Comparative Pangenomics of the Mammalian Gut Commensal Bifidobacterium longum
Abstract
:1. Introduction
2. Materials and Methods
2.1. Bifidobacterial Propagation and Isolation
2.2. Whole Genome Sequencing
2.3. Genomic and Pangenomic Analyses
2.4. Species-Wide Phylogenetic Inference
2.5. Carbohydrate Fermentation Phenotyping
3. Results
3.1. Bifidobacterium longum General Genome Characteristics
3.2. Bifidobacterium longum Inferred Phylogeny
3.3. Average Nucleotide Identity Analyses
3.4. The Bifidobacterium longum Pangenome
3.5. Comparative Pangenomics between Bifidobacterium longum Subspecies
3.6. Variation within the Bifidobacterium longum Subsp. Infantis HMO Gene Cluster
3.7. Bifidobacterium longum Carbohydrate Metabolism Phenotypes
4. Discussion
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Turroni, F.; van Sinderen, D.; Ventura, M. Genomics and ecological overview of the genus Bifidobacterium. Int. J. Food Microbiol. 2011, 149, 37–44. [Google Scholar] [CrossRef] [PubMed]
- Odamaki, T.; Bottacini, F.; Kato, K.; Mitsuyama, E.; Yoshida, K.; Horigome, A.; Xiao, J.-z.; van Sinderen, D. Genomic diversity and distribution of Bifidobacterium longum subsp. longum across the human lifespan. Sci. Rep. 2018, 8, 85. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Candela, M.; Perna, F.; Carnevali, P.; Vitali, B.; Ciati, R.; Gionchetti, P.; Rizzello, F.; Campieri, M.; Brigidi, P. Interaction of probiotic Lactobacillus and Bifidobacterium strains with human intestinal epithelial cells: Adhesion properties, competition against enteropathogens and modulation of IL-8 production. Int. J. Food Microbiol. 2008, 125, 286–292. [Google Scholar] [CrossRef] [PubMed]
- Hütt, P.; Shchepetova, J.; Loivukene, K.; Kullisaar, T.; Mikelsaar, M. Antagonistic activity of probiotic lactobacilli and bifidobacteria against entero-and uropathogens. J. Appl. Microbiol. 2006, 100, 1324–1332. [Google Scholar] [CrossRef] [PubMed]
- Furrie, E.; Macfarlane, S.; Kennedy, A.; Cummings, J.H.; Walsh, S.V.; O’neil, D.A.; Macfarlane, G.T. Synbiotic therapy (Bifidobacterium longum/Synergy 1) initiates resolution of inflammation in patients with active ulcerative colitis: A randomised controlled pilot trial. Gut 2005, 54, 242–249. [Google Scholar] [CrossRef] [PubMed]
- Matteuzzi, D.; Crociani, F.; Zani, O.; Trovatelli, L.D. Bifidobacterium suis n. sp.: A new species of the genus Bifidobacterium isolated from pig faces. Z. Allg. Mikrobiol. 1971, 11, 387–395. [Google Scholar] [CrossRef]
- Mattarelli, P.; Bonaparte, C.; Pot, B.; Biavati, B. Proposal to reclassify the three biotypes of Bifidobacterium longum as three subspecies: Bifidobacterium longum subsp. longum subsp. nov., Bifidobacterium longum subsp. infantis comb. nov. and Bifidobacterium longum subsp. suis comb. nov. Int. J. Syst. Evol. Microbiol. 2008, 58, 5. [Google Scholar] [CrossRef] [Green Version]
- Sakata, S.; Kitahara, M.; Sakamoto, M.; Hayashi, H.; Fukuyama, M.; Benno, Y. Unification of Bifidobacterium infantis and Bifidobacterium suis as Bifidobacterium longum. Int. J. Syst. Evol. Microbiol. 2002, 52, 1945–1951. [Google Scholar]
- Pokusaeva, K.; Fitzgerald, G.F.; van Sinderen, D. Carbohydrate metabolism in Bifidobacteria. Genes Nutr. 2011, 6, 285. [Google Scholar] [CrossRef] [Green Version]
- Rossi, M.; Corradini, C.; Amaretti, A.; Nicolini, M.; Pompei, A.; Zanoni, S.; Matteuzzi, D. Fermentation of fructooligosaccharides and inulin by bifidobacteria: A comparative study of pure and fecal cultures. Appl. Environ. Microbiol. 2005, 71, 6150–6158. [Google Scholar] [CrossRef] [Green Version]
- Fukuda, S.; Toh, H.; Hase, K.; Oshima, K.; Nakanishi, Y.; Yoshimura, K.; Tobe, T.; Clarke, J.M.; Topping, D.L.; Suzuki, T. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 2011, 469, 543–547. [Google Scholar] [CrossRef] [PubMed]
- Fukuda, S.; Toh, H.; Taylor, T.D.; Ohno, H.; Hattori, M. Acetate-producing bifidobacteria protect the host from enteropathogenic infection via carbohydrate transporters. Gut Microbes 2012, 3, 449–454. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Den Besten, G.; Lange, K.; Havinga, R.; van Dijk, T.H.; Gerding, A.; van Eunen, K.; Müller, M.; Groen, A.K.; Hooiveld, G.J.; Bakker, B.M. Gut-derived short-chain fatty acids are vividly assimilated into host carbohydrates and lipids. Am. J. Physiol. Gastrointest. Liver Physiol. 2013, 305, G900–G910. [Google Scholar] [CrossRef] [PubMed]
- LoCascio, R.G.; Desai, P.; Sela, D.A.; Weimer, B.; Mills, D.A. Broad conservation of milk utilization genes in Bifidobacterium longum subsp. infantis as revealed by comparative genomic hybridization. Appl. Environ. Microbiol. 2010, 76, 7373–7381. [Google Scholar] [CrossRef] [Green Version]
- Sela, D.A.; Chapman, J.; Adeuya, A.; Kim, J.H.; Chen, F.; Whitehead, T.R.; Lapidus, A.; Rokhsar, D.S.; Lebrilla, C.B.; German, J.B.; et al. The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. Proc. Natl. Acad. Sci. USA 2008, 105, 6. [Google Scholar] [CrossRef] [Green Version]
- De Leoz, M.L.A.; Wu, S.; Strum, J.S.; Niñonuevo, M.R.; Gaerlan, S.C.; Mirmiran, M.; German, J.B.; Mills, D.A.; Lebrilla, C.B.; Underwood, M.A. A quantitative and comprehensive method to analyze human milk oligosaccharide structures in the urine and feces of infants. Anal. Bioanal. Chem. 2013, 405, 4089–4105. [Google Scholar] [CrossRef] [Green Version]
- Dotz, V.; Rudloff, S.; Meyer, C.; Lochnit, G.; Kunz, C. Metabolic fate of neutral human milk oligosaccharides in exclusively breast-fed infants. Mol. Nutr. Food Res. 2015, 59, 355–364. [Google Scholar] [CrossRef]
- Chaplin, A.V.; Efimov, B.A.; Smeianov, V.V.; Kafarskaia, L.I.; Pikina, A.P.; Shkoporov, A.N. Intraspecies genomic diversity and long-term persistence of Bifidobacterium longum. PLoS ONE 2015, 10, e0135658. [Google Scholar] [CrossRef] [Green Version]
- Arboleya, S.; Bottacini, F.; O’Connell-Motherway, M.; Ryan, C.A.; Ross, R.P.; 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 Genom. 2018, 19, 33. [Google Scholar] [CrossRef]
- O’Callaghan, A.; Bottacini, F.; Motherway, M.C.; Van Sinderen, D. Pangenome analysis of Bifidobacterium longum and site-directed mutagenesis through by-pass of restriction-modification systems. BMC Genom. 2015, 16, 832. [Google Scholar] [CrossRef] [Green Version]
- Orban, J.I.; Patterson, J.A. Modification of the phosphoketolase assay for rapid identification of bifidobacteria. J. Microbiol. Methods 2000, 40, 221–224. [Google Scholar] [CrossRef]
- Milani, C.; Lugli, G.A.; Turroni, F.; Mancabelli, L.; Duranti, S.; Viappiani, A.; Mangifesta, M.; Segata, N.; van Sinderen, D.; Ventura, M. Evaluation of bifidobacterial community composition in the human gut by means of a targeted amplicon sequencing (ITS) protocol. FEMS Microbiol. Ecol. 2014, 90, 493–503. [Google Scholar] [CrossRef] [PubMed]
- Turroni, F.; Foroni, E.; Pizzetti, P.; Giubellini, V.; Ribbera, A.; Merusi, P.; Cagnasso, P.; Bizzarri, B.; de’Angelis, G.L.; Shanahan, F. Exploring the diversity of the bifidobacterial population in the human intestinal tract. Appl. Environ. Microbiol. 2009, 75, 1534–1545. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bankevich, A.; Nurk, S.; Antipov, D.; Gurevich, A.A.; Dvorkin, M.; Kulikov, A.S.; Lesin, V.M.; Nikolenko, S.I.; Pham, S.; Prjibelski, A.D. SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 2012, 19, 455–477. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Langmead, B.; Salzberg, S.L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 2012, 9, 357–359. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Walker, B.J.; Abeel, T.; Shea, T.; Priest, M.; Abouelliel, A.; Sakthikumar, S.; Cuomo, C.A.; Zeng, Q.; Wortman, J.; Young, S.K. Pilon: An integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 2014, 9, e112963. [Google Scholar] [CrossRef]
- Li, H.; Handsaker, B.; Wysoker, A.; Fennell, T.; Ruan, J.; Homer, N.; Marth, G.; Abecasis, G.; Durbin, R. The sequence alignment/map format and SAMtools. Bioinformatics 2009, 25, 2078–2079. [Google Scholar] [CrossRef] [Green Version]
- Wick, R.R.; Schultz, M.B.; Zobel, J.; Holt, K.E. Bandage: Interactive visualization of de novo genome assemblies. Bioinformatics 2015, 31, 3350–3352. [Google Scholar] [CrossRef] [Green Version]
- Brettin, T.; Davis, J.J.; Disz, T.; Edwards, R.A.; Gerdes, S.; Olsen, G.J.; Olson, R.; Overbeek, R.; Parrello, B.; Pusch, G.D. RASTtk: A modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci. Rep. 2015, 5, 8365. [Google Scholar] [CrossRef] [Green Version]
- Overbeek, R.; Olson, R.; Pusch, G.D.; Olsen, G.J.; Davis, J.J.; Disz, T.; Edwards, R.A.; Gerdes, S.; Parrello, B.; Shukla, M. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res. 2014, 42, D206–D214. [Google Scholar] [CrossRef]
- Seemann, T. Prokka: Rapid prokaryotic genome annotation. Bioinformatics 2014, 30, 2068–2069. [Google Scholar] [CrossRef] [PubMed]
- Chen, I.M.A.; Markowitz, V.M.; Chu, K.; Palaniappan, K.; Szeto, E.; Pillay, M.; Ratner, A.; Huang, J.; Andersen, E.; Huntemann, M. IMG/M: Integrated genome and metagenome comparative data analysis system. Nucleic Acids Res. 2016. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Benson, D.A.; Cavanaugh, M.; Clark, K.; Karsch-Mizrachi, I.; Ostell, J.; Pruitt, K.D.; Sayers, E.W. GenBank. Nucleic Acids Res. 2018, 46, D41. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Page, A.J.; Cummins, C.A.; Hunt, M.; Wong, V.K.; Reuter, S.; Holden, M.T.G.; Fookes, M.; Falush, D.; Keane, J.A.; Parkhill, J. Roary: Rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015, 31, 3691–3693. [Google Scholar] [CrossRef] [PubMed]
- Richter, M.; Rosselló-Móra, R. Shifting the genomic gold standard for the prokaryotic species definition. Proc. Natl. Acad. Sci. USA 2009, 106, 19126–19131. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pritchard, L.; Glover, R.H.; Humphris, S.; Elphinstone, J.G.; Toth, I.K. Genomics and taxonomy in diagnostics for food security: Soft-rotting enterobacterial plant pathogens. Anal. Methods 2016, 8, 12–24. [Google Scholar] [CrossRef]
- Sayers, E.W.; Agarwala, R.; Bolton, E.E.; Brister, J.R.; Canese, K.; Clark, K.; Connor, R.; Fiorini, N.; Funk, K.; Hefferon, T. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 2019, 47, D23. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Thompson, J.D.; Higgins, D.G.; Gibson, T.J. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994, 22, 4673–4680. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Silvestro, D.; Michalak, I. raxmlGUI: A graphical front-end for RAxML. Org. Divers. Evol. 2012, 12, 335–337. [Google Scholar] [CrossRef]
- Rambaut, A. FigTree v1. 4. Computer Program Distributed by the Author. Available online: http://tree.bio.ed.ac.uk/software/figtree (accessed on 25 November 2018).
- Huerta-Cepas, J.; Szklarczyk, D.; Forslund, K.; Cook, H.; Heller, D.; Walter, M.C.; Rattei, T.; Mende, D.R.; Sunagawa, S.; Kuhn, M. eggNOG 4.5: A hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Res. 2015, 44, D286–D293. [Google Scholar] [CrossRef] [Green Version]
- Huerta-Cepas, J.; Forslund, K.; Coelho, L.P.; Szklarczyk, D.; Jensen, L.J.; von Mering, C.; Bork, P. Fast genome-wide functional annotation through orthology assignment by eggNOG-mapper. Mol. Biol. Evol. 2017, 34, 2115–2122. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Potter, S.C.; Luciani, A.; Eddy, S.R.; Park, Y.; Lopez, R.; Finn, R.D. HMMER web server: 2018 update. Nucleic Acids Res. 2018, 46, W200–W204. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- El-Gebali, S.; Mistry, J.; Bateman, A.; Eddy, S.R.; Luciani, A.; Potter, S.C.; Qureshi, M.; Richardson, L.J.; Salazar, G.A.; Smart, A. The Pfam protein families database in 2019. Nucleic Acids Res. 2018, 47, D427–D432. [Google Scholar] [CrossRef] [PubMed]
- Lombard, V.; Golaconda Ramulu, H.; Drula, E.; Coutinho, P.M.; Henrissat, B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2013, 42, D490–D495. [Google Scholar] [CrossRef] [Green Version]
- Yin, Y.; Mao, X.; Yang, J.; Chen, X.; Mao, F.; Xu, Y. dbCAN: A web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 2012, 40, W445–W451. [Google Scholar] [CrossRef]
- Csűös, M. Count: Evolutionary analysis of phylogenetic profiles with parsimony and likelihood. Bioinformatics 2010, 26, 1910–1912. [Google Scholar] [CrossRef]
- Konstantinidis, K.T.; Tiedje, J.M. Genomic insights that advance the species definition for prokaryotes. Proc. Natl. Acad. Sci. USA 2005, 102, 2567–2572. [Google Scholar] [CrossRef] [Green Version]
- Kim, M.; Oh, H.-S.; Park, S.-C.; Chun, J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int. J. Syst. Evol. Microbiol. 2014, 64, 346–351. [Google Scholar] [CrossRef]
- Na, S.-I.; Kim, Y.O.; Yoon, S.-H.; Ha, S.-m.; Baek, I.; Chun, J. UBCG: Up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction. J. Microbiol. 2018, 56, 281–285. [Google Scholar] [CrossRef]
- Eddy, S. HMMER3: A New Generation of Sequence Homology Search Software. 2010. Available online: http://hmmer.janelia.org (accessed on 25 April 2018).
- Hyatt, D.; Chen, G.-L.; LoCascio, P.F.; Land, M.L.; Larimer, F.W.; Hauser, L.J. Prodigal: Prokaryotic gene recognition and translation initiation site identification. BMC Bioinform. 2010, 11, 119. [Google Scholar] [CrossRef] [Green Version]
- Katoh, K.; Standley, D.M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 2013, 30, 772–780. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stamatakis, A. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014, 30, 1312–1313. [Google Scholar] [CrossRef]
- Yanokura, E.; Oki, K.; Makino, H.; Modesto, M.; Pot, B.; Mattarelli, P.; Biavati, B.; Watanabe, K. Subspeciation of Bifidobacterium longum by multilocus approaches and amplified fragment length polymorphism: Description of B. longum subsp. suillum subsp. nov., isolated from the faeces of piglets. Syst. Appl. Microbiol. 2015, 38, 305–314. [Google Scholar] [CrossRef] [PubMed]
- Lugli, G.A.; Milani, C.; Duranti, S.; Mancabelli, L.; Mangifesta, M.; Turroni, F.; Viappiani, A.; van Sinderen, D.; Ventura, M. Tracking the taxonomy of the genus Bifidobacterium based on a phylogenomic approach. Appl. Environ. Microbiol. 2018, 84. [Google Scholar] [CrossRef] [Green Version]
- Cordeiro, R.L.; Pirolla, R.A.S.; Persinoti, G.F.; Gozzo, F.C.; de Giuseppe, P.O.; Murakami, M.T. N-glycan Utilization by Bifidobacterium Gut Symbionts Involves a Specialist β-Mannosidase. J. Mol. Biol. 2019, 431, 732–747. [Google Scholar] [CrossRef]
- Bertelli, C.; Pillonel, T.; Torregrossa, A.; Prod’hom, G.; Fischer, C.J.; Greub, G.; Giannoni, E. Bifidobacterium longum bacteremia in preterm infants receiving probiotics. Clin. Infect. Dis. 2014, 60, 924–927. [Google Scholar] [CrossRef] [Green Version]
- Esaiassen, E.; Hjerde, E.; Cavanagh, J.P.; Simonsen, G.S.; Klingenberg, C. Bifidobacterium Bacteremia: Clinical Characteristics and a Genomic Approach to Assess Pathogenicity. J. Clin. Microbiol. 2017, 55, 2234–2248. [Google Scholar] [CrossRef] [Green Version]
- Freitas, A.C.; Hill, J.E. Quantification, isolation and characterization of Bifidobacterium from the vaginal microbiomes of reproductive aged women. Anaerobe 2017, 47, 145–156. [Google Scholar] [CrossRef]
- Garrido, D.; Ruiz-Moyano, S.; Mills, D.A. Release and utilization of N-acetyl-D-glucosamine from human milk oligosaccharides by Bifidobacterium longum subsp. infantis. Anaerobe 2012, 18, 430–435. [Google Scholar] [CrossRef]
- Wanker, E.; Huber, A.; Schwab, H. Purification and characterization of the Bacillus subtilis levanase produced in Escherichia coli. Appl. Environ. Microbiol. 1995, 61, 1953–1958. [Google Scholar]
- Yin, X.; Chambers, J.R.; Barlow, K.; Park, A.S.; Wheatcroft, R. The gene encoding xylulose-5-phosphate/fructose-6-phosphate phosphoketolase (xfp) is conserved among Bifidobacterium species within a more variable region of the genome and both are useful for strain identification. FEMS Microbiol. Lett. 2005, 246, 251–257. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Milani, C.; Lugli, G.A.; Duranti, S.; Turroni, F.; Mancabelli, L.; Ferrario, C.; Mangifesta, M.; Hevia, A.; Viappiani, A.; Scholz, M. Bifidobacteria exhibit social behavior through carbohydrate resource sharing in the gut. Sci. Rep. 2015, 5, 15782. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lugli, G.A.; Milani, C.; Turroni, F.; Duranti, S.; Mancabelli, L.; Mangifesta, M.; Ferrario, C.; Modesto, M.; Mattarelli, P.; Jiří, K. Comparative genomic and phylogenomic analyses of the Bifidobacteriaceae family. BMC Genom. 2017, 18, 568. [Google Scholar] [CrossRef] [PubMed]
- Gullfot, F.; Ibatullin, F.M.; Sundqvist, G.; Davies, G.J.; Brumer, H. Functional characterization of xyloglucan glycosynthases from GH7, GH12, and GH16 scaffolds. Biomacromolecules 2009, 10, 1782–1788. [Google Scholar] [CrossRef]
- Nakai, H.; Kitaoka, M.; Svensson, B.; Ohtsubo, K.I. Recent development of phosphorylases possessing large potential for oligosaccharide synthesis. Curr. Opin. Chem. Biol. 2013, 17, 301–309. [Google Scholar] [CrossRef]
- Sela, D.A.; Mills, D.A. Nursing our microbiota: Molecular linkages between bifidobacteria and milk oligosaccharides. Trends Microbiol. 2010, 18, 298–307. [Google Scholar] [CrossRef] [Green Version]
- Benešová, E.; Lipovová, P.; Dvořáková, H.; Králová, B. α-L-fucosidase from Paenibacillus thiaminolyticus: Its hydrolytic and transglycosylation abilities. Glycobiology 2013, 23, 1052–1065. [Google Scholar] [CrossRef] [Green Version]
- Sela, D.A.; Garrido, D.; Lerno, L.; Wu, S.; Tan, K.; Eom, H.-J.; Joachimiak, A.; Lebrilla, C.B.; Mills, D.A. Bifidobacterium longum subsp. infantis ATCC 15697 α-fucosidases are active on fucosylated human milk oligosaccharides. Appl. Environ. Microbiol. 2012, 78, 795–803. [Google Scholar] [CrossRef] [Green Version]
- Sumida, T.; Fujimoto, K.; Ito, M. Molecular cloning and catalytic mechanism of a novel glycosphingolipid-degrading β-N-acetylgalactosaminidase from Paenibacillus sp. TS12. J. Biol. Chem. 2011, 286, 14065–14072. [Google Scholar] [CrossRef] [Green Version]
- Yu, Z.; An, B.; Ramshaw, J.A.M.; Brodsky, B. Bacterial collagen-like proteins that form triple-helical structures. J. Struct. Biol. 2014, 186, 451–461. [Google Scholar] [CrossRef] [Green Version]
- Sela, D.A. Bifidobacterial utilization of human milk oligosaccharides. Int. J. Food Microbiol. 2011, 149, 7. [Google Scholar] [CrossRef] [PubMed]
- Xiao, M.; Tanaka, K.; Qian, X.M.; Yamamoto, K.; Kumagai, H. High-yield production and characterization of α-galactosidase from Bifidobacterium breve grown on raffinose. Biotechnol. Lett. 2000, 22, 747–751. [Google Scholar] [CrossRef]
- Selak, M.; Rivière, A.; Moens, F.; Van den Abbeele, P.; Geirnaert, A.; Rogelj, I.; Leroy, F.; De Vuyst, L. Inulin-type fructan fermentation by bifidobacteria depends on the strain rather than the species and region in the human intestine. Appl. Microbiol. Biotechnol. 2016, 100, 4097–4107. [Google Scholar] [CrossRef] [PubMed]
- Mattarelli, P.; Biavati, B.; Holzapfel, W.H.; Wood, B.J. (Eds.) The Bifidobacteria and Related Organisms; Elsevier: Amsterdam, The Netherlands, 2018. [Google Scholar]
- Parche, S.; Amon, J.; Jankovic, I.; Rezzonico, E.; Beleut, M.; Barutçu, H.; Schendel, I.; Eddy, M.P.; Burkovski, A.; Arigoni, F. Sugar transport systems of Bifidobacterium longum NCC2705. J. Mol. Microbiol. Biotechnol. 2007, 12, 9–19. [Google Scholar] [CrossRef] [PubMed]
- Liu, D.; Wang, S.; Xu, B.; Guo, Y.; Zhao, J.; Liu, W.; Sun, Z.; Shao, C.; Wei, X.; Jiang, Z. Proteomics analysis of Bifidobacterium longum NCC2705 growing on glucose, fructose, mannose, xylose, ribose, and galactose. Proteomics 2011, 11, 2628–2638. [Google Scholar] [CrossRef] [PubMed]
Taxon | Average Genome Size (Mb) | Average % GC Content | Average No. of Genes | Substrate Preferences | Common Isolation Source |
---|---|---|---|---|---|
Bifidobacterium longum species | 2.42 | 59.97 | 2155 | Host-indigestible carbohydrates | Mammalian digestive tract |
subspecies longum | 2.38 | 60.03 | 2098 | Plant-derived carbohydrate substrates | Human adults |
subspecies infantis | 2.67 | 59.70 | 2524 | Human milk oligosaccharides (HMO) | Human infants |
subspecies suis 1 | 2.42 | 59.85 | 2179 | Plant-derived carbohydrate substrates | Nonhuman mammals |
Pangenome Scope | Core Genes | Soft Core Genes | Shell Genes | Cloud Genes | Total Genes |
---|---|---|---|---|---|
Bifidobacterium longum species | 551 | 340 | 1613 | 14,469 | 16,973 |
subspecies longum | 761 | 376 | 1194 | 10,278 | 12,609 |
subspecies infantis | 1019 | 231 | 1966 | 2980 | 6196 |
subspecies suis | 1187 | 0 | 1883 | 1653 | 4723 |
Core CAZy Domain | Representative Gene ID | Inferred Function |
---|---|---|
GH3 | nagZ | putative β-hexosaminidase |
GH13 | glgE1 | α-1,4-glucan:maltose-1-phosphate maltosyltransferase |
GH32 | sacA | β-fructofuranosidase |
GH36 | rafA | α-galactosidase |
GH77 | malQ | 4-α-glucanotransferase |
GT2 | kfoC | Putative glycosyltransferase |
GT4 | mgtA | glycosyltransferase |
GT28 | murG | UDP-N-acetylglucosamine--N-acetylmuramyl-(pentapeptide) pyrophosphoryl-undecaprenol N-acetylglucosamine transferase |
GT51 | pbpG | putative penicillin-binding protein |
Bifidobacterium longum Subspecies | CAZy Domain | Representative Gene ID | Inferred Function |
---|---|---|---|
longum | CBM25 | group_8095 * | amylopullulanase |
longum | CBM35 | hypBA2_4 | hypothetical protein |
longum | CE8 | group_812 * | pectinesterase |
longum | GH65 | kojP | glycoside hydrolase family 65 protein |
infantis | CBM5 | chiA | carbohydrate-binding protein |
infantis | CE2 | celE | electron transport complex, RnfABCDGE type, D subunit |
infantis | GH4 | licH | glucosidase |
infantis | GH151 | lacZ | β-galactosidase |
suis | GH16 | glcA | β-galactosidase |
suis | GH50 | group_2620 * | hypothetical protein |
suis | GH59 | group_1820 * | carbohydrate binding family 6 |
suis | GH154 | group_1814 * | hypothetical protein |
Gene Abbreviation Used in Figure 10 | Locus Tag | Gene Annotation |
---|---|---|
A | Blon_2334 | β-galactosidase |
B | Blon_2335 | α-L-fucosidase 2 (GH95) |
C | Blon_2336 | α-1,3/4-fucosidase (GH29) |
D | Blon_2337 | L-fucose mutarotase |
E | Blon_2338 | dihydrodipicolinate synthetase |
F | Blon_2339 | short-chain dehydrogenase/reductase SDR |
G | Blon_2340 | L-fuconate dehydratase |
H | Blon_2348 | exo-α -sialidase |
I | Blon_2349 | dihydrodipicolinate synthetase |
J | Blon_2355 | β-hexosaminidase |
K | Blon_2356 | haloacid dehalogenase domain protein hydrolase |
L | Blon_2358 | β-lactamase domain protein |
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Albert, K.; Rani, A.; Sela, D.A. Comparative Pangenomics of the Mammalian Gut Commensal Bifidobacterium longum. Microorganisms 2020, 8, 7. https://doi.org/10.3390/microorganisms8010007
Albert K, Rani A, Sela DA. Comparative Pangenomics of the Mammalian Gut Commensal Bifidobacterium longum. Microorganisms. 2020; 8(1):7. https://doi.org/10.3390/microorganisms8010007
Chicago/Turabian StyleAlbert, Korin, Asha Rani, and David A. Sela. 2020. "Comparative Pangenomics of the Mammalian Gut Commensal Bifidobacterium longum" Microorganisms 8, no. 1: 7. https://doi.org/10.3390/microorganisms8010007
APA StyleAlbert, K., Rani, A., & Sela, D. A. (2020). Comparative Pangenomics of the Mammalian Gut Commensal Bifidobacterium longum. Microorganisms, 8(1), 7. https://doi.org/10.3390/microorganisms8010007