Genetic differences of intestinal Bifidobacterium bifidum among school-age children in Yining, Xinjiang: a study based on multilocus sequence typing
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    Abstract:

    [Background] Bifidobacterium bifidum, an obligate intestinal bacterium that specifically metabolizes human milk oligosaccharides (HMOs) and mucin glycans of host gut epithelium, is essential for early life health and development. However, little is known about the genetic differences of this bacterium among different populations. [Objective] To investigate whether the B. bifidum strains from genetically similar populations with similar diets in a limited geographic area have population-specific regularities and to reveal the genetic differences of B. bifidum among different populations. [Methods] A total of 115 strains of B. bifidum were isolated and identified from school-age children of Uyghur and Kazak ethnic minorities in Yining, Xinjiang. Further, we performed multilocus sequence typing (MLST) for 53 representative strains screened out by rep-PCR to understand the genetic differences of B. bifidum between different ethnic groups. [Results] The 53 strains belonged to 37 sequence types (STs), showing high genetic diversity. Among them, 17 STs were identified for 26 isolates from the children of Uyghur ethnic minority, while 20 STs for 27 isolates from the children of Kazak ethnic minority. Only a few homologous genetic recombination events were detected between strains from both ethnic groups. goeBURST showed that B. bifidum isolates from the same population were more likely to be assigned to a specific phylogenetic clade or clonal complex than the isolates from the other population. [Conclusion] B. bifidum isolates from different ethnic groups showed high genetic diversity. The host (ethnic group) specificity of their genetic structure needs to be confirmed by larger sampling. Our findings provide a theoretical basis for further screening of elite probiotic strains tailored to localized population by in vivo and in vitro experiments.

    Reference
    [1] HARMSEN HJM, RAANGS GC, HE T, DEGENER JE, WELLING GW. Extensive set of 16S rRNA-based probes for detection of bacteria in human feces[J]. Applied and Environmental Microbiology, 2002, 68(6): 2982-2990.
    [2] ROGER LC, COSTABILE A, HOLLAND DT, HOYLES L, McCARTNEY AL. Examination of faecal Bifidobacterium populations in breast- and formula-fed infants during the first 18 months of life[J]. Microbiology, 2010, 156(11): 3329-3341.
    [3] VAISHAMPAYAN PA, KUEHL JV, FROULA JL, MORGAN JL, OCHMAN H, FRANCINO MP. Comparative metagenomics and population dynamics of the gut microbiota in mother and infant[J]. Genome Biology and Evolution, 2010, 2: 53-66.
    [4] VENTURA M, TURRONI F, MOTHERWAY MO, MACSHARRY J, van SINDEREN D. Host-microbe interactions that facilitate gut colonization by commensal bifidobacteria[J]. Trends in Microbiology, 2012, 20(10): 467-476.
    [5] WONG CB, ODAMAKI T, XIAO JZ. Insights into the reason of human-residential bifidobacteria (HRB) being the natural inhabitants of the human gut and their potential health-promoting benefits[J]. FEMS Microbiology Reviews, 2020, 44(3): 369-385.
    [6] TURRONI F, MILANI C, DURANTI S, FERRARIO C, LUGLI GA, MANCABELLI L, van SINDEREN D, VENTURA M. Bifidobacteria and the infant gut: an example of co-evolution and natural selection[J]. Cellular and Molecular Life Sciences, 2018, 75(1): 103-118.
    [7] TURRONI F, PEANO C, PASS DA, FORONI E, SEVERGNINI M, CLAESSON MJ, KERR C, HOURIHANE J, MURRAY D, FULIGNI F, GUEIMONDE M, MARGOLLES A, de BELLIS G, O’TOOLE PW, van SINDEREN D, MARCHESI JR, VENTURA M. Diversity of bifidobacteria within the infant gut microbiota[J]. PLoS One, 2012, 7(5): e36957.
    [8] LUGLI GA, MILANI C, DURANTI S, ALESSANDRI G, TURRONI F, MANCABELLI L, TATONI D, OSSIPRANDI MC, SINDEREN D, VENTURA M. Isolation of novel gut bifidobacteria using a combination of metagenomic and cultivation approaches[J]. Genome Biology, 2019, 20(1): 1-6.
    [9] DURANTI S, LUGLI GA, MANCABELLI L, ARMANINI F, TURRONI F, JAMES K, FERRETTI P, GORFER V, FERRARIO C, MILANI C, MANGIFESTA M, ANZALONE R, ZOLFO M, VIAPPIANI A, PASOLLI E, BARILETTI I, CANTO R, CLEMENTI R, COLOGNA M, CRIFÒ T, et al. Maternal inheritance of bifidobacterial communities and bifidophages in infants through vertical transmission[J]. Microbiome, 2017, 5(1): 1-13.
    [10] GUGLIELMETTI S, TAMAGNINI I, MINUZZO M, ARIOLI S, PARINI C, COMELLI E, MORA D. Study of the adhesion of Bifidobacterium bifidum MIMBb75 to human intestinal cell lines[J]. Current Microbiology, 2009, 59(2): 167-172.
    [11] SERAFINI F, STRATI F, RUAS-MADIEDO P, TURRONI F, FORONI E, DURANTI S, MILANO F, PEROTTI A, VIAPPIANI A, GUGLIELMETTI S, BUSCHINI A, MARGOLLES A, van SINDEREN D, VENTURA M. Evaluation of adhesion properties and antibacterial activities of the infant gut commensal Bifidobacterium bifidum PRL2010[J]. Anaerobe, 2013, 21: 9-17.
    [12] EGAN M, O’CONNELL MOTHERWAY M, KILCOYNE M, KANE M, JOSHI L, VENTURA M, van SINDEREN D. Cross-feeding by Bifidobacterium breve UCC2003 during co-cultivation with Bifidobacterium bifidum PRL2010 in a mucin-based medium[J]. BMC Microbiology, 2014, 14(1): 1-14.
    [13] TURRONI F, MILANI C, DURANTI S, MANCABELLI L, MANGIFESTA M, VIAPPIANI A, LUGLI GA, FERRARIO C, GIOIOSA L, FERRARINI A, LI J, PALANZA P, DELLEDONNE M, van SINDEREN D, VENTURA M. Deciphering bifidobacterial-mediated metabolic interactions and their impact on gut microbiota by a multi-omics approach[J]. The ISME Journal, 2016, 10(7): 1656-1668.
    [14] DURANTI S, LUGLI GA, MILANI C, JAMES K, MANCABELLI L, TURRONI F, ALESSANDRI G, MANGIFESTA M, MANCINO W, OSSIPRANDI MC, IORI A, ROTA C, GARGANO G, BERNASCONI S, di PIERRO F, SINDEREN D, VENTURA M. Bifidobacterium bifidum and the infant gut microbiota: an intriguing case of microbe-host co-evolution[J]. Environmental Microbiology, 2019, 21(10): 3683-3695.
    [15] TURRONI F, van SINDEREN D, VENTURA M. Bifidobacteria: insights into the biology of a key microbial group of early life gut microbiota[J]. Microbiome Research Reports, 2021:1-2.
    [16] DURANTI S, MILANI C, LUGLI GA, TURRONI F, MANCABELLI L, SANCHEZ B, FERRARIO C, VIAPPIANI A, MANGIFESTA M, MANCINO W, GUEIMONDE M, MARGOLLES A, van SINDEREN D, VENTURA M. Insights from genomes of representatives of the human gut commensal Bifidobacterium bifidum[J]. Environmental Microbiology, 2015, 17(7): 2515-2531.
    [17] YUAN LX, ZHANG XL, LUO BL, LI X, TIAN FW, YAN WL, NI YQ. Ethnic specificity of species and strain composition of Lactobacillus populations from mother-infant pairs, uncovered by multilocus sequence typing[J]. Frontiers in Microbiology, 2022, 13: 814284.
    [18] ASSOCIATION WM. World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects[J]. The Journal of the American Medical Association, 2013, 310(20): 2191-2194.
    [19] VLKOVÁ E, SALMONOVÁ H, BUNEŠOVÁ V, GEIGEROVÁ M, RADA V, MUSILOVÁ Š. A new medium containing mupirocin, acetic acid, and norfloxacin for the selective cultivation of bifidobacteria[J]. Anaerobe, 2015, 34: 27-33.
    [20] MODESTO M. Isolation, cultivation, and storage of bifidobacteria[M]//The Bifidobacteria and Related Organisms. Amsterdam: Elsevier, 2018: 67-98.
    [21] VENTURA M, RENIERO R, ZINK R. Specific identification and targeted characterization of Bifidobacterium lactis from different environmental isolates by a combined multiplex-PCR approach[J]. Applied and Environmental Microbiology, 2001, 67(6): 2760-2765.
    [22] JAROCKI P, PODLEŚNY M, KOMOŃ-JANCZARA E, KUCHARSKA J, GLIBOWSKA A, TARGOŃSKI Z. Comparison of various molecular methods for rapid differentiation of intestinal bifidobacteria at the species, subspecies and strain level[J]. BMC Microbiology, 2016, 16(1): 159.
    [23] MAKINO H, KUSHIRO A, ISHIKAWA E, KUBOTA H, GAWAD A, SAKAI T, OISHI K, MARTIN R, BEN-AMOR K, KNOL J, TANAKA R. Mother-to-infant transmission of intestinal bifidobacterial strains has an impact on the early development of vaginally delivered infant’s microbiota[J]. PLoS One, 2013, 8(11): e78331.
    [24] DIANCOURT L, PASSET V, CHERVAUX C, GARAULT P, SMOKVINA T, BRISSE S. Multilocus sequence typing of Lactobacillus casei reveals a clonal population structure with low levels of homologous recombination[J]. Applied and Environmental Microbiology, 2007, 73(20): 6601-6611.
    [25] KUMAR S, STECHER G, TAMURA K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets[J]. Molecular Biology and Evolution, 2016, 33(7): 1870-1874.
    [26] LIBRADO P, ROZAS J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data[J]. Bioinformatics, 2009, 25(11): 1451-1452.
    [27] HUSON DH, BRYANT D. Application of phylogenetic networks in evolutionary studies[J]. Molecular Biology and Evolution, 2006, 23(2): 254-267.
    [28] FEIL EJ, LI BC, AANENSEN DM, HANAGE WP, SPRATT BG. eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data[J]. Journal of Bacteriology, 2004, 186(5): 1518-1530.
    [29] KRYAZHIMSKIY S, PLOTKIN JB. The population genetics of dN/dS[J]. PLoS Genetics, 2008, 4(12): e1000304.
    [30] ZHANG WY, LIU WJ, SONG YQ, XU HY, MENGHE B, ZHANG HP, SUN ZH. Multilocus sequence typing of a dairy-associated Leuconostoc mesenteroides population reveals clonal structure with intragenic homologous recombination[J]. Journal of Dairy Science, 2015, 98(4): 2284-2293.
    [31] ALBERDI A, MARTIN BIDEGUREN G, AIZPURUA O. Diversity and compositional changes in the gut microbiota of wild and captive vertebrates: a meta-analysis[J]. Scientific Reports, 2021, 11: 22660.
    [32] WANG SP, RYAN CA, BOYAVAL P, DEMPSEY EM, ROSS RP, STANTON C. Maternal vertical transmission affecting early-life microbiota development[J]. Trends in Microbiology, 2020, 28(1): 28-45.
    [33] HOU FY, TANG JY, LIU YY, TAN YF, WANG Y, ZHENG LJ, LIANG DB, LIN YQ, WANG LK, PAN ZY, YANG RF, BI YJ, ZHI FC. Safety evaluation and probiotic potency screening of Akkermansia muciniphila strains isolated from human feces and breast milk[J]. Microbiology Spectrum, 2023, 11(2): e0336122.
    [34] MILANI C, MANCABELLI L, LUGLI GA, DURANTI S, TURRONI F, FERRARIO C, MANGIFESTA M, VIAPPIANI A, FERRETTI P, GORFER V, TETT A, SEGATA N, van SINDEREN D, VENTURA M. Exploring vertical transmission of bifidobacteria from mother to child[J]. Applied and Environmental Microbiology, 2015, 81(20): 7078-7087.
    [35] TURRONI F, MILANI C, DURANTI S, MAHONY J, van SINDEREN D, VENTURA M. Glycan utilization and cross-feeding activities by bifidobacteria[J]. Trends in Microbiology, 2018, 26(4): 339-350.
    [36] BUNESOVA V, LACROIX C, SCHWAB C. Mucin cross-feeding of infant bifidobacteria and Eubacterium hallii[J]. Microbial Ecology, 2018, 75(1): 228-238.
    [37] TURRONI F, ÖZCAN E, MILANI C, MANCABELLI L, VIAPPIANI A, van SINDEREN D, SELA DA, VENTURA M. Glycan cross-feeding activities between bifidobacteria under in vitro conditions[J]. Frontiers in Microbiology, 2015, 6: 1030.
    [38] DERRIEN M, TURRONI F, VENTURA M, SINDEREN D. Insights into endogenous Bifidobacterium species in the human gut microbiota during adulthood[J]. Trends in Microbiology, 2022, 30(10): 940-947.
    [39] ZHANG WY, VERVOORT J, PAN JC, GAO P, ZHU HQ, WANG XD, ZHANG YM, CHEN BR, LIU Y, LI YY, PANG XY, ZHANG SW, JIANG SL, LU J, LYU JP. Comparison of twelve human milk oligosaccharides in mature milk from different areas in China in the Chinese Human Milk Project (CHMP) study[J]. Food Chemistry, 2022, 395: 133554.
    [40] ZHANG M, HANG XM, TAN J, YANG H. The host genotype and environment affect strain types of Bifidobacterium longum subsp. longum inhabiting the intestinal tracts of twins[J]. Applied and Environmental Microbiology, 2015, 81(14): 4774-4781.
    [41] MAKINO H, KUSHIRO A, ISHIKAWA E, MUYLAERT D, KUBOTA H, SAKAI T, OISHI K, MARTIN R, BEN AMOR K, OOZEER R, KNOL J, TANAKA R. Transmission of intestinal Bifidobacterium longum subsp. longum strains from mother to infant, determined by multilocus sequencing typing and amplified fragment length polymorphism[J]. Applied and Environmental Microbiology, 2011, 77(19): 6788-6793.
    [42] LU WW, PEI ZM, ZANG MN, LEE YK, ZHAO JX, CHEN W, WANG HC, ZHANG H. Comparative genomic analysis of Bifidobacterium bifidum strains isolated from different niches[J]. Genes, 2021, 12(10): 1504.
    [43] OH PL, BENSON AK, PETERSON DA, PATIL PB, MORIYAMA EN, ROOS S, WALTER J. Diversification of the gut symbiont Lactobacillus reuteri as a result of host-driven evolution[J]. The ISME Journal, 2010, 4(3): 377-387.
    [44] MARTINO ME, BAYJANOV JR, CAFFREY BE, WELS M, JONCOUR P, HUGHES S, GILLET B, KLEEREBEZEM M, van HIJUM SAFT, LEULIER F. Nomadic lifestyle of Lactobacillus plantarum revealed by comparative genomics of 54 strains isolated from different habitats[J]. Environmental Microbiology, 2016, 18(12): 4974-4989.
    [45] ZOETENDAL EG, AKKERMANS ADL, AKKERMANS-VAN VLIET WM, de VISSER JAGM, de VOS WM. The host genotype affects the bacterial community in the human gastrointestinal tract[J]. Microbial Ecology in Health & Disease, 2001, 13(3): 4774-4781.
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JIN Zhixuan, WANG Ping, ZHANG Xueling, TIAN Fengwei, NI Yongqing. Genetic differences of intestinal Bifidobacterium bifidum among school-age children in Yining, Xinjiang: a study based on multilocus sequence typing[J]. Microbiology China, 2023, 50(12): 5487-5504

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  • Received:April 21,2023
  • Adopted:June 10,2023
  • Online: December 06,2023
  • Published: December 20,2023
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