The Bifidobacterium adolescentis BAD_1527 gene encodes GH43_22 α-L-arabinofuranosidase of AXH-m type.

Bifidobacterium adolescentis Arabinan Arabinoxylan Positional specificity Substrate specificity α-L-Arabinofuranosidase

Journal

AMB Express
ISSN: 2191-0855
Titre abrégé: AMB Express
Pays: Germany
ID NLM: 101561785

Informations de publication

Date de publication:
20 Jul 2024
Historique:
received: 21 04 2024
accepted: 25 06 2024
medline: 21 7 2024
pubmed: 21 7 2024
entrez: 20 7 2024
Statut: epublish

Résumé

Bifidobacterium adolescentis gene BAD_1527 has previously been suggested to code for a β-xylosidase (Kobayashi et al., Mar Drugs 18:174, 2020). Our detailed investigation of the substrate specificity of the GH43_22 protein using a wide spectrum of natural and artificial substrates showed that the enzyme hydrolyzed neither linear xylooligosaccharides nor glucuronoxylan. Xylose was released only from the artificial 4-nitrophenyl β-D-xylopyranoside (1.58 mU/mg). The corresponding α-L-arabinofuranoside was by three orders of magnitude better substrate (2.17 U/mg). Arabinose was the only monosaccharide liberated from arabinoxylan and α-1,3- or α-1,2-singly arabinosylated xylooligosaccharides. Moreover, the enzyme efficiently debranched sugar beet arabinan and singly arabinosylated α-1,5-L-arabinooligosaccharides, although short linear α-1,5-L-arabinooligosaccharides were also slowly degraded. On the other hand, debranched arabinan, arabinogalactan as well as 2,3-doubly arabinosylated main chain residues of arabinan and arabinoxylan did not serve as substrates. Thus, the enzyme encoded by the BAD_1527 gene is a typical α-L-arabinofuranosidase of AXH-m specificity.

Identifiants

pubmed: 39033088
doi: 10.1186/s13568-024-01738-9
pii: 10.1186/s13568-024-01738-9
doi:

Types de publication

Journal Article

Langues

eng

Pagination

83

Subventions

Organisme : Agentúra na Podporu Výskumu a Vývoja
ID : APVV-20-0591
Organisme : Vedecká Grantová Agentúra MŠVVaŠ SR a SAV
ID : 2/0171/22

Informations de copyright

© 2024. The Author(s).

Références

Amaretti A, Bernardi T, Leonardi A, Raimondi S, Zanoni S, Rossi M (2013) Fermentation of xylooligosaccharides by Bifidobacterium adolescentis DSMZ 18350: kinetics, metabolism, and β-xylosidase activities. Appl Microbiol Biotechnol 97:3109–3117. https://doi.org/10.1007/s00253-012-4509-y
doi: 10.1007/s00253-012-4509-y pubmed: 23099913
Beylot M-H, Emami K, McKie VA, Gilbert HJ, Pell G (2001) Pseudomonas cellulosa expresses a single membrane-bound glycoside hydrolase family 51 arabinofuranosidase. Biochem J 358:599–605. https://doi.org/10.1042/bj3580599
doi: 10.1042/bj3580599 pubmed: 11535121 pmcid: 1222094
Derrien M, Turroni F, Ventura M, van Sinderen D (2022) Insights into endogenous Bifidobacterium species in the human gut microbiota during adulthood. Trends Microbiol 30:940–947. https://doi.org/10.1016/j.tim.2022.04.004
doi: 10.1016/j.tim.2022.04.004 pubmed: 35577716
Duranti S, Milani C, Lugli GA, Mancabelli L, Turroni F, Ferrario C, Mangifesta M, Viappiani A, Sánchez B, Margolles A, van Sinderen D, Ventura M (2016) Evaluation of genetic diversity among strains of the human gut commensal Bifidobacterium adolescentis. Sci Rep 6:23971. https://doi.org/10.1038/srep23971
doi: 10.1038/srep23971 pubmed: 27035119 pmcid: 4817515
Ebringerová A, Kramár A, Rendoš F, Domanský R (1967) Fractional extraction of hemicellulose from wood of hornbeam (Carpinus betulus L.). Holzforschung 21:74–77. https://doi.org/10.1515/hfsg.1967.21.3.74
doi: 10.1515/hfsg.1967.21.3.74
Fujita K, Sakamoto A, Kaneko S, Kotake T, Tsumuraya Y, Kitahara K (2019) Degradative enzymes for type II arabinogalactan side chains in Bifidobacterium longum subsp. longum. Appl Microbiol Biotechnol 103:1299–1310. https://doi.org/10.1007/s00253-018-9566-4
doi: 10.1007/s00253-018-9566-4 pubmed: 30564851
Jones DR, Thomas D, Alger N, Ghavidel A, Inglis GD, Abbott DW (2018) SACCHARIS: an automated pipeline to streamline discovery of carbohydrate active enzyme activities within polyspecific families and de novo sequence datasets. Biotechnol Biofuels 11:27. https://doi.org/10.1186/s13068-018-1027-x
doi: 10.1186/s13068-018-1027-x pubmed: 29441125 pmcid: 5798181
Kobayashi M, Kumagai Y, Yamamoto Y, Yasui H, Kishimura H (2020) Identification of a key enzyme for the hydrolysis of β-(1→3)-xylosyl linkage in red alga dulse xylooligosaccharide from Bifidobacterium adolescentis. Mar Drugs 18:174. https://doi.org/10.3390/md18030174
doi: 10.3390/md18030174 pubmed: 32245121 pmcid: 7142710
Komeno M, Hayamizu H, Fujita K, Ashida H (2019) Two novel α-L-arabinofuranosidases from Bifidobacterium longum subsp. longum belonging to glycoside hydrolase family 43 cooperatively degrade arabinan. Appl Environ Microbiol 85:02582–02618. https://doi.org/10.1128/AEM.02582-18
doi: 10.1128/AEM.02582-18
Komeno M, Yoshihara Y, Kawasaki J, Nabeshima W, Maeda K, Sasaki Y, Fujita K, Ashida H (2022) Two α-L-arabinofuranosidases from Bifidobacterium longum subsp. longum are involved in arabinoxylan utilization. Appl Microbiol Biotechnol 106:1957–1965. https://doi.org/10.1007/s00253-022-11845-x
doi: 10.1007/s00253-022-11845-x pubmed: 35235007
Kormelink FJM, Searl-Van Leeuwen MJF, Wood TM, Voragen AGJ (1991) Purification and characterization of a (1,4)-β-D-arabinoxylan arabinofuranohydrolase from Aspergillus awamori. Appl Microbiol Biotechnol 35:753–758. https://doi.org/10.1007/BF00169890
doi: 10.1007/BF00169890
Kormelink FJM, Gruppen H, Voragen AGJ (1993) Mode of action of (1,4)-β-D-arabinoxylan arabinofuranohydrolase (AXH) and α-L-arabinofuranosidases on alkali-extractable wheat-flour arabinoxylan. Carbohydr Res 249:345–353. https://doi.org/10.1016/0008-6215(93)84099-R
doi: 10.1016/0008-6215(93)84099-R pubmed: 8275504
Lagaert S, Pollet A, Delcour JA, Lavigne R, Courtin CM, Volckaert G (2010) Substrate specificity of three recombinant α-L-arabinofuranosidases from Bifidobacterium adolescentis and their divergent action on arabinoxylan and arabinoxylan oligosaccharides. Biochem Biophys Res Commun 402:644–650. https://doi.org/10.1016/j.bbrc.2010.10.075
doi: 10.1016/j.bbrc.2010.10.075 pubmed: 20971079
Liu Y, Vanderhaeghen S, Feiler W, Angelov A, Baudrexl M, Zverlov V, Liebl W (2021) Characterization of two α-L-arabinofuranosidases from Acetivibrio mesophilus and their synergistic effect in degradation of arabinose-containing substrates. Microorganisms 9:1467. https://doi.org/10.3390/microorganisms9071467
doi: 10.3390/microorganisms9071467 pubmed: 34361903 pmcid: 8307384
Park J-M, Jang M-U, Oh GW, Lee E-H, Kang J-H, Song Y-B, Han NS, Kim T-J (2015) Synergistic action modes of arabinan degradation by exo- and endo-arabinosyl hydrolases. J Microbiol Biotechnol 25:227–233. https://doi.org/10.4014/jmb.1411.11055
doi: 10.4014/jmb.1411.11055 pubmed: 25433551
Rudjito RC, Jiménez-Quero A, Muñoz MDCC, Kuil T, Olsson L, Stringer MA, Mørkeberg Krogh KBR, Eklöf J, Vilaplana F (2023) Arabinoxylan source and xylanase specificity influence the production of oligosaccharides with prebiotic potential. Carbohydr Polym 320:121233. https://doi.org/10.1016/j.carbpol.2023.121233
doi: 10.1016/j.carbpol.2023.121233 pubmed: 37659797
Sakka M, Yamada K, Kitamura T, Kunitake E, Kimura T, Sakka K (2019) The modular arabinanolytic enzyme Abf43A-Abf43B-Abf43C from Ruminiclostridium josui consists of three GH43 modules classified in different subfamilies. Enzyme Microb Technol 124:23–31. https://doi.org/10.1016/j.enzmictec.2019.01.011
doi: 10.1016/j.enzmictec.2019.01.011 pubmed: 30797476
Sasaki Y, Komeno M, Ishiwata A, Horigome A, Odamaki T, Xiao J-Z, Tanaka K, Ito Y, Kitahara K, Ashida H, Fujita K (2022) Mechanism of cooperative degradation of gum Arabic arabinogalactan protein by Bifidobacterium longum surface enzymes. Appl Environ Microbiol 88:e02187-e2221. https://doi.org/10.1128/aem.02187-21
doi: 10.1128/aem.02187-21 pubmed: 35108084 pmcid: 8939339
Si Z, Cai Y, Zhao L, Han L, Wang F, Yang X, Gao X, Lu M, Liu W (2023) Structure and function characterization of the α-L-arabinofuranosidase from the white-rot fungus Trametes hirsuta. Appl Microbiol Biotechnol 107:3967–3981. https://doi.org/10.1007/s00253-023-12561-w
doi: 10.1007/s00253-023-12561-w pubmed: 37178306
Taylor EJ, Smith NL, Turkenburg JP, D’Souza S, Gilbert HJ, Davies GJ (2006) Structural insight into the ligand specificity of a thermostable family 51 arabinofuranosidase, Araf51, from Clostridium thermocellum. Biochem J 395:31–37. https://doi.org/10.1042/BJ20051780
doi: 10.1042/BJ20051780 pubmed: 16336192 pmcid: 1409695
van den Broek LAM, Lloyd RM, Beldman G, Verdoes JC, McCleary BV, Voragen AGJ (2005) Cloning and characterization of arabinoxylan arabinofuranohydrolase-D3 (AXHd3) from Bifidobacterium adolescentis DSM20083. Appl Microbiol Biotechnol 67:641–647. https://doi.org/10.1007/s00253-004-1850-9
doi: 10.1007/s00253-004-1850-9 pubmed: 15650848
Van Laere KMJ, Beldman G, Voragen AGJ (1997) A new arabinofuranohydrolase from Bifidobacterium adolescentis able to remove arabinosyl residues from double-substituted xylose units in arabinoxylan. Appl Microbiol Biotechnol 47:231–235. https://doi.org/10.1007/s002530050918
doi: 10.1007/s002530050918 pubmed: 9114514
Van Laere KMJ, Voragen CHL, Kroef T, van den Broek LAM, Beldman G, Voragen AGJ (1999) Purification and mode of action of two different arabinoxylan arabinofuranohydrolases from Bifidobacterium adolescentis DSM 20083. Appl Microbiol Biotechnol 51:606–613. https://doi.org/10.1007/s002530051439
doi: 10.1007/s002530051439
Wang A, Zhong Q (2024) Drying of probiotics to enhance the viability during preparation, storage, food application, and digestion: a review. Compr Rev Food Sci Food Saf 23:1–30. https://doi.org/10.1111/1541-4337.13287
doi: 10.1111/1541-4337.13287
Zhang XJ, Wang L, Wang S, Chen ZL, Li YH (2021) Contributions and characteristics of two bifunctional GH43 β-xylosidase/α-L-arabinofuranosidases with different structures on the xylan degradation of Paenibacillus physcomitrellae strain XB. Microbiol Res 253:126886. https://doi.org/10.1016/j.micres.2021.126886
doi: 10.1016/j.micres.2021.126886 pubmed: 34687975

Auteurs

Walid Fathallah (W)

Institute of Chemistry, Slovak Academy of Sciences, Dúbravská cesta 9, 845 38, Bratislava, Slovakia.
Faculty of Science, Beni-Suef University, Beni-Suef, 625 11, Egypt.

Vladimír Puchart (V)

Institute of Chemistry, Slovak Academy of Sciences, Dúbravská cesta 9, 845 38, Bratislava, Slovakia. vladimir.puchart@savba.sk.

Classifications MeSH