Comparative Genomics Guides Elucidation of Vitamin B12 Biosynthesis in Novel Human-Associated Akkermansia Strains

Kirmiz, Nina; Galindo, Kadir; Cross, Karissa L.; Luna, Estefani; Rhodes, Nicholas; Podar, Mircea; Flores, Gilberto E.

doi:10.1128/AEM.02117-19

Title: Comparative Genomics Guides Elucidation of Vitamin B₁₂ Biosynthesis in Novel Human-Associated Akkermansia Strains

Journal Article · 22 November 2019 · Applied and Environmental Microbiology

DOI: https://doi.org/10.1128/AEM.02117-19 · OSTI ID:1606768

Kirmiz, Nina ^[1]; Galindo, Kadir ^[1]; Cross, Karissa L. ^[2]; Luna, Estefani ^[1]; Rhodes, Nicholas ^[3];

^[2];

^[1]

California State Univ., Northridge, CA (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
California State Univ., Northridge, CA (United States); Univ. of California, Irvine, CA (United States)

Akkermansia muciniphila is a mucin-degrading bacterium found in the gut of most humans and is considered a “next-generation probiotic.” However, knowledge of the genomic and physiological diversity of human-associated Akkermansia sp. strains is limited. Here, we reconstructed 35 metagenome-assembled genomes and combined them with 40 publicly available genomes for comparative genomic analysis. We identified at least four species-level phylogroups (AmI to AmIV), with distinct functional potentials. Most notably, we identified genes for cobalamin (vitamin B₁₂) biosynthesis within the AmII and AmIII phylogroups. To verify these predictions, 10 Akkermansia strains were isolated from adults and screened for vitamin B₁₂ biosynthesis genes via PCR. Two AmII strains were positive for the presence of cobalamin biosynthesis genes, while all 9 AmI strains tested were negative. To demonstrate vitamin B₁₂ biosynthesis, we measured the production of acetate, succinate, and propionate in the presence and absence of vitamin supplementation in representative strains of the AmI and AmII phylogroups, since cobalamin is an essential cofactor in propionate metabolism. Results showed that the AmII strain produced acetate and propionate in the absence of supplementation, which is indicative of vitamin B₁₂ biosynthesis. In contrast, acetate and succinate were the main fermentation products for the AmI strains when vitamin B₁₂ was not supplied in the culture medium. Lastly, two bioassays were used to confirm vitamin B₁₂ production by the AmII phylogroup. This novel physiological trait of human-associated Akkermansia strains may affect how these bacteria interact with the human host and other members of the human gut microbiome.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1606768

Journal Information:: Applied and Environmental Microbiology, Vol. 86, Issue 3; ISSN 0099-2240

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 35 works

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References (85)

Anvi’o: an advanced analysis and visualization platform for ‘omics data Eren, A. Murat; Esen, Özcan C.; Quince, Christopher PeerJ, Vol. 3 https://doi.org/10.7717/peerj.1319	journal	January 2015
The Mucin Degrader Akkermansia muciniphila Is an Abundant Resident of the Human Intestinal Tract Derrien, M.; Collado, M. C.; Ben-Amor, K. Applied and Environmental Microbiology, Vol. 74, Issue 5 https://doi.org/10.1128/AEM.01226-07	journal	December 2007
Akkermansia muciniphila induces gut microbiota remodelling and controls islet autoimmunity in NOD mice Hänninen, Arno; Toivonen, Raine; Pöysti, Sakari Gut, Vol. 67, Issue 8 https://doi.org/10.1136/gutjnl-2017-314508	journal	December 2017
An SHR–SCR module specifies legume cortical cell fate to enable nodulation Dong, Wentao; Zhu, Yayun; Chang, Huizhong Nature, Vol. 589, Issue 7843 https://doi.org/10.1038/s41586-020-3016-z	journal	December 2020
Bacterial Community Variation in Human Body Habitats Across Space and Time Costello, E. K.; Lauber, C. L.; Hamady, M. Science, Vol. 326, Issue 5960 https://doi.org/10.1126/science.1177486	journal	November 2009
Shifting the genomic gold standard for the prokaryotic species definition Richter, Michael; Rosselló-Móra, Ramon Proceedings of the National Academy of Sciences, Vol. 106, Issue 45 https://doi.org/10.1073/pnas.0906412106	journal	October 2009
Quality control and preprocessing of metagenomic datasets Schmieder, R.; Edwards, R. Bioinformatics, Vol. 27, Issue 6 https://doi.org/10.1093/bioinformatics/btr026	journal	January 2011
Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes Kim, M.; Oh, H. -S.; Park, S. -C. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 64, Issue Pt 2 https://doi.org/10.1099/ijs.0.059774-0	journal	February 2014
Using MCL to Extract Clusters from Networks van Dongen, Stijn; Abreu-Goodger, Cei Bacterial Molecular Networks https://doi.org/10.1007/978-1-61779-361-5_15	book	October 2011
Next-Generation Beneficial Microbes: The Case of Akkermansia muciniphila Cani, Patrice D.; de Vos, Willem M. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01765	journal	September 2017
Microbiota-Produced Succinate Improves Glucose Homeostasis via Intestinal Gluconeogenesis De Vadder, Filipe; Kovatcheva-Datchary, Petia; Zitoun, Carine Cell Metabolism, Vol. 24, Issue 1 https://doi.org/10.1016/j.cmet.2016.06.013	journal	July 2016
Investigating Deep Phylogenetic Relationships among Cyanobacteria and Plastids by Small Subunit rRNA Sequence Analysis Turner, SeÁN; Pryer, Kathleen M.; Miao, Vivian P. W. The Journal of Eukaryotic Microbiology, Vol. 46, Issue 4 https://doi.org/10.1111/j.1550-7408.1999.tb04612.x	journal	July 1999
CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Thompson, Julie D.; Higgins, Desmond G.; Gibson, Toby J. Nucleic Acids Research, Vol. 22, Issue 22, p. 4673-4680 https://doi.org/10.1093/nar/22.22.4673	journal	January 1994
Detection of Succinate by Intestinal Tuft Cells Triggers a Type 2 Innate Immune Circuit Nadjsombati, Marija S.; McGinty, John W.; Lyons-Cohen, Miranda R. Immunity, Vol. 49, Issue 1 https://doi.org/10.1016/j.immuni.2018.06.016	journal	July 2018
Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants the Keio collection Baba, Tomoya; Ara, Takeshi; Hasegawa, Miki Molecular Systems Biology, Vol. 2, Article No. 2006.0008 https://doi.org/10.1038/msb4100050	journal	February 2006
Alterations in the Abundance and Co-occurrence of Akkermansia muciniphila and Faecalibacterium prausnitzii in the Colonic Mucosa of Inflammatory Bowel Disease Subjects Lopez-Siles, Mireia; Enrich-Capó, Núria; Aldeguer, Xavier Frontiers in Cellular and Infection Microbiology, Vol. 8 https://doi.org/10.3389/fcimb.2018.00281	journal	September 2018
Faecal levels of Bifidobacterium and Clostridium coccoides but not plasma lipopolysaccharide are inversely related to insulin and HOMA index in women F. S. Teixeira, T.; Grześkowiak, Łukasz M.; Salminen, Seppo Clinical Nutrition, Vol. 32, Issue 6 https://doi.org/10.1016/j.clnu.2013.02.008	journal	December 2013
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
From Dietary Fiber to Host Physiology: Short-Chain Fatty Acids as Key Bacterial Metabolites Koh, Ara; De Vadder, Filipe; Kovatcheva-Datchary, Petia Cell, Vol. 165, Issue 6 https://doi.org/10.1016/j.cell.2016.05.041	journal	June 2016
Reconstruction of regulatory and metabolic pathways in metal-reducing δ-proteobacteria Rodionov, Dmitry A.; Dubchak, Inna; Arkin, Adam Genome Biology, Vol. 5, Issue 11, p. R90 https://doi.org/10.1186/gb-2004-5-11-r90	journal	January 2004
Genomics and taxonomy in diagnostics for food security: soft-rotting enterobacterial plant pathogens Pritchard, Leighton; Glover, Rachel H.; Humphris, Sonia Analytical Methods, Vol. 8, Issue 1 https://doi.org/10.1039/C5AY02550H	journal	January 2016
Mucolytic Bacteria With Increased Prevalence in IBD Mucosa Augment In Vitro Utilization of Mucin by Other Bacteria Png, Chin Wen; Lindén, Sara K.; Gilshenan, Kristen S. American Journal of Gastroenterology, Vol. 105, Issue 11 https://doi.org/10.1038/ajg.2010.281	journal	January 2010
Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample Caporaso, J. G.; Lauber, C. L.; Walters, W. A. Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1 https://doi.org/10.1073/pnas.1000080107	journal	June 2010
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P. PLoS ONE, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pone.0009490	journal	March 2010
IMG: the integrated microbial genomes database and comparative analysis system Markowitz, V. M.; Chen, I. -M. A.; Palaniappan, K. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr1044	journal	December 2011
MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities Kang, Dongwan D.; Froula, Jeff; Egan, Rob PeerJ, Vol. 3 https://doi.org/10.7717/peerj.1165	journal	January 2015
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
Characterization and functional analysis of phytoene synthase gene family in tobacco Wang, Zhaojun; Zhang, Lin; Dong, Chen BMC Plant Biology, Vol. 21, Issue 1 https://doi.org/10.1186/s12870-020-02816-3	journal	January 2021
Uneven distribution of cobamide biosynthesis and dependence in bacteria predicted by comparative genomics Shelton, Amanda N.; Seth, Erica C.; Mok, Kenny C. The ISME Journal, Vol. 13, Issue 3 https://doi.org/10.1038/s41396-018-0304-9	journal	November 2018
Microbial Metabolic Networks at the Mucus Layer Lead to Diet-Independent Butyrate and Vitamin B ₁₂ Production by Intestinal Symbionts Belzer, Clara; Chia, Loo Wee; Aalvink, Steven mBio, Vol. 8, Issue 5 https://doi.org/10.1128/mBio.00770-17	journal	September 2017
Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: relationship with gut microbiome richness and ecology Dao, Maria Carlota; Everard, Amandine; Aron-Wisnewsky, Judith Gut, Vol. 65, Issue 3 https://doi.org/10.1136/gutjnl-2014-308778	journal	June 2015
Phylogenetic Analysis of Dysbiosis in Ulcerative Colitis During Remission Rajilić-Stojanović, Mirjana; Shanahan, Fergus; Guarner, Francisco Inflammatory Bowel Diseases, Vol. 19, Issue 3 https://doi.org/10.1097/MIB.0b013e31827fec6d	journal	January 2013
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T. Genome Research, Vol. 25, Issue 7 https://doi.org/10.1101/gr.186072.114	journal	May 2015
Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium Derrien, M. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 54, Issue 5 https://doi.org/10.1099/ijs.0.02873-0	journal	September 2004
Vitamin B 12 as a Modulator of Gut Microbial Ecology Degnan, Patrick H.; Taga, Michiko E.; Goodman, Andrew L. Cell Metabolism, Vol. 20, Issue 5 https://doi.org/10.1016/j.cmet.2014.10.002	journal	November 2014
Intestinal Integrity and Akkermansia muciniphila, a Mucin-Degrading Member of the Intestinal Microbiota Present in Infants, Adults, and the Elderly Collado, M. C.; Derrien, M.; Isolauri, E. Applied and Environmental Microbiology, Vol. 73, Issue 23 https://doi.org/10.1128/AEM.01477-07	journal	October 2007
UGA is an additional glycine codon in uncultured SR1 bacteria from the human microbiota Campbell, J. H.; O'Donoghue, P.; Campbell, A. G. Proceedings of the National Academy of Sciences, Vol. 110, Issue 14, p. 5540-5545 https://doi.org/10.1073/pnas.1303090110	journal	March 2013
Effect of Different Extraction Methods on Vitamin B12 from Blue Green Algae, Spirulina Platensis Kumudha, Anantharajappa Pharmaceutica Analytica Acta, Vol. 06, Issue 02 https://doi.org/10.4172/2153-2435.1000337	journal	January 2015
Dietary Habits of 2- to 9-Year-Old American Children Are Associated with Gut Microbiome Composition Herman, Dena R.; Rhoades, Nicholas; Mercado, Jasmine Journal of the Academy of Nutrition and Dietetics, Vol. 120, Issue 4 https://doi.org/10.1016/j.jand.2019.07.024	journal	April 2020
Pili-like proteins of Akkermansia muciniphila modulate host immune responses and gut barrier function Ottman, Noora; Reunanen, Justus; Meijerink, Marjolein PLOS ONE, Vol. 12, Issue 3 https://doi.org/10.1371/journal.pone.0173004	journal	March 2017
Temporal variability is a personalized feature of the human microbiome Flores, Gilberto E.; Caporaso, J. Gregory; Henley, Jessica B. Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0531-y	journal	December 2014
Moving pictures of the human microbiome Caporaso, J. Gregory; Lauber, Christian L.; Costello, Elizabeth K. Genome Biology, Vol. 12, Issue 5 https://doi.org/10.1186/gb-2011-12-5-r50	journal	January 2011
Expanded microbial genome coverage and improved protein family annotation in the COG database Galperin, Michael Y.; Makarova, Kira S.; Wolf, Yuri I. Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1223	journal	November 2014
The Genome of Akkermansia muciniphila, a Dedicated Intestinal Mucin Degrader, and Its Use in Exploring Intestinal Metagenomes van Passel, Mark W. J.; Kant, Ravi; Zoetendal, Erwin G. PLoS ONE, Vol. 6, Issue 3 https://doi.org/10.1371/journal.pone.0016876	journal	March 2011
Isolation and Characterization of an H2-Oxidizing Thermophilic Methanogen Ferguson, Thomas J.; Mah, Robert A. Applied and Environmental Microbiology, Vol. 45, Issue 1 https://doi.org/10.1128/AEM.45.1.265-274.1983	journal	January 1983
ARB: a software environment for sequence data Ludwig, W. Nucleic Acids Research, Vol. 32, Issue 4 https://doi.org/10.1093/nar/gkh293	journal	February 2004
Fast Identification and Removal of Sequence Contamination from Genomic and Metagenomic Datasets Schmieder, Robert; Edwards, Robert PLoS ONE, Vol. 6, Issue 3 https://doi.org/10.1371/journal.pone.0017288	journal	March 2011
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry Journal of Computational Biology, Vol. 19, Issue 5 https://doi.org/10.1089/cmb.2012.0021	journal	May 2012
The Microbiota of the Gut in Preschool Children With Normal and Excessive Body Weight Karlsson, Caroline L. J.; Önnerfält, Jenny; Xu, Jie Obesity, Vol. 20, Issue 11 https://doi.org/10.1038/oby.2012.110	journal	November 2012
Linking pangenomes and metagenomes: the Prochlorococcus metapangenome Delmont, Tom O.; Eren, A. Murat PeerJ, Vol. 6 https://doi.org/10.7717/peerj.4320	journal	January 2018
Tissue-specific transcriptomics and proteomics of a filarial nematode and its Wolbachia endosymbiont Luck, Ashley N.; Anderson, Kathryn G.; McClung, Colleen M. BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-015-2083-2	journal	November 2015
Adaptation of Akkermansia muciniphila to the Oxic-Anoxic Interface of the Mucus Layer Ouwerkerk, Janneke P.; van der Ark, Kees C. H.; Davids, Mark Applied and Environmental Microbiology, Vol. 82, Issue 23 https://doi.org/10.1128/AEM.01641-16	journal	September 2016
Effects of targeted delivery of propionate to the human colon on appetite regulation, body weight maintenance and adiposity in overweight adults Chambers, Edward S.; Viardot, Alexander; Psichas, Arianna Gut, Vol. 64, Issue 11 https://doi.org/10.1136/gutjnl-2014-307913	journal	December 2014
ITEP: An integrated toolkit for exploration of microbial pan-genomes Benedict, Matthew N.; Henriksen, James R.; Metcalf, William W. BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-8	journal	January 2014
Short-chain fatty acids in control of energy metabolism Hu, Jiamiao; Lin, Shaoling; Zheng, Baodong Critical Reviews in Food Science and Nutrition, Vol. 58, Issue 8 https://doi.org/10.1080/10408398.2016.1245650	journal	June 2017
MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro Molecular Biology and Evolution, Vol. 33, Issue 7 https://doi.org/10.1093/molbev/msw054	journal	March 2016
Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity Everard, A.; Belzer, C.; Geurts, L. Proceedings of the National Academy of Sciences, Vol. 110, Issue 22 https://doi.org/10.1073/pnas.1219451110	journal	May 2013
Cobalamin-Dependent Methionine Synthase Is a Modular Protein with Distinct Regions for Binding Homocysteine, Methyltetrahydrofolate, Cobalamin, and Adenosylmethionine ^† Goulding, Celia W.; Postigo, Dellma; Matthews, Rowena G. Biochemistry, Vol. 36, Issue 26 https://doi.org/10.1021/bi9705164	journal	July 1997
Human Gut Microbes Use Multiple Transporters to Distinguish Vitamin B12 Analogs and Compete in the Gut Degnan, Patrick H.; Barry, Natasha A.; Mok, Kenny C. Cell Host & Microbe, Vol. 15, Issue 1 https://doi.org/10.1016/j.chom.2013.12.007	journal	January 2014
Effects of short chain fatty acids on gut morphology and function. Scheppach, W. Gut, Vol. 35, Issue 1 Suppl https://doi.org/10.1136/gut.35.1_suppl.s35	journal	January 1994
Genome sequencing of 39 Akkermansia muciniphila isolates reveals its population structure, genomic and functional diverisity, and global distribution in mammalian gut microbiotas Guo, Xianfeng; Li, Shenghui; Zhang, Jiachun BMC Genomics, Vol. 18, Issue 1 https://doi.org/10.1186/s12864-017-4195-3	journal	October 2017
Deciphering the trophic interaction between Akkermansia muciniphila and the butyrogenic gut commensal Anaerostipes caccae using a metatranscriptomic approach Chia, Loo Wee; Hornung, Bastian V. H.; Aalvink, Steven Antonie van Leeuwenhoek, Vol. 111, Issue 6 https://doi.org/10.1007/s10482-018-1040-x	journal	February 2018
An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice Shin, Na-Ri; Lee, June-Chul; Lee, Hae-Youn Gut, Vol. 63, Issue 5 https://doi.org/10.1136/gutjnl-2012-303839	journal	June 2013
Identification and Characterization of a Novel FosA7 Member from Fosfomycin-Resistant Escherichia coli Clinical Isolates from Canadian Hospitals Milner, Kieran A.; Bay, Denice C.; Alexander, David Antimicrobial Agents and Chemotherapy, Vol. 65, Issue 1 https://doi.org/10.1128/aac.00865-20	journal	December 2020
The Microbial Genomes Atlas (MiGA) webserver: taxonomic and gene diversity analysis of Archaea and Bacteria at the whole genome level Rodriguez-R, Luis M.; Gunturu, Santosh; Harvey, William T. Nucleic Acids Research, Vol. 46, Issue W1 https://doi.org/10.1093/nar/gky467	journal	June 2018
Library construction for next-generation sequencing: Overviews and challenges Head, Steven R.; Komori, H. Kiyomi; LaMere, Sarah A. BioTechniques, Vol. 56, Issue 2 https://doi.org/10.2144/000114133	journal	February 2014
IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes Chen, I-Min A.; Chu, Ken; Palaniappan, Krishna Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky901	journal	October 2018
Akkermansia muciniphila in the Human Gastrointestinal Tract: When, Where, and How? Geerlings, Sharon; Kostopoulos, Ioannis; de Vos, Willem Microorganisms, Vol. 6, Issue 3 https://doi.org/10.3390/microorganisms6030075	journal	July 2018
Genome-Scale Model and Omics Analysis of Metabolic Capacities of Akkermansia muciniphila Reveal a Preferential Mucin-Degrading Lifestyle Ottman, Noora; Davids, Mark; Suarez-Diez, Maria Applied and Environmental Microbiology, Vol. 83, Issue 18 https://doi.org/10.1128/AEM.01014-17	journal	July 2017
Current IUBMB recommendations on enzyme nomenclature and kinetics Cornish-Bowden, Athel Perspectives in Science, Vol. 1, Issue 1-6 https://doi.org/10.1016/j.pisc.2014.02.006	journal	May 2014
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
Microbes inside—from diversity to function: the case of Akkermansia Belzer, Clara; de Vos, Willem M. The ISME Journal, Vol. 6, Issue 8 https://doi.org/10.1038/ismej.2012.6	journal	March 2012
A next-generation beneficial microbe: Akkermansia muciniphila Naito, Yuji; Uchiyama, Kazuhiko; Takagi, Tomohisa Journal of Clinical Biochemistry and Nutrition, Vol. 63, Issue 1 https://doi.org/10.3164/jcbn.18-57	journal	January 2018
Changes in Gut Microbiota Composition after Bariatric Surgery: a New Balance to Decode Palmisano, Silvia; Campisciano, Giuseppina; Silvestri, Marta Journal of Gastrointestinal Surgery, Vol. 24, Issue 8 https://doi.org/10.1007/s11605-019-04321-x	journal	August 2019
Dark chocolate as a stable carrier of microencapsulated Akkermansia muciniphila and Lactobacillus casei . Marcial-Coba, Martín Sebastián; Saaby, Lasse; Knøchel, Susanne FEMS Microbiology Letters, Vol. 366, Issue 2 https://doi.org/10.1093/femsle/fny290	journal	December 2018
Characterization of Outer Membrane Proteome of Akkermansia muciniphila Reveals Sets of Novel Proteins Exposed to the Human Intestine Ottman, Noora; Huuskonen, Laura; Reunanen, Justus Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01157	journal	July 2016
A purified membrane protein from Akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice Plovier, Hubert; Everard, Amandine; Druart, Céline Nature Medicine, Vol. 23, Issue 1 https://doi.org/10.1038/nm.4236	journal	November 2016
Akkermansia glycaniphila sp. nov., an anaerobic mucin-degrading bacterium isolated from reticulated python faeces Ouwerkerk, Janneke P.; Aalvink, Steven; Belzer, Clara International Journal of Systematic and Evolutionary Microbiology, Vol. 66, Issue 11 https://doi.org/10.1099/ijsem.0.001399	journal	November 2016
Alcohol pretreatment of stools effect on culturomics Afouda, Pamela; Hocquart, Marie; Pham, Thi-Phuong-Thao Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-62068-x	journal	March 2020
Akkermansia muciniphila and its role in regulating host functions Derrien, Muriel; Belzer, Clara; de Vos, Willem M. Microbial Pathogenesis, Vol. 106 https://doi.org/10.1016/j.micpath.2016.02.005	journal	May 2017
Cohabiting family members share microbiota with one another and with their dogs Song, Se Jin; Lauber, Christian; Costello, Elizabeth K. eLife, Vol. 2 https://doi.org/10.7554/eLife.00458	journal	April 2013
Purification and Properties of 5-Methyltetrahydropteroyltriglutamate-Homocysteine Transmethylase Whitfield, Carolyn D.; Steers, Edward J.; Weissbach, Herbert Journal of Biological Chemistry, Vol. 245, Issue 2 https://doi.org/10.1016/S0021-9258(18)63404-0	journal	January 1970
Cloning and Sequence Analysis of the Escherichia coli metH Gene Encoding Cobalamin-dependent Methionine Synthase and Isolation of a Tryptic Fragment Containing the Cobalamin-binding Domain Banerjee, R. V.; Johnston, N. L.; Sobeski, J. K. Journal of Biological Chemistry, Vol. 264, Issue 23 https://doi.org/10.1016/S0021-9258(18)80083-7	journal	August 1989
Dark chocolate as a stable carrier of microencapsulated Akkermansia muciniphila and Lactobacillus casei Marcial-Coba, Martín Sebastián; Saaby, Lasse; Knøchel, Susanne FEMS Microbiology Letters, Vol. 366, Issue Supplement_1 https://doi.org/10.1093/femsle/fny290s	journal	December 2018
Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes Kim, M.; Oh, H. -S.; Park, S. -C. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 64, Issue Pt 5 https://doi.org/10.1099/ijs.0.064931-0	journal	May 2014

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Title: Comparative Genomics Guides Elucidation of Vitamin B12 Biosynthesis in Novel Human-Associated Akkermansia Strains

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Title: Comparative Genomics Guides Elucidation of Vitamin B₁₂ Biosynthesis in Novel Human-Associated Akkermansia Strains