Cited by 73Infant Nutrition and HealthGut microbiota and healthMicrobial Metabolites in Food Biotechnology

Utilization Efficiency of Human Milk Oligosaccharides by Human-Associated Akkermansia Is Strain Dependent

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Luna, Estefani, Parkar, Shanthi G., Kirmiz, Nina, Hartel, Stephanie, Hearn, Erik, Hossine, Marziiah, Kurdian, Arinnae, Mendoza, Claudia +11 more·2022·Applied and Environmental Microbiology

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Abstract

Human milk oligosaccharides (HMOs) are the third most abundant component of breast milk and provide several benefits to developing infants, including the recruitment of beneficial bacteria to the human gut. Akkermansia strains are largely considered beneficial bacteria and have been detected in colostrum, breast milk, and young infants. A. muciniphila Muc T belonging to the AmI phylogroup contributes to the HMO deconstruction capacity of the infant. Here, using phylogenomics, we examined the genomic capacities of four Akkermansia phylogroups to deconstruct HMOs.

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  1. [2]Kim S, Shin Y-C, Kim T-Y, Kim Y, Lee Y-S, Lee S-H, Kim M-N, O E, Kim KS, Kweon M-N. 2021. Mucin degrader Akkermansia muciniphila accelerates intestinal stem cell-mediated epithelial development. Gut Microbes 13: 1892441. 10.1080/19490976.2021.1892441. PMC7946046 33678130 · DOI
  2. [3]Dao MC, Everard A, Aron-Wisnewsky J, Sokolovska N, Prifti E, Verger EO, Kayser BD, Levenez F, Chilloux J, Hoyles L, MICRO-Obes Consortium, Dumas M-E, Rizkalla SW, Doré J, Cani PD, Clément K. 2016. Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: relationship with gut microbiome richness and ecology. Gut 65: 426– 436. 10.1136/gutjnl-2014-308778. 26100928 · DOI · Paper page
  3. [4]Rajilic-Stojanovic M, Shanahan F, Guarner F, de Vos WM. 2013. Phylogenetic analysis of dysbiosis in ulcerative colitis during remission. Inflamm Bowel Dis 19: 481– 488. 10.1097/MIB.0b013e31827fec6d. 23385241 · DOI
  4. [6]Lee M-J, Kang M-J, Lee S-Y, Lee E, Kim K, Won S, Suh DI, Kim KW, Sheen YH, Ahn K, Kim B-S, Hong S-J. 2018. Perturbations of gut microbiome genes in infants with atopic dermatitis according to feeding type. J Allergy Clin Immunol 141: 1310– 1319. 10.1016/j.jaci.2017.11.045. 29339259 · DOI
  5. [7]Ouwerkerk JP, van der Ark KCH, Davids M, Claassens NJ, Finestra TR, de Vos WM, Belzer C. 2016. Adaptation of Akkermansia muciniphila to the oxic-anoxic interface of the mucus layer. Appl Environ Microbiol 82: 6983– 6993. 10.1128/AEM.01641-16. 27663027 PMC5103097 · DOI
  6. [8]Robbe C, Capon C, Coddeville B, Michalski JC. 2004. Structural diversity and specific distribution of O-glycans in normal human mucins along the intestinal tract. Biochem J 384: 307– 316. 10.1042/BJ20040605. 15361072 PMC1134114 · DOI
  7. [9]Ottman N, Davids M, Suarez-Diez M, Boeren S, Schaap PJ, Martins Dos Santos VAP, Smidt H, Belzer C, de Vos WM. 2017. Genome-scale model and omics analysis of metabolic capacities of Akkermansia muciniphila reveal a preferential mucin-degrading lifestyle. Appl Environ Microbiol 83: e01014-17. 10.1128/AEM.01014-17. 28687644 PMC5583483 · DOI · Paper page
  8. [10]Kirmiz N, Galindo K, Cross KL, Luna E, Rhoades N, Podar M, Flores GE. 2020. Comparative genomics guides elucidation of vitamin B12 biosynthesis in novel human-associated Akkermansia strains. Appl Environ Microbiol 86: e02117-19. 10.1128/AEM.02117-19. 31757822 PMC6974653 · DOI · Paper page
  9. [11]Chia LW, Hornung BVH, Aalvink S, Schaap PJ, de Vos WM, Knol J, Belzer C. 2018. Deciphering the trophic interaction between Akkermansia muciniphila and the butyrogenic gut commensal Anaerostipes caccae using a metatranscriptomic approach. Antonie Van Leeuwenhoek 111: 859– 873. 10.1007/s10482-018-1040-x. 29460206 PMC5945754 · DOI
  10. [12]Cani PD, Van Hul M, Lefort C, Depommier C, Rastelli M, Everard A. 2019. Microbial regulation of organismal energy homeostasis. Nat Metab 1: 34– 46. 10.1038/s42255-018-0017-4. 32694818 · DOI · Paper page
  11. [13]Ottman N, Reunanen J, Meijerink M, Pietila TE, Kainulainen V, Klievink J, Huuskonen L, Aalvink S, Skurnik M, Boeren S, Satokari R, Mercenier A, Palva A, Smidt H, de Vos WM, Belzer C. 2017. Pili-like proteins of Akkermansia muciniphila modulate host immune responses and gut barrier function. PLoS One 12: e0173004. 10.1371/journal.pone.0173004. 28249045 PMC5332112 · DOI
  12. [15]Guo X, Li S, Zhang J, Wu F, Li X, Wu D, Zhang M, Ou Z, Jie Z, Yan Q, Li P, Yi J, Peng Y. 2017. Genome sequencing of 39 Akkermansia muciniphila isolates reveals its population structure, genomic and functional diverisity [sic], and global distribution in mammalian gut microbiotas. BMC Genomics 18: 800. 10.1186/s12864-017-4195-3. 29047329 PMC5648452 · DOI
  13. [16]Bode L. 2012. Human milk oligosaccharides: every baby needs a sugar mama. Glycobiology 22: 1147– 1162. 10.1093/glycob/cws074. 22513036 PMC3406618 · DOI · Paper page
  14. [17]Coker JK, Moyne O, Rodionov DA, Zengler K. 2021. Carbohydrates great and small, from dietary fiber to sialic acids: how glycans influence the gut microbiome and affect human health. Gut Microbes 13: 1869502. 10.1080/19490976.2020.1869502. PMC7899658 33615984 · DOI
  15. [18]Bode L, Jantscher-Krenn E. 2012. Structure-function relationships of human milk oligosaccharides. Adv Nutr 3: 383S– 391S. 10.3945/an.111.001404. 22585916 PMC3649474 · DOI
  16. [19]Kunz C, Rudloff S, Baier W, Klein N, Strobel S. 2000. Oligosaccharides in human milk: structural, functional, and metabolic aspects. Annu Rev Nutr 20: 699– 722. 10.1146/annurev.nutr.20.1.699. 10940350 · DOI
  17. [20]Garrido D, Barile D, Mills DA. 2012. A molecular basis for bifidobacterial enrichment in the infant gastrointestinal tract. Adv Nutr 3: 415S– 421S. 10.3945/an.111.001586. 22585920 PMC3649478 · DOI · Paper page
  18. [21]Kuntz S, Kunz C, Rudloff S. 2009. Oligosaccharides from human milk induce growth arrest via G2/M by influencing growth-related cell cycle genes in intestinal epithelial cells. Br J Nutr 101: 1306– 1315. 10.1017/S0007114508079622. 19079835 · DOI
  19. [22]Morrow AL, Ruiz-Palacios GM, Jiang X, Newburg DS. 2005. Human-milk glycans that inhibit pathogen binding protect breast-feeding infants against infectious diarrhea. J Nutr 135: 1304– 1307. 10.1093/jn/135.5.1304. 15867329 · DOI
  20. [23]Ward RE, Niñonuevo M, Mills DA, Lebrilla CB, German JB. 2006. In vitro fermentation of breast milk oligosaccharides by Bifidobacterium infantis and Lactobacillus gasseri. Appl Environ Microbiol 72: 4497– 4499. 10.1128/AEM.02515-05. 16751577 PMC1489581 · DOI
  21. [24]Marcobal A, Barboza M, Froehlich JW, Block DE, German JB, Lebrilla CB, Mills DA. 2010. Consumption of human milk oligosaccharides by gut-related microbes. J Agric Food Chem 58: 5334– 5340. 10.1021/jf9044205. 20394371 PMC2866150 · DOI · Paper page
  22. [25]Yu ZT, Chen C, Newburg DS. 2013. Utilization of major fucosylated and sialylated human milk oligosaccharides by isolated human gut microbes. Glycobiology 23: 1281– 1292. 10.1093/glycob/cwt065. 24013960 PMC3796377 · DOI
  23. [26]Kostopoulos I, Elzinga J, Ottman N, Klievink JT, Blijenberg B, Aalvink S, Boeren S, Mank M, Knol J, de Vos WM, Belzer C. 2020. Akkermansia muciniphila uses human milk oligosaccharides to thrive in the early life conditions in vitro. Sci Rep 10: 14330. 10.1038/s41598-020-71113-8. 32868839 PMC7459334 · DOI
  24. [27]Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. 2009. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37: D233– D238. 10.1093/nar/gkn663. 18838391 PMC2686590 · DOI
  25. [28]Yin Y, Mao X, Yang J, Chen X, Mao F, Xu Y. 2012. dbCAN: a Web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 40: W445– W451. 10.1093/nar/gks479. 22645317 PMC3394287 · DOI
  26. [29]Zhang H, Yohe T, Huang L, Entwistle S, Wu P, Yang Z, Busk PK, Xu Y, Yin Y. 2018. dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 46: W95– W101. 10.1093/nar/gky418. 29771380 PMC6031026 · DOI
  27. [30]Tailford LE, Crost EH, Kavanaugh D, Juge N. 2015. Mucin glycan foraging in the human gut microbiome. Front Genet 6: 81. 10.3389/fgene.2015.00081. 25852737 PMC4365749 · DOI
  28. [31]Katoh T, Ojima MN, Sakanaka M, Ashida H, Gotoh A, Katayama T. 2020. Enzymatic adaptation of Bifidobacterium bifidum to host glycans, viewed from glycoside hydrolyases and carbohydrate-binding modules. Microorganisms 8: 481. 10.3390/microorganisms8040481. PMC7232152 32231096 · DOI · Paper page
  29. [32]Low KE, Smith SP, Abbott DW, Boraston AB. 2021. The glycoconjugate-degrading enzymes of Clostridium perfringens: tailored catalysts for breaching the intestinal mucus barrier. Glycobiology 31: 681– 690. 10.1093/glycob/cwaa050. 32472136 · DOI
  30. [33]Ioannou A, Knol J, Belzer C. 2021. Microbial glycoside hydrolases in the first year of life: an analysis review on their presence and importance in infant gut. Front Microbiol 12: 631282. 10.3389/fmicb.2021.631282. 34122357 PMC8194493 · DOI · Paper page
  31. [34]Chen H, Kim J, Kendall DA. 1996. Competition between functional signal peptides demonstrates variation in affinity for the secretion pathway. J Bacteriol 178: 6658– 6664. 10.1128/jb.178.23.6658-6664.1996. 8955279 PMC178558 · DOI
  32. [35]Owji H, Nezafat N, Negahdaripour M, Hajiebrahimi A, Ghasemi Y. 2018. A comprehensive review of signal peptides: structure, roles, and applications. Eur J Cell Biol 97: 422– 441. 10.1016/j.ejcb.2018.06.003. 29958716 · DOI · Paper page
  33. [36]Zhai Q, Feng S, Arjan N, Chen W. 2019. A next generation probiotic, Akkermansia muciniphila. Crit Rev Food Sci Nutr 59: 3227– 3236. 10.1080/10408398.2018.1517725. 30373382 · DOI
  34. [37]Becken B, Davey L, Middleton DR, Mueller KD, Sharma A, Holmes ZC, Dallow E, Remick B, Barton GM, David LA, McCann JR, Armstrong SC, Malkus P, Valdivia RH. 2021. Genotypic and phenotypic diversity among human isolates of Akkermansia muciniphila. mBio 12: e00478-21. 10.1128/mBio.00478-21. 34006653 PMC8262928 · DOI · Paper page
  35. [38]Sela DA, Garrido D, Lerno L, Wu S, Tan K, Eom H-J, Joachimiak A, Lebrilla CB, Mills DA. 2012. Bifidobacterium longum subsp. infantis ATCC 15697 α-fucosidases are active on fucosylated human milk oligosaccharides. Appl Environ Microbiol 78: 795– 803. 10.1128/AEM.06762-11. 22138995 PMC3264123 · DOI
  36. [39]Kiyohara M, Tanigawa K, Chaiwangsri T, Katayama T, Ashida H, Yamamoto K. 2011. An exo-alpha-sialidase from bifidobacteria involved in the degradation of sialyloligosaccharides in human milk and intestinal glycoconjugates. Glycobiology 21: 437– 447. 10.1093/glycob/cwq175. 21036948 · DOI
  37. [41]Matsuki T, Yahagi K, Mori H, Matsumoto H, Hara T, Tajima S, Ogawa E, Kodama H, Yamamoto K, Yamada T, Matsumoto S, Kurokawa K. 2016. A key genetic factor for fucosyllactose utilization affects infant gut microbiota development. Nat Commun 7: 11939. 10.1038/ncomms11939. 27340092 PMC4931012 · DOI
  38. [42]James K, Motherway MO, Bottacini F, van Sinderen D. 2016. Bifidobacterium breve UCC2003 metabolises the human milk oligosaccharides lacto-N-tetraose and lacto-N-neo-tetraose through overlapping, yet distinct pathways. Sci Rep 6: 38560. 10.1038/srep38560. 27929046 PMC5144078 · DOI
  39. [43]Garrido D, Ruiz-Moyano S, Kirmiz N, Davis JC, Totten SM, Lemay DG, Ugalde JA, German JB, Lebrilla CB, Mills DA. 2016. A novel gene cluster allows preferential utilization of fucosylated milk oligosaccharides in Bifidobacterium longum subsp. longum SC596. Sci Rep 6: 35045. 10.1038/srep35045. 27756904 PMC5069460 · DOI
  40. [45]Garrido D, Kim JH, German JB, Raybould HE, Mills D. 2011. Oligosaccharide binding proteins from Bifidobacterium longum subsp. infantis reveal a preference for host glycans. PLoS One 6: e17315. 10.1371/journal.pone.0017315. 21423604 PMC3057974 · DOI
  41. [46]Yoshida E, Sakurama H, Kiyohara M, Nakajima M, Kitaoka M, Ashida H, Hirose J, Katayama T, Yamamoto K, Kumagai H. 2012. Bifidobacterium longum subsp. infantis uses two different β-galactosidases for selectively degrading type-1 and type-2 human milk oligosaccharides. Glycobiology 22: 361– 368. 10.1093/glycob/cwr116. 21926104 · DOI
  42. [47]Ruiz-Moyano S, Totten SM, Garrido D, Smilowitz JT, German JB, Lebrilla CB, Mills DA. 2013. Variation in consumption of human milk oligosaccharides by infant gut-associated strains of Bifidobacterium breve. Appl Environ Microbiol 79: 6040– 6049. 10.1128/AEM.01843-13. 23892749 PMC3811376 · DOI
  43. [48]Turroni F, Bottacini F, Foroni E, Mulder I, Kim JH, Zomer A, Sanchez B, Bidossi A, Ferrarini A, Giubellini V, Delledonne M, Henrissat B, Coutinho P, Oggioni M, Fitzgerald GF, Mills D, Margolles A, Kelly D, van Sinderen D, Ventura M. 2010. Genome analysis of Bifidobacterium bifidum PRL2010 reveals metabolic pathways for host-derived glycan foraging. Proc Natl Acad Sci USA 107: 19514– 19519. 10.1073/pnas.1011100107. 20974960 PMC2984195 · DOI · Paper page
  44. [49]Marcobal A, Sonnenburg JL. 2012. Human milk oligosaccharide consumption by intestinal microbiota. Clin Microbiol Infect 18: 12– 15. 10.1111/j.1469-0691.2012.03863.x. 22647041 PMC3671919 · DOI
  45. [50]Laursen MF, Bahl MI, Licht TR. 2021. Settlers of our inner surface—factors shaping the gut microbiota from birth to toddlerhood. FEMS Microbiol Rev 45: fuab001. 10.1093/femsre/fuab001. 33428723 PMC8371275 · DOI
  46. [51]Sampson EM, Bobik TA. 2008. Microcompartments for B12-dependent 1,2-propanediol degradation provide protection from DNA and cellular damage by a reactive metabolic intermediate. J Bacteriol 190: 2966– 2971. 10.1128/JB.01925-07. 18296526 PMC2293232 · DOI
  47. [52]Engels C, Ruscheweyh H-J, Beerenwinkel N, Lacroix C, Schwab C. 2016. The common gut microbe Eubacterium hallii also contributes to intestinal propionate formation. Front Microbiol 7: 713. 10.3389/fmicb.2016.00713. 27242734 PMC4871866 · DOI · Paper page
  48. [53]Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, Heath AC, Warner B, Reeder J, Kuczynski J, Caporaso JG, Lozupone CA, Lauber C, Clemente JC, Knights D, Knight R, Gordon JI. 2012. Human gut microbiome viewed across age and geography. Nature 486: 222– 227. 10.1038/nature11053. 22699611 PMC3376388 · DOI · Paper page
  49. [54]Collado MC, Derrien M, Isolauri E, de Vos WM, Salminen S. 2007. Intestinal integrity and Akkermansia muciniphila, a mucin-degrading member of the intestinal microbiota present in infants, adults, and the elderly. Appl Environ Microbiol 73: 7767– 7770. 10.1128/AEM.01477-07. 17933936 PMC2168041 · DOI · Paper page
  50. [55]Collado MC, Laitinen K, Salminen S, Isolauri E. 2012. Maternal weight and excessive weight gain during pregnancy modify the immunomodulatory potential of breast milk. Pediatr Res 72: 77– 85. 10.1038/pr.2012.42. 22453296 · DOI
  51. [56]Lackey KA, Williams JE, Meehan CL, Zachek JA, Benda ED, Price WJ, Foster JA, Sellen DW, Kamau-Mbuthia EW, Kamundia EW, Mbugua S, Moore SE, Prentice AM, K DG, Kvist LJ, Otoo GE, Garcia-Carral C, Jimenez E, Ruiz L, Rodriguez JM, Pareja RG, Bode L, McGuire MA, McGuire MK. 2019. What’s normal? Microbiomes in human milk and infant feces are related to each other but vary geographically: the INSPIRE study. Front Nutr 6: 45. 10.3389/fnut.2019.00045. 31058158 PMC6479015 · DOI
  52. [57]Korpela K, Salonen A, Hickman B, Kunz C, Sprenger N, Kukkonen K, Savilahti E, Kuitunen M, de Vos WM. 2018. Fucosylated oligosaccharides in mother’s milk alleviate the effects of caesarean birth on infant gut microbiota. Sci Rep 8: 13757. 10.1038/s41598-018-32037-6. 30214024 PMC6137148 · DOI
  53. [58]Aakko J, Kumar H, Rautava S, Wise A, Autran C, Bode L, Isolauri E, Salminen S. 2017. Human milk oligosaccharide categories define the microbiota composition in human colostrum. Benef Microbes 8: 563– 567. 10.3920/BM2016.0185. 28726512 · DOI
  54. [59]Thurl S, Munzert M, Henker J, Boehm G, Müller-Werner B, Jelinek J, Stahl B. 2010. Variation of human milk oligosaccharides in relation to milk groups and lactational periods. Br J Nutr 104: 1261– 1271. 10.1017/S0007114510002072. 20522272 · DOI
  55. [60]Wang B, Brand-Miller J. 2003. The role and potential of sialic acid in human nutrition. Eur J Clin Nutr 57: 1351– 1369. 10.1038/sj.ejcn.1601704. 14576748 · DOI
  56. [62]Jacobi SK, Yatsunenko T, Li D, Dasgupta S, Yu RK, Berg BM, Chichlowski M, Odle J. 2016. Dietary isomers of sialyllactose increase ganglioside sialic acid concentrations in the corpus callosum and cerebellum and modulate the colonic microbiota of formula-fed piglets. J Nutr 146: 200– 208. 10.3945/jn.115.220152. 26701794 · DOI
  57. [63]Almagro-Moreno S, Boyd EF. 2010. Bacterial catabolism of nonulosonic (sialic) acid and fitness in the gut. Gut Microbes 1: 45– 50. 10.4161/gmic.1.1.10386. 21327116 PMC3035139 · DOI
  58. [64]Egan M, O’Connell Motherway M, Ventura M, van Sinderen D. 2014. Metabolism of sialic acid by Bifidobacterium breve UCC2003. Appl Environ Microbiol 80: 4414– 4426. 10.1128/AEM.01114-14. 24814790 PMC4068672 · DOI
  59. [65]van der Ark KCH, Aalvink S, Suarez-Diez M, Schaap PJ, de Vos WM, Belzer C. 2018. Model-driven design of a minimal medium for Akkermansia muciniphila confirms mucus adaptation. Microb Biotechnol 11: 476– 485. 10.1111/1751-7915.13033. 29377524 PMC5902328 · DOI
  60. [66]Rokhsefat S, Lin A, Comelli EM. 2016. Mucin-microbiota interaction during postnatal maturation of the intestinal ecosystem: clinical implications. Dig Dis Sci 61: 1473– 1486. 10.1007/s10620-016-4032-6. 26792279 · DOI
  61. [67]Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar, Buchner A, Lai T, Steppi S, Jobb G, Forster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, Konig A, Liss T, Lussmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer K-H. 2004. ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363– 1371. 10.1093/nar/gkh293. 14985472 PMC390282 · DOI
  62. [68]Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 33: 1870– 1874. 10.1093/molbev/msw054. 27004904 PMC8210823 · DOI
  63. [69]Oliver A, Kay M, Cooper KK. 2018. Comparative genomics of cocci-shaped Sporosarcina strains with diverse spatial isolation. BMC Genomics 19: 310. 10.1186/s12864-018-4635-8. 29716534 PMC5930826 · DOI
  64. [70]Parker CT, Cooper KK, Huynh S, Smith TP, Bono JL, Cooley M. 2018. Genome sequences of eight Shiga toxin-producing Escherichia coli strains isolated from a produce-growing region in California. Microbiol Resour Announc 7: e00807-18. 10.1128/MRA.00807-18. 30533611 PMC6211345 · DOI
  65. [71]Wattam AR, Davis JJ, Assaf R, Boisvert S, Brettin T, Bun C, Conrad N, Dietrich EM, Disz T, Gabbard JL, Gerdes S, Henry CS, Kenyon RW, Machi D, Mao C, Nordberg EK, Olsen GJ, Murphy-Olson DE, Olson R, Overbeek R, Parrello B, Pusch GD, Shukla M, Vonstein V, Warren A, Xia F, Yoo H, Stevens RL. 2017. Improvements to PATRIC, the all-bacterial bioinformatics database and analysis resource center. Nucleic Acids Res 45: D535– D542. 10.1093/nar/gkw1017. 27899627 PMC5210524 · DOI
  66. [72]Wick RR, Judd LM, Gorrie CL, Holt KE. 2017. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 13: e1005595. 10.1371/journal.pcbi.1005595. 28594827 PMC5481147 · DOI
  67. [73]Brettin T, Davis JJ, Disz T, Edwards RA, Gerdes S, Olsen GJ, Olson R, Overbeek R, Parrello B, Pusch GD, Shukla M, Thomason JA, III, Stevens R, Vonstein V, Wattam AR, Xia F. 2015. RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep 5: 8365. 10.1038/srep08365. 25666585 PMC4322359 · DOI
  68. [74]van Passel MW, Kant R, Zoetendal EG, Plugge CM, Derrien M, Malfatti SA, Chain PS, Woyke T, Palva A, de Vos WM, Smidt H. 2011. The genome of Akkermansia muciniphila, a dedicated intestinal mucin degrader, and its use in exploring intestinal metagenomes. PLoS One 6: e16876. 10.1371/journal.pone.0016876. 21390229 PMC3048395 · DOI
  69. [75]Finn RD, Clements J, Eddy SR. 2011. HMMER Web server: interactive sequence similarity searching. Nucleic Acids Res 39: W29– W37. 10.1093/nar/gkr367. 21593126 PMC3125773 · DOI · Paper page
  70. [76]Buchfink B, Xie C, Huson DH. 2015. Fast and sensitive protein alignment using DIAMOND. Nat Methods 12: 59– 60. 10.1038/nmeth.3176. 25402007 · DOI · Paper page
  71. [77]Busk PK, Pilgaard B, Lezyk MJ, Meyer AS, Lange L. 2017. Homology to peptide pattern for annotation of carbohydrate-active enzymes and prediction of function. BMC Bioinformatics 18: 214. 10.1186/s12859-017-1625-9. 28403817 PMC5389127 · DOI
  72. [81]Campbell JH, O’Donoghue P, Campbell AG, Schwientek P, Sczyrba A, Woyke T, Soll D, Podar M. 2013. UGA is an additional glycine codon in uncultured SR1 bacteria from the human microbiota. Proc Natl Acad Sci USA 110: 5540– 5545. 10.1073/pnas.1303090110. 23509275 PMC3619370 · DOI
  73. [82]Eren AM, Esen OC, Quince C, Vineis JH, Morrison HG, Sogin ML, Delmont TO. 2015. Anvi’o: an advanced analysis and visualization platform for ‘omics data. PeerJ 3: e1319. 10.7717/peerj.1319. 26500826 PMC4614810 · DOI
  74. [83]Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792– 1797. 10.1093/nar/gkh340. 15034147 PMC390337 · DOI · Paper page
  75. [84]Jones DT, Taylor WR, Thornton JM. 1992. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8: 275– 282. 10.1093/bioinformatics/8.3.275. 1633570 · DOI
  76. [85]Hardy MR, Townsend RR, Lee YC. 1988. Monosaccharide analysis of glycoconjugates by anion exchange chromatography with pulsed amperometric detection. Anal Biochem 170: 54– 62. 10.1016/0003-2697(88)90089-9. 3389518 · DOI
  77. [86]Townsend RR, Hardy MR, Cumming DA, Carver JP, Bendiak B. 1989. Separation of branched sialylated oligosaccharides using high-pH anion-exchange chromatography with pulsed amperometric detection. Anal Biochem 182: 1– 8. 10.1016/0003-2697(89)90708-2. 2481411 · DOI

Authors
Luna, E., Parkar, S. G., Kirmiz, N., Hartel, S., Hearn, E., Hossine, M., Kurdian, A., Mendoza, C., Orr, K., Padilla, L., Ramirez, K., Salcedo, P., Serrano, E., Choudhury, B., Paulchakrabarti, M., Parker, C. T., Huynh, S., Cooper, K., & Flores, G. E.
Affiliations
  • California State University, Northridge (US)
  • UC San Diego Health System (US)
  • Agricultural Research Service (US)
  • University of Arizona (US)
Corresponding author
Flores, Gilberto E.
Venue
Applied and Environmental Microbiology
Published
2022-01-11
Volume
88
Issue
1
ISSN
  • 0099-2240 (ISSN-L)
  • 1098-5336
OpenAlex
W4288059046
Cited by
73
References
84
Citations by year
2026: 13 · 2025: 18 · 2024: 20 · 2023: 17 · 2022: 5
FWCI
6.69
Type
journal article
Language
en
Open access
Locations
  • Applied and Environmental Microbiology (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
Funders
HHS | NIH | National Institute of General Medical Sciences (SC2GM122620 and SC1GM136546, TL4GM118977 RL5GM118975 and UL1GM118976)
Topics
  • Health Sciences › Nursing › Nutrition and Dietetics › Infant Nutrition and Health
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Health Sciences › Nursing › Nutrition and Dietetics › Microbial Metabolites in Food Biotechnology
Keywords
human milk oligosaccharides, Akkermansia, Akkermansia muciniphila, infant gut microbiota, phylogenomics, colostrum, breast milk

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