela M, Mogensen G, Fondén R, Mättö J, Mattila Sandholm T (2000) Probiotic bacteria: safety, functional and technological properties. J Biotech 84(3):197–215. https://doi.org/10.1016/s0168-1656(00)00375-8
doi: 10.1016/s0168-1656(00)00375-8
Saulnier MA, Molenaar D, de Vos WM, Kolida GGR, S, (2007) Identification of prebiotic fructooligosaccharide metabolism in Lactobacillus plantarum WCFS1 through microarrays. Appl Environ Microb 73:1753–1765. https://doi.org/10.1128/AEM.01151-06
doi: 10.1128/AEM.01151-06
Sridhar J, Eiteman M, Wiegel J (2000) Elucidation of enzymes in fermentation pathways used by Clostridium thermosuccino genes growing on inulin. Appl Environ Microb 66(1):246–250. https://doi.org/10.1128/AEM.66.1.246-251.2000
doi: 10.1128/AEM.66.1.246-251.2000
Szutowska J, Gwiazdowska D (2020) Probiotic potential of lactic acid bacteria obtained from fermented curly kale juice. Arch Microb 203:975–988. https://doi.org/10.1007/s00203-020-02095-4
doi: 10.1007/s00203-020-02095-4
Thongprayoon C, Kaewput W, Hatch ST, Bathini T, Sharma K, Wijarnpreecha K, Ungprasert P, D’Costa M, Mao MA, Cheungp-asitporn W (2019) Effects of probiotics on inflammation and uremictoxins among patients on dialysis: a systematic review and meta-analysis. Dig Dis Sci 64:469–479. https://doi.org/10.1007/s10620-018-5243-9
doi: 10.1007/s10620-018-5243-9
pubmed: 30099652
Wang C, Cui Y, Qu X (2017) Mechanisms and improvement of acid resistance in lactic acid bacteria. Arch Microb 200(2):195–201. https://doi.org/10.1007/s00203-017-1446-2
doi: 10.1007/s00203-017-1446-2
Wu C, Huang J, Zhou R (2014) Progress in engineering acid stress resistance of lactic acid bacteria. Appl Microb Biotechnol 98:1055–1063. https://doi.org/10.1007/s00253-013-5435-3
doi: 10.1007/s00253-013-5435-3
Zheng J, Wittouck S, Salvetti E, Franz C, Harris H, Mattarelli P, O’Toole P, Pot B, Vandamme P, Walter J, Watanabe K, Wuyts S, Felis G, Gänzle M, Lebeer S (2020) A taxonomic note on the genus Lactobacillus: description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. Int J Syst Evol Microb 70:2782–2858. https://doi.org/10.1099/ijsem.0.004107
doi: 10.1099/ijsem.0.004107
Zhu Y, Liu J, Lopez JM, Mills DA (2020) Inulin fermentation by lactobacilli and bifidobacteria from dairy calves. Appl Environ Microb 87(1):1–12. https://doi.org/10.1128/aem.01738-20
doi: 10.1128/aem.01738-20