Cited by 10Probiotics and Fermented FoodsInfant Nutrition and HealthGut microbiota and health

The DOI matches its Crossref record; 6 of the 6 references it cites were found in a registry or an index.

Genome analysis and 2’-fucosyllactose utilization characteristics of a new Akkermansia muciniphila strain isolated from mice feces

Abstract

Akkermansia muciniphila is considered to be a next-generation probiotic, and closely related to host metabolism and immune response. Compared with other probiotics, little is known about its genomic analysis. Therefore, further researches about isolating more A. muciniphila strains and exploring functional genes are needed. In the present study, a new strain isolated from mice feces was identified as A. muciniphila (Muc X). Whole-genome sequencing and annotation revealed that Muc X possesses key genes necessary for human milk oligosaccharides (HMO) utilization, including α-L-fucosidases, β-galactosidases, exo-α-sialidases, and β-acetylhexosaminidases. The complete metabolic pathways for γ-aminobutyric acid and squalene and genes encoding functional proteins, such as the outer membrane protein Amuc_1100, were annotated in the Muc X genome. Comparative genome analysis was used to identify functional genes unique to Muc X compared to six other A. muciniphila strains. Results showed Muc X genome possesses unique genes, including sugar transporters and transferases. Single-strain incubation revealed faster utilization of 2'-fucosyllactose (2'-FL), galacto-oligosaccharides, and lactose by Muc X than by A. muciniphila DSM 22959. This study isolated and identified an A. muciniphila strain that can utilize 2'-FL, and expolored the genes related to HMO utilization and special metabolites, which provided a theoretical basis for the further excavation of A. muciniphila function and the compound application with fucosylated oligosaccharides.

Overview

Integrity signals

Registry

Crossref · 10.1007/s00438-022-01937-8

Cites

6 of 6 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 53

  1. 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 · DOI
  2. Arnold JW, Roach J, Fabela S, Moorfield E, Ding S, Blue E, Dagher S, Magness S, Tamayo R, Bruno-Barcena JM, Azcarate-Peril MA (2021) The pleiotropic effects of prebiotic galacto-oligosaccharides on the aging gut. Microbiome 9:31 · DOI
  3. Bertelli C, Tilley KE, Brinkman FSL (2019) Microbial genomic island discovery, visualization and analysis. Brief Bioinform 20(5):1685–1698 · DOI
  4. Bian X, Wu W, Yang L, Lv L, Wang Q, Li Y, Ye J, Fang D, Wu J, Jiang X, Shi D, Li L (2019) Administration of Akkermansia muciniphila ameliorates dextran sulfate sodium-induced ulcerative colitis in mice. Front Microbiol 10:2259 · DOI
  5. Bisson LF, Fan Q, Walker GA (2016) Sugar and glycerol transport in saccharomyces cerevisiae. Adv Exp Med Biol 892:125–168 · DOI
  6. Buchfink B, Xie C, Huson DH (2015) Fast and sensitive protein alignment using DIAMOND. Nat Methods 12:59–60 · DOI · Paper page
  7. 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:D233-238 · DOI
  8. Chapman GB, Hillier J (1953) Electron microscopy of ultra-thin sections of bacteria I. Cellular division in Bacillus cereus. J Bacteriol 66:362–373 · DOI
  9. Curiel J, Peirotén Á, Landete J, Bastida A, Langa S, Arqués J (2021) Architecture insight of bifidobacterial α-l-fucosidases. Int J Mol Sci 22(16):8462 · DOI
  10. Delcher AL, Bratke KA, Powers EC, Salzberg SL (2007) Identifying bacterial genes and endosymbiont DNA with glimmer. Bioinformatic 23(6):673–679 · DOI
  11. Derrien M, Vaughan EE, Plugge CM, de Vos WM (2004) Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol 54:1469–1476 · DOI · Paper page
  12. Ghimire GP, Thuan NH, Koirala N, Sohng JK (2016) Advances in biochemistry and microbial production of squalene and its derivatives. J Microbiol Biotechnol 26(3):441–451 · DOI
  13. Grześkowiak Ł, Collado MC, Mangani C, Maleta K, Laitinen K, Ashorn P, Isolauri E, Salminen S (2012) Distinct gut microbiota in southeastern African and northern European infants. J Pediatr Gastroenterol Nutr 54:812–816 · DOI
  14. 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 diversity, and global distribution in mammalian gut microbiotas. BMC Genomics 18(1):800 · DOI
  15. Hagi T, Geerlings SY, Nijsse B, Belzer C (2020) The effect of bile acids on the growth and global gene expression profiles in Akkermansia muciniphila. Appl Microbiol Biotechnol 104:10641–10653 · DOI
  16. Hasan MM, Khan SN, Karim MM, Begum A, Hoq MM (2019) Complete genome and plasmid sequence of a novel Bacillus sp. BD59S, a parasporal protein synthesizing bacterium. 3 Biotech 9:318 · DOI
  17. Henrick BM, Rodriguez L, Lakshmikanth T, Pou C, Henckel E, Arzoomand A, Olin A, Wang J, Mikes J, Tan Z, Chen Y, Ehrlich AM, Bernhardsson AK, Mugabo CH, Ambrosiani Y, Gustafsson A, Chew S, Brown HK, Prambs J, Bohlin K, Mitchell RD, Underwood MA, Smilowitz JT, German JB, Frese SA, Brodin P (2021) Bifidobacteria-mediated immune system imprinting early in life. Cell 184:3884–3898 · DOI
  18. Higarza SG, Arboleya S, Arias JL, Gueimonde M, Arias N (2021) Akkermansia muciniphila and environmental enrichment reverse cognitive impairment associated with high-fat high-cholesterol consumption in rats. Gut Microbes 13:1880240 · DOI
  19. Karcher N, Nigro E, Punčochář M, Blanco-Míguez A, Ciciani M, Manghi P, Zolfo M, Cumbo F, Manara S, Golzato D, Cereseto A, Arumugam M, Bui TPN, Tytgat HLP, Valles-Colomer M, de Vos WM, Segata N (2021) Genomic diversity and ecology of human-associated Akkermansia species in the gut microbiome revealed by extensive metagenomic assembly. Genome Biol 22:209 · DOI · Paper page
  20. Korpela K, Salonen A, Hickman B, Kunz C, Sprenger N, Kukkonen K, Savilahti E, Kuitunen M, de Vos W (2018) Fucosylated oligosaccharides in mother’s milk alleviate the effects of caesarean birth on infant gut microbiota. Sci Rep 8:13757 · DOI
  21. Koskiniemi S, Lamoureux JG, Nikolakakis KC, de Roodenbeke C, Kaplan MD, Low DA, Hayes CS (2013) Rhs proteins from diverse bacteria mediate intercellular competition. Proc Natl Acad Sci USA 110:7032–7037 · DOI
  22. 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 · DOI
  23. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 70 for bigger datasets. Mol Biol Evol 33(7):1870–1874 · DOI
  24. Lawson MAE, O’Neill IJ, Kujawska M, Gowrinadh Javvadi S, Wijeyesekera A, Flegg Z, Chalklen L, Hall LJ (2020) Breast milk-derived human milk oligosaccharides promote Bifidobacterium interactions within a single ecosystem. ISME J 14:635–648 · DOI
  25. Li N, Fu X, Xiao M, Wei X, Yang M, Liu Z, Mou H (2020) Enzymatic preparation of a low-molecular-weight polysaccharide rich in uronic acid from the seaweed Laminaria japonica and evaluation of its hypolipidemic effect in mice. Food Funct 11:2395–2405 · DOI
  26. Li N, Liu B, Diao M, Lu J, Liu W, Tong Y (2021) Construction of squalene producing cell factories and screening, cloning and expression of key genes. Chin J Biotechnol 37:2813–2824
  27. Liu N, Zhu L, Zhang Z, Huang H, Jiang L (2019) Draft genome sequence of a multidrug-resistant blaOXA-69-producing Acinetobacter baumannii L13 isolated from Tarim River sample in China. J Global Antimicrob Resist 18:145–147 · DOI
  28. Lowe TM, Chan PP (2016) tRNAscan-SE on-line: Search and contextual analysis of transfer RNA genes. Nucleic Acids Res 44:W54-57 · DOI
  29. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar BA, 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 KH (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371 · DOI
  30. Luna E, Parkar SG, 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 CT, Huynh S, Cooper K, Flores GE (2022) Utilization efficiency of human milk oligosaccharides by human-associated Akkermansia is strain dependent. Appl Environ Microbiol 88(1):e01487-e1521 · DOI · Paper page
  31. Meng X, Zhang J, Wu H, Yu D, Fang X (2020) Akkermansia muciniphila aspartic protease Amuc_1434* inhibits human colorectal cancer LS174T cell viability via TRAIL-mediated apoptosis pathway. Int J Mol Sci 21:3385 · DOI
  32. Olson CA, Vuong HE, Yano JM, Liang QY, Nusbaum DJ, Hsiao EY (2018) The gut microbiota mediates the anti-seizure effects of the ketogenic diet. Cell 173:1728–1741 · DOI · Paper page
  33. Ottman N (2015) Host immunostimulation and substrate utilization of the gut symbiont Akkermansia muciniphila. PhD thesis. Wageningen University, Wageningen, the Netherlands
  34. 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-e1017 · DOI · Paper page
  35. Ouwerkerk JP, Aalvink S, Belzer C, de Vos WM (2016) Akkermansia glycaniphila sp. nov., an anaerobic mucin-degrading bacterium isolated from reticulated python faeces. Int J Syst Evol Microbiol 66(11):4614–4620 · DOI
  36. Plovier H, Everard A, Druart C, Depommier C, Van Hul M, Geurts L, Chilloux J, Ottman N, Duparc T, Lichtenstein L, Myridakis A, Delzenne NM, Klievink J, Bhattacharjee A, van der Ark KC, Aalvink S, Martinez LO, Dumas ME, Maiter D, Loumaye A, Hermans MP, Thissen JP, Belzer C, de Vos WM, Cani PD (2017) A purified membrane protein from Akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice. Nat Med 23:107–113 · DOI · Paper page
  37. Régnier M, Rastelli M, Morissette A, Suriano F, Le Roy T, Pilon G, Delzenne NM, Marette A, Van Hul M, Cani PD (2020) Rhubarb supplementation prevents diet-induced obesity and diabetes in association with increased Akkermansia muciniphila in mice. Nutrients 12:2932 · DOI
  38. Ribo S, Sánchez-Infantes D, Martinez-Guino L, García-Mantrana I, Ramon-Krauel M, Tondo M, Arning E, Nofrarías M, Osorio-Conles Ó, Fernández-Pérez A, González-Torres P, Cebrià J, Gavaldà-Navarro A, Chenoll E, Isganaitis E, Villarroya F, Vallejo M, Segalés J, Jiménez-Chillarón JC, Bottiglieri T, Demerath EW, Fields DA, Collado MC, Lerin C (2021) Increasing breast milk betaine modulates Akkermansia abundance in mammalian neonates and improves long-term metabolic health. Sci Transl Med 13:eabb0322 · DOI
  39. Richter M, Rosselló-Móra R, Glöckner FO, Peplies J (2015) JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 32(6):929–931 · DOI
  40. Sánchez-Fidalgo S, Villegas I, Rosillo MÁ, Aparicio-Soto M, de la Lastra CA (2015) Dietary squalene supplementation improves DSS-induced acute colitis by downregulating p38 MAPK and NFkB signaling pathways. Mol Nutr Food Res 59:284–292 · DOI
  41. Sela DA, Chapman J, Adeuya A, Kim JH, Chen F, Whitehead TR, Lapidus A, Rokhsar DS, Lebrilla CB, German JB, Price NP, Richardson PM, Mills DA (2008) The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. Proc Natl Acad Sci USA 105:18964–18969 · DOI
  42. Shi L, Muthukumar V, Stachon T, Latta L, Elhawy MI, Gunaratnam G, Orosz E, Seitz B, Kiderlen AF, Bischoff M, Szentmáry N (2020) The effect of anti-amoebic agents and Ce6-PDT on Acanthamoeba castellanii trophozoites and cysts, in vitro. Transl vis Sci Technol 9:29 · DOI
  43. Spanova M, Zweytick D, Lohner K, Klug L, Leitner E, Hermetter A, Daum G (2012) Influence of squalene on lipid particle/droplet and membrane organization in the yeast Saccharomyces cerevisiae. Biochem Biophys Acta 1821:647–653
  44. Takada H, Katoh T, Katayama T (2020) Sialylated O -Glycans from hen egg white ovomucin are decomposed by mucin-degrading gut microbes. J Appl Glycosci 67:31–39 · DOI
  45. Thanapreedawat P, Kobayashi H, Inui N, Sakamoto K, Kim M, Yoto A, Yokogoshi H (2013) GABA affects novel object recognition memory and working memory in rats. J Nutr Sci Vitaminol 59:152–157 · DOI
  46. 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(3):e16876 · DOI
  47. Wu R, Zhou M, Wu H (2021) Purification and characterization of an active N-acetylglucosaminyltransferase enzyme complex from Streptococci. Appl Environ Microbiol 76:7966–7971 · DOI
  48. Wu J, Xu R, Lu J, Liu W, Yu H, Liu M, Li J, Yin M, Peng H, Zha L (2022) Molecular cloning and functional characterization of two squalene synthase genes in Atractylodes lancea. Planta 255:8 · DOI
  49. Xiao M, Ren X, Cui J, Li R, Liu Z, Zhu L, Kong Q, Fu X, Mou H (2022) A novel glucofucobiose with potential prebiotic activity prepared from the exopolysaccharides of Clavibacter michiganensis M1. Food Chem 377:132001 · DOI
  50. Yoon HS, Cho CH, Yun MS, Jang SJ, You HJ, Kim JH, Han D, Cha KH, Moon SH, Lee K, Kim YJ, Lee SJ, Nam TW, Ko G (2021) Akkermansia muciniphila secretes a glucagon-like peptide-1-inducing protein that improves glucose homeostasis and ameliorates metabolic disease in mice. Nat Microbiol 6:563–573 · DOI · Paper page
  51. Zhai R, Xue X, Zhang L, Yang X, Zhao L, Zhang C (2019) Strain-specific anti-inflammatory properties of two Akkermansia muciniphila strains on chronic colitis in mice. Front Cell Infect Microbiol 9:239 · DOI · Paper page
  52. Zhu L, Zhang D, Zhu H, Zhu J, Weng S, Dong L, Liu T, Hu Y, Shen X (2017) Berberine treatment increases Akkermansia in the gut and improves high-fat diet-induced atherosclerosis in Apoe-/- mice. Atherosclerosis 268:117–126 · DOI
  53. Zou Y, Wang J, Wang Y, Peng B, Liu J, Zhang B, Lv H, Wang S (2020) Protection of galacto-oligosaccharide against E coli O157 colonization through enhancing gut barrier function and modulating gut microbiota. Foods 9:1710 · DOI

Cited by

Sorted by citations

Metadata

Authors
Gao, W., Xiao, M., Gu, Z., Fu, X., Ren, X., Yu, Y., Liu, Z., Zhu, C., Kong, Q., & Mou, H.
Affiliations
  • Ocean University of China (CN)
  • Nanchang University (CN)
Corresponding author
Mou, Haijin
Venue
Molecular Genetics and Genomics
Published
2022-08-10
Volume
297
Issue
6
Pages
1515-1528
ISSN
  • 1617-4615 (ISSN-L)
  • 1617-4623
OpenAlex
W4290960081
Cited by
10
References
6
Citations by year
2026: 1 · 2025: 5 · 2024: 1 · 2023: 3
FWCI
1.20
Type
journal article
Language
en
Open access
closed
Locations
  • Molecular Genetics and Genomics (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Natural Science Foundation of China (31872893)
  • China Postdoctoral Science Foundation (2021M701547)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
  • Health Sciences › Nursing › Nutrition and Dietetics › Infant Nutrition and Health
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Keywords
Akkermansia muciniphila, human milk oligosaccharides, gut microbiota, probiotics, whole genome sequencing, comparative genomics, sugar transporters, galactooligosaccharides, lactose metabolism, Amuc_1100
MeSH terms
Akkermansia, Animals, beta-Galactosidase, Feces, gamma-Aminobutyric Acid, Humans, Lactose, Membrane Proteins, Oligosaccharides, Squalene, Transferases, Trisaccharides, Mice, Verrucomicrobia

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review