645
Views
0
CrossRef citations to date
0
Altmetric
Research Paper

Two extracellular α-arabinofuranosidases are required for cereal-derived arabinoxylan metabolism by Bifidobacterium longum subsp. longum

, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, & show all
Article: 2353229 | Received 26 Feb 2024, Accepted 03 May 2024, Published online: 16 May 2024

References

  • Barko PC, McMichael MA, Swanson KS, Williams DA. The gastrointestinal microbiome: a review. Veterinary Internal Medicne. 2018;32(1):9–20. doi:10.1111/jvim.14875.
  • O’Callaghan A, van Sinderen D. Bifidobacteria and their role as members of the human gut microbiota. Front Microbiol. 2016;7. doi:10.3389/fmicb.2016.00925.
  • Turroni F, Peano C, Pass DA, Foroni E, Severgnini M, Claesson MJ, Kerr C, Hourihane J, Murray D, Fuligni F. et al. Diversity of bifidobacteria within the infant gut microbiota. PLOS ONE. 2012;7(5):e36957. doi:10.1371/journal.pone.0036957.
  • Arboleya S, Bottacini F, O’Connell-Motherway M, Ryan CA, Ross RP, van Sinderen D, Stanton C. Gene-trait matching across the Bifidobacterium longum pan-genome reveals considerable diversity in carbohydrate catabolism among human infant strains. BMC Genomics. 2018;19(1). doi:10.1186/s12864-017-4388-9.
  • Ventura M, Canchaya C, Tauch A, Chandra G, Fitzgerald GF, Chater KF, van Sinderen D. Genomics of Actinobacteria: tracing the evolutionary history of an ancient phylum. Microbiol Mol Biol R. 2007;71(3):495–548. doi:10.1128/mmbr.00005-07.
  • Arboleya S, Watkins C, Stanton C, Ross RP. Gut bifidobacteria populations in human health and aging. Front Microbiol. 2016;7. doi:10.3389/fmicb.2016.01204.
  • Modesto M, Ngom-Bru C, Scarafile D, Bruttin A, Pruvost S, Sarker SA, Ahmed T, Sakwinska O, Mattarelli P, Duboux S. Bifidobacterium longum subsp. iuvenis subsp. nov. a novel subspecies isolated from the faeces of weaning infants. Int J Syst Evol Microbiol. 2023;73(10). doi:10.1099/ijsem.0.006013.
  • Schell M, Karmirantzou M, Snel B, Vilanova D, Berger B, Pessi G, Zwahlen MC, Desiere F, Bork P, Delley M. et al. The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. PNAS. 2002;99(22):14422–14427. doi:10.1073/pnas.212527599.
  • Fukuda S, Toh H, Hase K, Oshima K, Nakanishi Y, Yoshimura K, Tobe T, Clarke JM, Topping DL, Suzuki T. et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature. 2011;469(7331):543–549. doi:10.1038/nature09646.
  • Stanton C, Ross RP, Fitzgerald GF, Van Sinderen D. Fermented functional foods based on probiotics and their biogenic metabolites. Curr Opin Biotechnol. 2005;16(2):198–203. doi:10.1016/j.copbio.2005.02.008.
  • Flint HJ, Scott KP, Duncan SH, Louis P, Forano E. Microbial degradation of complex carbohydrates in the gut. Gut Microbes. 2012;3(4):289–306. doi:10.4161/gmic.19897.
  • Komeno M, Hayamizu H, Fujita K, Ashidaa H. Two novel α-larabinofuranosidases from Bifidobacterium longum subsp. longum belonging to glycoside hydrolase family 43 cooperatively degrade arabinan. Appl Environ Microbiol. 2019;85(6). doi:10.1128/AEM.02582-18.
  • Fang F, Mukherjee I, Okoniewska M, Yao T, Campanella OH, Hamaker BR. Soluble corn arabinoxylan has desirable material properties for high incorporation in expanded cereal extrudates. Food Hydrocoll. 2022;133:133. doi:10.1016/j.foodhyd.2022.107939.
  • Kale MS, Pai DA, Hamaker BR, Campanella OH. Structure-function relationships for corn bran arabinoxylans. J Cereal Sci. 2010;52(3):368–372. doi:10.1016/j.jcs.2010.06.010.
  • Wang J, Bai J, Fan M, Li T, Li Y, Qian H, Wang L, Zhang H, Qi X, Rao Z. Cereal-derived arabinoxylans: structural features and structure–activity correlations. Trends Food Sci Technol. 2020;96:157–165. doi:10.1016/j.tifs.2019.12.016.
  • Whistler RL, Masak E Jr. Enzymatic hydrolysis of Xylan. J Am Chem Soc. 1955;77(5):1241–1243. doi:10.1021/ja01610a042.
  • Drula E, Garron ML, Dogan S, Lombard V, Henrissat B, Terrapon N. The carbohydrate-active enzyme database: functions and literature. Nucleic Acids Res. 2022;50(D1):D571–D577. doi:10.1093/nar/gkab1045.
  • Kaji A, Saheki T. Endo-arabinanase from Bacillus subtilis F-11. Biochima et Biophys Acta (BBA)-Enzymol. 1975;410(2):354–360. doi:10.1016/0005-2744(75)90237-5.
  • Howard BH, Jones G, Purdom MR. The pentosanases of some rumen bacteria. Biochem J. 1960;74(1):173. doi:10.1042/bj0740173.
  • Collins T, Gerday C, Feller G. Xylanases, xylanase families and extremophilic xylanases. FEMS Microbiol Rev. 2005;29(1):3–23. doi:10.1016/j.femsre.2004.06.005.
  • Rivière A, Moens F, Selak M, Maes D, Weckx S, De Vuyst L. The ability of bifidobacteria to degrade arabinoxylan oligosaccharide constituents and derived oligosaccharides is strain dependent. Appl Environ Microbiol. 2014;80(1):204–217. doi:10.1128/AEM.02853-13.
  • Komeno M, Yoshihara Y, Kawasaki J, Nabeshima W, Maeda K, Sasaki Y, Fujita K, Ashida H. Two α-l-arabinofuranosidases from Bifidobacterium longum subsp. longum are involved in arabinoxylan utilization. Appl Microbiol Biotechnol. 2022;106(5–6):1957–1965. doi:10.1007/s00253-022-11845-x.
  • Arzamasov AA, van Sinderen D, Rodionov DA. Comparative genomics reveals the regulatory complexity of bifidobacterial arabinose and arabino-oligosaccharide utilization. Front Microbiol. 2018;9. doi:10.3389/fmicb.2018.00776.
  • Kelly SM, O’Callaghan J, Kinsella M, Van Sinderen D. Characterisation of a hydroxycinnamic acid esterase from the Bifidobacterium longum subsp. longum taxon. Front Microbiol. 2018;9. doi:10.3389/fmicb.2018.02690.
  • Terzaghi BE, Sandine W. Improved medium for lactic streptococci and their bacteriophages. Appl Microbiol. 1975;29(6):807–813. doi:10.1128/am.29.6.807-813.1975.
  • Watson D, O’Connell Motherway M, Schoterman MHC, van Neerven RJJ, Nauta A, Van Sinderen D. Selective carbohydrate utilization by lactobacilli and bifidobacteria. J Appl Microbiol. 2013;114(4):1132–1146. doi:10.1111/jam.12105.
  • Yates A, Allen J, Amode RM, Azov AG, Barba M, Becerra A, Bhai J, Campbell LI, Carbajo Martinez M, Chakiachvili M, et al. Ensembl Genomes 2022: an expanding genome resource for non-vertebrates. Nucleic Acids Research. 2022;50(D1):D996–D1003. doi:10.1093/nar/gkab1007.
  • Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9(4):357–359. doi:10.1038/nmeth.1923.
  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25(17):3389–3402. doi:10.1093/nar/25.17.3389.
  • Green M, Sambrook J. Transformation of Escherichia coli by electroporation. Cold Spring Harb Protoc. 2020;(6):db–prot101220. doi:10.1101/pdb.prot101220.
  • Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227(5259):680–685. doi:10.1038/227680a0.
  • O’Callaghan A, Bottacini F, O’Connell Motherway M, van Sinderen D. Pangenome analysis of Bifidobacterium longum and site-directed mutagenesis through by-pass of restriction-modification systems. BMC Genomics. 2015;16(1). doi:10.1186/s12864-015-1968-4.
  • Shiver AL, Sun J, Culver R, Violette A, Nieckarz M, Paula Mattiello S, Kaur Sekhon P, Carlson HK, Wong D, Higginbottom S. et al. A mutant fitness compendium in bifidobacteria reveals molecular 1 determinants of colonization and host-microbe interactions 2 3. bioRxiv. Published online 2023. doi:10.1101/2023.08.29.555234.
  • Park MJ, Park MS, Ji GE. Improvement of electroporation-mediated transformation efficiency for a Bifidobacterium strain to a reproducibly high level. J Microbiol Methods. 2019;159:112–119. doi:10.1016/j.mimet.2018.11.019.
  • Ruiz L, Motherway MOC, Lanigan N, van Sinderen D, de Crécy-Lagard V. Transposon mutagenesis in Bifidobacterium breve: construction and characterization of a Tn5 transposon mutant library for Bifidobacterium breve UCC2003. PLOS ONE. 2013;8(5):e64699. doi:10.1371/journal.pone.0064699.
  • Huang PH, Chen S, Shiver AL, Culver RN, Huang KC, Buie CR, Waldor MK. M-TUBE enables large-volume bacterial gene delivery using a high-throughput microfluidic electroporation platform. PLOS Biol. 2022;20(9):e3001727. doi:10.1371/journal.pbio.3001727.
  • Isawa K, Hojo K, Yoda N, Kamiyama T, Makino S, Saito M, Sugano H, Mizoguchi C, Kurama S, Shibasaki M. et al. Isolation and identification of a new bifidogenic growth stimulator produced by Propionibacterium freudenreichii ET-3. Biosci Biotechnol Biochem. 2002;66(3):679–681. doi:10.1271/bbb.66.679.
  • Feehily C, O’Neill IJ, Walsh CJ, Moore RL, Killeen SL, Geraghty AA, Lawton EM, Byrne D, Sanchez-Gallardo R, Nori SRC. et al. Detailed mapping of bifidobacterium strain transmission from mother to infant via a dual culture-based and metagenomic approach. Nat Commun. 2023;14(1). doi:10.1038/s41467-023-38694-0.
  • Moore RL, Feehily C, Killeen SL, Yelverton CA, Geraghty AA, Walsh CJ, O’Neill IJ, Nielsan IB, Lawton EM, Sanchez-Gallardo R. et al. Ability of Bifidobacterium breve 702258 to transfer from mother to infant: the MicrobeMom randomized controlled trial. Am J Obstet Gynecol MFM. 2023;5(7):100994. doi:10.1016/j.ajogmf.2023.100994.
  • Hinz SWA, Pastink MI, Van Den Broek LAM, Vincken JP, Voragen AGJ. Bifidobacterium longum endogalactanase liberates galactotriose from type I galactans. Appl Environ Microbiol. 2005;71(9):5501–5510. doi:10.1128/AEM.71.9.5501-5510.2005.
  • O’Connell Motherway M, Fitzgerald GF, van Sinderen D. Metabolism of a plant derived galactose-containing polysaccharide by Bifidobacterium breve UCC2003. Microb Biotechnol. 2011;4(3):403–416. doi:10.1111/j.1751-7915.2010.00218.x.
  • Finn RD, Clements J, Eddy SR. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res. 2011;39(Suppl. 2):W29–W37. doi:10.1093/nar/gkr367.
  • Fujita K, Sakamoto A, Kaneko S, Kotake T, Tsumuraya Y, Kitahara K. Degradative enzymes for type II arabinogalactan side chains in Bifidobacterium longum subsp. longum. Appl Microbiol Biotechnol. 2019;103(3):1299–1310. doi:10.1007/s00253-018-9566-4.
  • Chang C, Tesar C, Li X, Kim Y, Rodionov DA, Joachimiak A. A novel transcriptional regulator of L-arabinose utilization in human gut bacteria. Nucleic Acids Res. 2015;43(21):10546–10559. doi:10.1093/nar/gkv1005.
  • Pokusaeva K, Fitzgerald GF, Van Sinderen D. Carbohydrate metabolism in bifidobacteria. Genes Nutr. 2011;6(3):285–306. doi:10.1007/s12263-010-0206-6.
  • Boekhorst J, Been MWHJ D, Kleerebezem M, Siezen RJ. Genome-wide detection and analysis of cell wall-bound proteins with LPxTG-like sorting motifs. J Bacteriol. 2005;187(14):4928–4934. doi:10.1128/JB.187.14.4928-4934.2005.
  • Zimmermann L, Stephens A, Nam SZ, Rau D, Kübler J, Lozajic M, Gabler F, Söding J, Lupas AN, Alva V. A completely reimplemented MPI bioinformatics toolkit with a New HHpred Server at its core. J Mol Biol. 2018;430(15):2237–2243. doi:10.1016/j.jmb.2017.12.007.
  • Mckee LS, Peña MJ, Rogowski A, Jackson A, Lewis RJ, York WS, Krogh KBRM, Viksø-Nielsen A, Skjøt M, Gilbert HJ. et al. Introducing endo-xylanase activity into an exo-acting arabinofuranosidase that targets side chains. Proc Natl Acad Sci. 2012;109(17):6537–6542. doi:10.1073/pnas.1117686109.
  • Santos CR, Polo CC, Costa MCMF, Nascimento AFZ, Meza AN, Cota J, Hoffmam ZB, Honorato RV, Oliveira PSL, Goldman GH. et al. Mechanistic strategies for catalysis adopted by evolutionary distinct family 43 arabinanases. J Biol Chem. 2014;289(11):7362–7373. doi:10.1074/jbc.M113.537167.
  • De Sanctis D, Inácio JM, Lindley PF, De Sá-Nogueira I, Bento I. New evidence for the role of calcium in the glycosidase reaction of GH43 arabinanases. FEBS J. 2010;277(21):4562–4574. doi:10.1111/j.1742-4658.2010.07870.x.
  • Vandermarliere E, Bourgois TM, Winn MD, Van Campenhout S, Volckaert G, Delcour JA, Strelkov SV, Rabijns A, Courtin CM. Structural analysis of a glycoside hydrolase family 43 arabinoxylan arabinofuranohydrolase in complex with xylotetraose reveals a different binding mechanism compared with other members of the same family. Biochem J. 2009;418(1):39–47. doi:10.1042/BJ20081256.
  • Savard P, Roy D. Determination of differentially expressed genes involved in arabinoxylan degradation by Bifidobacterium longum NCC2705 using real-time RT-PCR. Probiotics Antimicrob Proteins. 2009;1(2):121–129. doi:10.1007/s12602-009-9015-x.
  • Sonnenburg JL, Chen CTL, Gordon JI, Eisen J. Genomic and metabolic studies of the impact of probiotics on a model gut symbiont and host. PLOS Biol. 2006;4(12):2213–2226. doi:10.1371/journal.pbio.0040413.
  • Gosalbes MJ, Pérez-González JA, Gonzalez R, Navarro A. Two beta-glycanase genes are clustered in bacillus polymyxa: molecular cloning, expression, and sequence analysis of genes encoding a xylanase and an endo-beta-(1, 3)-(1, 4)-glucanase. J Bacteriol. 1991;173(23):7705–7710. doi:10.1128/jb.173.23.7705-7710.1991.
  • Cartmell A, McKee LS, Pena MJ, Larsbrink J, Brumer H, Kaneko S, Ichinose H, Lewis RJ, Viksø-Nielsen A, Gilbert HJ. et al. The structure and function of an arabinan-specific α-1,2- arabinofuranosidase identified from screening the activities of bacterial GH43 glycoside hydrolases. J Biol Chem. 2011;286(17):15483–15495. doi:10.1074/jbc.M110.215962.
  • Gibson GR, Probert HM, Van LJ, Rastall RA, Roberfroid MB. Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutr Res Rev. 2004;17(2):259–275. doi:10.1079/nrr200479.
  • Bindels LB, Delzenne NM, Cani PD, Walter J. Opinion: towards a more comprehensive concept for prebiotics. Nat Rev Gastroenterol Hepatol. 2015;12(5):303–310. doi:10.1038/nrgastro.2015.47.
  • O’Neill IJ, Sanchez Gallardo R, Saldova R, Murphy EF, Cotter PD, McAuliffe FM, van Sinderen D. Maternal and infant factors that shape neonatal gut colonization by bacteria. Expert Rev Gastroenterol Hepatol. 2020;14(8):651–664. doi:10.1080/17474124.2020.1784725.
  • Likotrafiti E, Tuohy KM, Gibson GR, Rastall RA. An invitro study of the effect of probiotics, prebiotics and synbiotics on the elderly faecal microbiota. Anaerobe. 2014;27:50–55. doi:10.1016/j.anaerobe.2014.03.009.
  • Neyrinck AM, Possemiers S, Druart C, van de Wiele T, de Backer F, Cani PD, Larondelle Y, Delzenne NM, Brennan L. Prebiotic effects of wheat Arabinoxylan related to the increase in bifidobacteria, roseburia and bacteroides/prevotella in diet-induced obese mice. PLOS ONE. 2011;6(6):e20944. doi:10.1371/journal.pone.0020944.
  • Grootaert C, Verstraete W, Van de Wiele T, Microbial metabolism and prebiotic potency of arabinoxylan oligosaccharides in the human intestine. Trends Food Sci Technol. 2007;18(2):64–71. doi:10.1016/j.tifs.2006.08.004.
  • Rogowski A, Briggs JA, Mortimer JC, Tryfona T, Terrapon N, Lowe EC, Baslé A, Morland C, Day AM, Zheng H. et al. Glycan complexity dictates microbial resource allocation in the large intestine. Nat Commun. 2015;6(1):6. doi:10.1038/ncomms8481.
  • Blanco G, Ruiz L, Tamés H, Ruas-Madiedo P, Fdez-Riverola F, Sánchez B, Lourenço A, Margolles A. Revisiting the metabolic capabilities of Bifidobacterium longum susbp. longum and Bifidobacterium longum subsp. infantis from a glycoside hydrolase perspective. Microorganisms. 2020;8(5):723. doi:10.3390/microorganisms8050723.
  • Russell DA, Ross RP, Fitzgerald GF, Stanton C. Metabolic activities and probiotic potential of bifidobacteria. Int J Food Microbiol. 2011;149(1):88–105. doi:10.1016/j.ijfoodmicro.2011.06.003.
  • Maldonado-Gómez MX, Martínez I, Bottacini F, O’Callaghan A, Ventura M, van Sinderen D, Hillmann B, Vangay P, Knights D, Hutkins RW. et al. Stable engraftment of Bifidobacterium longum AH1206 in the human gut depends on individualized features of the resident microbiome. Cell Host Microbe. 2016;20(4):515–526. doi:10.1016/j.chom.2016.09.001.
  • Den Broek LAM V, Lloyd RM, Beldman G, Verdoes JC, McCleary BV, Voragen AGJ. Cloning and characterization of arabinoxylan arabinofuranohydrolase-D3 (AXHd3) from Bifidobacterium adolescentis DSM20083. Appl Microbiol Biotechnol. 2005;67(5):641–647. doi:10.1007/s00253-004-1850-9.
  • De Vries W, Stouthamer AH. Pathway of glucose fermentation in relation to the taxonomy of bifidobacteria. J Bacteriol. 1967;93(2):574–576. doi:10.1128/jb.93.2.574-576.1967.