Decoding the Genomic Variability among Members of the Bifidobacterium dentium Species
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
PubMed
33152994
PubMed Central
PMC7693768
DOI
10.3390/microorganisms8111720
PII: microorganisms8111720
Knihovny.cz E-zdroje
- Klíčová slova
- bifidobacteria, genomics, pangenome, phylogeny,
- Publikační typ
- časopisecké články MeSH
Members of the Bifidobacterium dentium species are usually identified in the oral cavity of humans and associated with the development of plaque and dental caries. Nevertheless, they have also been detected from fecal samples, highlighting a widespread distribution among mammals. To explore the genetic variability of this species, we isolated and sequenced the genomes of 18 different B. dentium strains collected from fecal samples of several primate species and an Ursus arctos. Thus, we investigated the genomic variability and metabolic abilities of the new B. dentium isolates together with 20 public genome sequences. Comparative genomic analyses provided insights into the vast metabolic repertoire of the species, highlighting 19 glycosyl hydrolases families shared between each analyzed strain. Phylogenetic analysis of the B. dentium taxon, involving 1140 conserved genes, revealed a very close phylogenetic relatedness among members of this species. Furthermore, low genomic variability between strains was also confirmed by an average nucleotide identity analysis showing values higher than 98.2%. Investigating the genetic features of each strain, few putative functional mobile elements were identified. Besides, a consistent occurrence of defense mechanisms such as CRISPR-Cas and restriction-modification systems may be responsible for the high genome synteny identified among members of this taxon.
Department of Veterinary Medical Science University of Parma 43126 Parma Italy
Microbiome Research Hub University of Parma 13121 Parma Italy
Zobrazit více v PubMed
Kostic A.D., Howitt M.R., Garrett W.S. Exploring host-microbiota interactions in animal models and humans. Genes Dev. 2013;27:701–718. doi: 10.1101/gad.212522.112. PubMed DOI PMC
Turnbaugh P.J., Ley R.E., Hamady M., Fraser-Liggett C.M., Knight R., Gordon J.I. The human microbiome project. Nature. 2007;449:804–810. doi: 10.1038/nature06244. PubMed DOI PMC
Donovan S.M. Introduction to the special focus issue on the impact of diet on gut microbiota composition and function and future opportunities for nutritional modulation of the gut microbiome to improve human health. Gut Microbes. 2017;8:75–81. doi: 10.1080/19490976.2017.1299309. PubMed DOI PMC
Milani C., Duranti S., Bottacini F., Casey E., Turroni F., Mahony J., Belzer C., Delgado Palacio S., Arboleya Montes S., Mancabelli L., et al. The First Microbial Colonizers of the Human Gut: Composition, Activities, and Health Implications of the Infant Gut Microbiota. Microbiol. Mol. Biol. Rev. Mmbr. 2017;81 doi: 10.1128/MMBR.00036-17. PubMed DOI PMC
Lugli G.A., Mangifesta M., Duranti S., Anzalone R., Milani C., Mancabelli L., Alessandri G., Turroni F., Ossiprandi M.C., van Sinderen D., et al. Phylogenetic classification of six novel species belonging to the genus Bifidobacterium comprising Bifidobacterium anseris sp. nov., Bifidobacterium criceti sp. nov., Bifidobacterium imperatoris sp. nov., Bifidobacterium italicum sp. nov., Bifidobacterium margollesii sp. nov. and Bifidobacterium parmae sp. nov. Syst. Appl. Microbiol. 2018;41:173–183. doi: 10.1016/j.syapm.2018.01.002. PubMed DOI
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 doi: 10.1128/AEM.02249-17. PubMed DOI PMC
Duranti S., Mangifesta M., Lugli G.A., Turroni F., Anzalone R., Milani C., Mancabelli L., Ossiprandi M.C., Ventura M. Bifidobacterium vansinderenii sp. nov., isolated from faeces of emperor tamarin (Saguinus imperator) Int. J. Syst. Evol. Microbiol. 2017;67:3987–3995. doi: 10.1099/ijsem.0.002243. PubMed DOI
Modesto M., Michelini S., Oki K., Biavati B., Watanabe K., Mattarelli P. Bifidobacterium catulorum sp. nov., a novel taxon from the faeces of the baby common marmoset (Callithrix jacchus) Int. J. Syst. Evol. Microbiol. 2018;68:575–581. doi: 10.1099/ijsem.0.002545. PubMed DOI
Modesto M., Puglisi E., Bonetti A., Michelini S., Spiezio C., Sandri C., Sgorbati B., Morelli L., Mattarelli P. Bifidobacterium primatium sp. nov., Bifidobacterium scaligerum sp. nov., Bifidobacterium felsineum sp. nov. and Bifidobacterium simiarum sp. nov.: Four novel taxa isolated from the faeces of the cotton top tamarin (Saguinus oedipus) and the emperor tamarin (Saguinus imperator) Syst. Appl. Microbiol. 2018;41:593–603. doi: 10.1016/j.syapm.2018.07.005. PubMed DOI
Modesto M., Michelini S., Sansosti M.C., De Filippo C., Cavalieri D., Qvirist L., Andlid T., Spiezio C., Sandri C., Pascarelli S., et al. Bifidobacterium callitrichidarum sp. nov. from the faeces of the emperor tamarin (Saguinus imperator) Int. J. Syst. Evol. Microbiol. 2018;68:141–148. doi: 10.1099/ijsem.0.002472. PubMed DOI
Michelini S., Modesto M., Filippini G., Spiezio C., Sandri C., Biavati B., Pisi A., Mattarelli P. Corrigendum to “Bifidobacterium aerophilum sp. nov., Bifidobacterium avesanii sp. nov. and Bifidobacterium ramosum sp. nov.: Three novel taxa from the faeces of cotton-top tamarin (Saguinus oedipus L.)” [Syst. Appl. Microbiol. 39 (2016) 229–236] Syst. Appl. Microbiol. 2018;41:528. doi: 10.1016/j.syapm.2018.05.002. PubMed DOI
Pechar R., Killer J., Salmonova H., Geigerova M., Svejstil R., Svec P., Sedlacek I., Rada V., Benada O. Bifidobacterium apri sp. nov., a thermophilic actinobacterium isolated from the digestive tract of wild pigs (Sus scrofa) Int. J. Syst. Evol. Microbiol. 2017;67:2349–2356. doi: 10.1099/ijsem.0.001956. PubMed DOI
Alberoni D., Gaggia F., Baffoni L., Modesto M.M., Biavati B., Di Gioia D. Bifidobacterium xylocopae sp. nov. and Bifidobacterium aemilianum sp. nov., from the carpenter bee (Xylocopa violacea) digestive tract. Syst. Appl. Microbiol. 2019;42:205–216. doi: 10.1016/j.syapm.2018.11.005. PubMed DOI
Modesto M., Watanabe K., Arita M., Satti M., Oki K., Sciavilla P., Patavino C., Camma C., Michelini S., Sgorbati B., et al. Bifidobacterium jacchi sp. nov., isolated from the faeces of a baby common marmoset (Callithrix jacchus) Int. J. Syst. Evol. Microbiol. 2019;69:2477–2485. doi: 10.1099/ijsem.0.003518. PubMed DOI
Modesto M., Satti M., Watanabe K., Puglisi E., Morelli L., Huang C.H., Liou J.S., Miyashita M., Tamura T., Saito S., et al. Characterization of Bifidobacterium species in feaces of the Egyptian fruit bat: Description of B. vespertilionis sp. nov. and B. rousetti sp. nov. Syst. Appl. Microbiol. 2019;42:126017. doi: 10.1016/j.syapm.2019.126017. PubMed DOI
Eckel V.P.L., Ziegler L.M., Vogel R.F., Ehrmann M. Bifidobacterium tibiigranuli sp. nov. isolated from homemade water kefir. Int. J. Syst. Evol. Microbiol. 2020;70:1562–1570. doi: 10.1099/ijsem.0.003936. PubMed DOI
Duranti S., Lugli G.A., Viappiani A., Mancabelli L., Alessandri G., Anzalone R., Longhi G., Milani C., Ossiprandi M.C., Turroni F., et al. Characterization of the phylogenetic diversity of two novel species belonging to the genus Bifidobacterium: Bifidobacterium cebidarum sp. nov. and Bifidobacterium leontopitheci sp. nov. Int. J. Syst. Evol. Microbiol. 2020;70:2288–2297. doi: 10.1099/ijsem.0.004032. PubMed DOI
Neuzil-Bunesova V., Lugli G.A., Modrackova N., Makovska M., Mrazek J., Mekadim C., Musilova S., Svobodova I., Spanek R., Ventura M., et al. Bifidobacterium canis sp. nov., a novel member of the Bifidobacterium pseudolongum phylogenetic group isolated from faeces of a dog (Canis lupus f. familiaris) Int. J. Syst. Evol. Microbiol. 2020 doi: 10.1099/ijsem.0.004378. PubMed DOI
Modesto M., Satti M., Watanabe K., Scarafile D., Huang C.H., Liou J.S., Tamura T., Saito S., Watanabe M., Mori K., et al. Phylogenetic characterization of two novel species of the genus Bifidobacterium: Bifidobacterium saimiriisciurei sp. nov. and Bifidobacterium platyrrhinorum sp. nov. Syst. Appl. Microbiol. 2020;43:126111. doi: 10.1016/j.syapm.2020.126111. PubMed DOI
Modesto M., Biavati B., Mattarelli P. Occurrence of the family bifidobacteriaceae in human dental caries and plaque. Caries Res. 2006;40:271–276. doi: 10.1159/000092237. PubMed DOI
Mantzourani M., Fenlon M., Beighton D. Association between Bifidobacteriaceae and the clinical severity of root caries lesions. Oral Microbiol. Immunol. 2009;24:32–37. doi: 10.1111/j.1399-302X.2008.00470.x. PubMed DOI
Mantzourani M., Gilbert S.C., Fenlon M., Beighton D. Non-oral bifidobacteria and the aciduric microbiota of the denture plaque biofilm. Mol. Oral Microbiol. 2010;25:190–199. doi: 10.1111/j.2041-1014.2009.00565.x. PubMed DOI
Ventura M., Turroni F., Zomer A., Foroni E., Giubellini V., Bottacini F., Canchaya C., Claesson M.J., He F., Mantzourani M., et al. The Bifidobacterium dentium Bd1 genome sequence reflects its genetic adaptation to the human oral cavity. PLoS Genet. 2009;5:e1000785. doi: 10.1371/journal.pgen.1000785. PubMed DOI PMC
Henne K., Rheinberg A., Melzer-Krick B., Conrads G. Aciduric microbial taxa including Scardovia wiggsiae and Bifidobacterium spp. in caries and caries free subjects. Anaerobe. 2015;35:60–65. doi: 10.1016/j.anaerobe.2015.04.011. PubMed DOI
Neves B.G., Stipp R.N., Bezerra D.D.S., Guedes S.F.F., Rodrigues L.K.A. Quantitative analysis of biofilm bacteria according to different stages of early childhood caries. Arch. Oral Biol. 2018;96:155–161. doi: 10.1016/j.archoralbio.2018.09.007. PubMed DOI
Milani C., Mangifesta M., Mancabelli L., Lugli G.A., James K., Duranti S., Turroni F., Ferrario C., Ossiprandi M.C., van Sinderen D., et al. Unveiling bifidobacterial biogeography across the mammalian branch of the tree of life. Isme J. 2017;11:2834–2847. doi: 10.1038/ismej.2017.138. PubMed DOI PMC
Duranti S., Milani C., Lugli G.A., Turroni F., Mancabelli L., Sanchez B., Ferrario C., Viappiani A., Mangifesta M., Mancino W., et al. Insights from genomes of representatives of the human gut commensal Bifidobacterium bifidum. Environ. Microbiol. 2015;17:2515–2531. doi: 10.1111/1462-2920.12743. PubMed DOI
Duranti S., Milani C., Lugli G.A., Mancabelli L., Turroni F., Ferrario C., Mangifesta M., Viappiani A., Sanchez B., Margolles A., et al. Evaluation of genetic diversity among strains of the human gut commensal Bifidobacterium adolescentis. Sci. Rep. 2016;6:23971. doi: 10.1038/srep23971. PubMed DOI PMC
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 Genom. 2015;16:832. doi: 10.1186/s12864-015-1968-4. PubMed DOI PMC
Lugli G.A., Duranti S., Albert K., Mancabelli L., Napoli S., Viappiani A., Anzalone R., Longhi G., Milani C., Turroni F., et al. Unveiling Genomic Diversity among Members of the Species Bifidobacterium pseudolongum, a Widely Distributed Gut Commensal of the Animal Kingdom. Appl. Environ. Microbiol. 2019;85 doi: 10.1128/AEM.03065-18. PubMed DOI PMC
Ventura M., Zink R., Fitzgerald G.F., van Sinderen D. Gene structure and transcriptional organization of the dnaK operon of Bifidobacterium breve UCC 2003 and application of the operon in bifidobacterial tracing. Appl. Environ. Microbiol. 2005;71:487–500. doi: 10.1128/AEM.71.1.487-500.2005. PubMed DOI PMC
Strandwitz P., Kim K.H., Terekhova D., Liu J.K., Sharma A., Levering J., McDonald D., Dietrich D., Ramadhar T.R., Lekbua A., et al. GABA-modulating bacteria of the human gut microbiota. Nat. Microbiol. 2019;4:396–403. doi: 10.1038/s41564-018-0307-3. PubMed DOI PMC
Duranti S., Ruiz L., Lugli G.A., Tames H., Milani C., Mancabelli L., Mancino W., Longhi G., Carnevali L., Sgoifo A., et al. Bifidobacterium adolescentis as a key member of the human gut microbiota in the production of GABA. Sci. Rep. 2020;10:14112. doi: 10.1038/s41598-020-70986-z. PubMed DOI PMC
Pokusaeva K., Johnson C., Luk B., Uribe G., Fu Y., Oezguen N., Matsunami R.K., Lugo M., Major A., Mori-Akiyama Y., et al. GABA-producing Bifidobacterium dentium modulates visceral sensitivity in the intestine. Neurogastroenterol. Motil. Off. J. Eur. Gastrointest. Motil. Soc. 2017;29 doi: 10.1111/nmo.12904. PubMed DOI PMC
Engevik M.A., Luk B., Chang-Graham A.L., Hall A., Herrmann B., Ruan W., Endres B.T., Shi Z., Garey K.W., Hyser J.M., et al. Bifidobacterium dentium Fortifies the Intestinal Mucus Layer via Autophagy and Calcium Signaling Pathways. mBio. 2019;10 doi: 10.1128/mBio.01087-19. PubMed DOI PMC
Turroni F., Marchesi J.R., Foroni E., Gueimonde M., Shanahan F., Margolles A., van Sinderen D., Ventura M. Microbiomic analysis of the bifidobacterial population in the human distal gut. Isme J. 2009;3:745–751. doi: 10.1038/ismej.2009.19. PubMed DOI
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. doi: 10.1111/1574-6941.12410. PubMed DOI
Lugli G.A., Milani C., Mancabelli L., van Sinderen D., Ventura M. MEGAnnotator: A user-friendly pipeline for microbial genomes assembly and annotation. Fems Microbiol. Lett. 2016;363 doi: 10.1093/femsle/fnw049. PubMed DOI
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., et al. SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. A J. Comput. Mol. Cell Biol. 2012;19:455–477. doi: 10.1089/cmb.2012.0021. PubMed DOI PMC
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. doi: 10.1186/1471-2105-11-119. PubMed DOI PMC
Zhao Y., Tang H., Ye Y. RAPSearch2: A fast and memory-efficient protein similarity search tool for next-generation sequencing data. Bioinformatics. 2012;28:125–126. doi: 10.1093/bioinformatics/btr595. PubMed DOI PMC
Lowe T.M., Eddy S.R. tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 1997;25:955–964. doi: 10.1093/nar/25.5.955. PubMed DOI PMC
Lagesen K., Hallin P., Rodland E.A., Staerfeldt H.H., Rognes T., Ussery D.W. RNAmmer: Consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 2007;35:3100–3108. doi: 10.1093/nar/gkm160. PubMed DOI PMC
Brooks L., Kaze M., Sistrom M. A Curated, Comprehensive Database of Plasmid Sequences. Microbiol. Resour. Announc. 2019;8 doi: 10.1128/MRA.01325-18. PubMed DOI PMC
Arredondo-Alonso S., Rogers M.R.C., Braat J.C., Verschuuren T.D., Top J., Corander J., Willems R.J.L., Schurch A.C. mlplasmids: A user-friendly tool to predict plasmid- and chromosome-derived sequences for single species. Microb. Genom. 2018;4 doi: 10.1099/mgen.0.000224. PubMed DOI PMC
Zhao Y., Wu J., Yang J., Sun S., Xiao J., Yu J. PGAP: Pan-genomes analysis pipeline. Bioinformatics. 2012;28:416–418. doi: 10.1093/bioinformatics/btr655. PubMed DOI PMC
Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990;215:403–410. doi: 10.1016/S0022-2836(05)80360-2. PubMed DOI
Vlietstra W.J., Zielman R., van Dongen R.M., Schultes E.A., Wiesman F., Vos R., van Mulligen E.M., Kors J.A. Automated extraction of potential migraine biomarkers using a semantic graph. J. Biomed. Inf. 2017;71:178–189. doi: 10.1016/j.jbi.2017.05.018. PubMed DOI
Katoh K., Misawa K., Kuma K., Miyata T. MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002;30:3059–3066. doi: 10.1093/nar/gkf436. PubMed DOI PMC
Chenna R., Sugawara H., Koike T., Lopez R., Gibson T.J., Higgins D.G., Thompson J.D. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 2003;31:3497–3500. doi: 10.1093/nar/gkg500. PubMed DOI PMC
Jain C., Rodriguez R.L., Phillippy A.M., Konstantinidis K.T., Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat. Commun. 2018;9:5114. doi: 10.1038/s41467-018-07641-9. PubMed DOI PMC
Lombard V., Golaconda Ramulu H., Drula E., Coutinho P.M., Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2014;42:D490–D495. doi: 10.1093/nar/gkt1178. PubMed DOI PMC
Wheeler T.J., Eddy S.R. nhmmer: DNA homology search with profile HMMs. Bioinformatics. 2013;29:2487–2489. doi: 10.1093/bioinformatics/btt403. PubMed DOI PMC
Zhang H., Yohe T., Huang L., Entwistle S., Wu P., Yang Z., Busk P.K., Xu Y., Yin Y. dbCAN2: A meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 2018;46:W95–W101. doi: 10.1093/nar/gky418. PubMed DOI PMC
Roberts R.J., Vincze T., Posfai J., Macelis D. REBASE—A database for DNA restriction and modification: Enzymes, genes and genomes. Nucleic Acids Res. 2015;43:D298–D299. doi: 10.1093/nar/gku1046. PubMed DOI PMC
Couvin D., Bernheim A., Toffano-Nioche C., Touchon M., Michalik J., Neron B., Rocha E.P.C., Vergnaud G., Gautheret D., Pourcel C. CRISPRCasFinder, an update of CRISRFinder, includes a portable version, enhanced performance and integrates search for Cas proteins. Nucleic Acids Res. 2018;46:W246–W251. doi: 10.1093/nar/gky425. PubMed DOI PMC
Waack S., Keller O., Asper R., Brodag T., Damm C., Fricke W.F., Surovcik K., Meinicke P., Merkl R. Score-based prediction of genomic islands in prokaryotic genomes using hidden Markov models. BMC Bioinform. 2006;7:142. doi: 10.1186/1471-2105-7-142. PubMed DOI PMC
Milani C., Lugli G.A., Duranti S., Turroni F., Bottacini F., Mangifesta M., Sanchez B., Viappiani A., Mancabelli L., Taminiau B., et al. Genomic encyclopedia of type strains of the genus Bifidobacterium. Appl. Environ. Microbiol. 2014;80:6290–6302. doi: 10.1128/AEM.02308-14. PubMed DOI PMC
Lugli G.A., Milani C., Turroni F., Tremblay D., Ferrario C., Mancabelli L., Duranti S., Ward D.V., Ossiprandi M.C., Moineau S., et al. Prophages of the genus Bifidobacterium as modulating agents of the infant gut microbiota. Environ. Microbiol. 2016;18:2196–2213. doi: 10.1111/1462-2920.13154. PubMed DOI
Arndt D., Grant J.R., Marcu A., Sajed T., Pon A., Liang Y., Wishart D.S. PHASTER: A better, faster version of the PHAST phage search tool. Nucleic Acids Res. 2016;44:W16–W21. doi: 10.1093/nar/gkw387. PubMed DOI PMC
Lakin S.M., Dean C., Noyes N.R., Dettenwanger A., Ross A.S., Doster E., Rovira P., Abdo Z., Jones K.L., Ruiz J., et al. MEGARes: An antimicrobial resistance database for high throughput sequencing. Nucleic Acids Res. 2017;45:D574–D580. doi: 10.1093/nar/gkw1009. PubMed DOI PMC
Van Heel A.J., de Jong A., Montalban-Lopez M., Kok J., Kuipers O.P. BAGEL3: Automated identification of genes encoding bacteriocins and (non-)bactericidal posttranslationally modified peptides. Nucleic Acids Res. 2013;41:W448–W453. doi: 10.1093/nar/gkt391. PubMed DOI PMC
Xie Y., Wei Y., Shen Y., Li X., Zhou H., Tai C., Deng Z., Ou H.Y. TADB 2.0: An updated database of bacterial type II toxin-antitoxin loci. Nucleic Acids Res. 2018;46:D749–D753. doi: 10.1093/nar/gkx1033. PubMed DOI PMC
Saeed A.I., Sharov V., White J., Li J., Liang W., Bhagabati N., Braisted J., Klapa M., Currier T., Thiagarajan M., et al. TM4: A free, open-source system for microarray data management and analysis. BioTechniques. 2003;34:374–378. doi: 10.2144/03342mt01. PubMed DOI
Tettelin H., Masignani V., Cieslewicz M.J., Donati C., Medini D., Ward N.L., Angiuoli S.V., Crabtree J., Jones A.L., Durkin A.S., et al. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: Implications for the microbial "pan-genome". Proc. Natl. Acad. Sci. USA. 2005;102:13950–13955. doi: 10.1073/pnas.0506758102. PubMed DOI PMC
Albert K., Rani A., Sela D.A. Comparative Pangenomics of the Mammalian Gut Commensal Bifidobacterium longum. Microorganisms. 2019;8:7. doi: 10.3390/microorganisms8010007. PubMed DOI PMC
Bottacini F., O’Connell Motherway M., Kuczynski J., O’Connell K.J., Serafini F., Duranti S., Milani C., Turroni F., Lugli G.A., Zomer A., et al. Comparative genomics of the Bifidobacterium breve taxon. BMC Genom. 2014;15:170. doi: 10.1186/1471-2164-15-170. PubMed DOI PMC
Lugli G.A., Milani C., Turroni F., Duranti S., Mancabelli L., Mangifesta M., Ferrario C., Modesto M., Mattarelli P., Jiri K., et al. Comparative genomic and phylogenomic analyses of the Bifidobacteriaceae family. BMC Genom. 2017;18:568. doi: 10.1186/s12864-017-3955-4. PubMed DOI PMC
Lugli G.A., Milani C., Turroni F., Duranti S., Ferrario C., Viappiani A., Mancabelli L., Mangifesta M., Taminiau B., Delcenserie V., et al. Investigation of the evolutionary development of the genus Bifidobacterium by comparative genomics. Appl. Environ. Microbiol. 2014;80:6383–6394. doi: 10.1128/AEM.02004-14. PubMed DOI PMC
Richter M., Rossello-Mora R. Shifting the genomic gold standard for the prokaryotic species definition. Proc. Natl. Acad. Sci. USA. 2009;106:19126–19131. doi: 10.1073/pnas.0906412106. PubMed DOI PMC
Milani C., Lugli G.A., Duranti S., Turroni F., Mancabelli L., Ferrario C., Mangifesta M., Hevia A., Viappiani A., Scholz M., et al. Bifidobacteria exhibit social behavior through carbohydrate resource sharing in the gut. Sci. Rep. 2015;5:15782. doi: 10.1038/srep15782. PubMed DOI PMC
Botstein D. A theory of modular evolution for bacteriophages. Ann. N.Y. Acad. Sci. 1980;354:484–490. doi: 10.1111/j.1749-6632.1980.tb27987.x. PubMed DOI
Bernheim A., Sorek R. The pan-immune system of bacteria: Antiviral defence as a community resource. Nat. Rev. Microbiol. 2020;18:113–119. doi: 10.1038/s41579-019-0278-2. PubMed DOI
Briner A.E., Lugli G.A., Milani C., Duranti S., Turroni F., Gueimonde M., Margolles A., van Sinderen D., Ventura M., Barrangou R. Occurrence and Diversity of CRISPR-Cas Systems in the Genus Bifidobacterium. PLoS ONE. 2015;10:e0133661. doi: 10.1371/journal.pone.0133661. PubMed DOI PMC
Ershova A.S., Rusinov I.S., Spirin S.A., Karyagina A.S., Alexeevski A.V. Role of Restriction-Modification Systems in Prokaryotic Evolution and Ecology. Biochemistry (Moscow) 2015;80:1373–1386. doi: 10.1134/S0006297915100193. PubMed DOI
Duranti S., Lugli G.A., Mancabelli L., Turroni F., Milani C., Mangifesta M., Ferrario C., Anzalone R., Viappiani A., van Sinderen D., et al. Prevalence of Antibiotic Resistance Genes among Human Gut-Derived Bifidobacteria. Appl. Environ. Microbiol. 2017;83 doi: 10.1128/AEM.02894-16. PubMed DOI PMC
Mancino W., Lugli G.A., Sinderen D.V., Ventura M., Turroni F. Mobilome and Resistome Reconstruction from Genomes Belonging to Members of the Bifidobacterium Genus. Microorganisms. 2019;7:638. doi: 10.3390/microorganisms7120638. PubMed DOI PMC