Comparative Genomics Guides Elucidation of Vitamin B12 Biosynthesis in Novel Human-Associated Akkermansia Strains
Abstract
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 vitaminmore »
- Authors:
-
- 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)
- Publication Date:
- Research Org.:
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1606768
- Grant/Contract Number:
- AC05-00OR22725
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Applied and Environmental Microbiology
- Additional Journal Information:
- Journal Volume: 86; Journal Issue: 3; Journal ID: ISSN 0099-2240
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Akkermansia; human gut microbiome; intestinal bacteria; probiotics; vitamin B12
Citation Formats
Kirmiz, Nina, Galindo, Kadir, Cross, Karissa L., Luna, Estefani, Rhodes, Nicholas, Podar, Mircea, and Flores, Gilberto E. Comparative Genomics Guides Elucidation of Vitamin B12 Biosynthesis in Novel Human-Associated Akkermansia Strains. United States: N. p., 2019.
Web. doi:10.1128/AEM.02117-19.
Kirmiz, Nina, Galindo, Kadir, Cross, Karissa L., Luna, Estefani, Rhodes, Nicholas, Podar, Mircea, & Flores, Gilberto E. Comparative Genomics Guides Elucidation of Vitamin B12 Biosynthesis in Novel Human-Associated Akkermansia Strains. United States. https://doi.org/10.1128/AEM.02117-19
Kirmiz, Nina, Galindo, Kadir, Cross, Karissa L., Luna, Estefani, Rhodes, Nicholas, Podar, Mircea, and Flores, Gilberto E. Fri .
"Comparative Genomics Guides Elucidation of Vitamin B12 Biosynthesis in Novel Human-Associated Akkermansia Strains". United States. https://doi.org/10.1128/AEM.02117-19. https://www.osti.gov/servlets/purl/1606768.
@article{osti_1606768,
title = {Comparative Genomics Guides Elucidation of Vitamin B12 Biosynthesis in Novel Human-Associated Akkermansia Strains},
author = {Kirmiz, Nina and Galindo, Kadir and Cross, Karissa L. and Luna, Estefani and Rhodes, Nicholas and Podar, Mircea and Flores, Gilberto E.},
abstractNote = {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.},
doi = {10.1128/AEM.02117-19},
journal = {Applied and Environmental Microbiology},
number = 3,
volume = 86,
place = {United States},
year = {2019},
month = {11}
}
Web of Science
Works referenced in this record:
Anvi’o: an advanced analysis and visualization platform for ‘omics data
journal, January 2015
- Eren, A. Murat; Esen, Özcan C.; Quince, Christopher
- PeerJ, Vol. 3
The Mucin Degrader Akkermansia muciniphila Is an Abundant Resident of the Human Intestinal Tract
journal, December 2007
- Derrien, M.; Collado, M. C.; Ben-Amor, K.
- Applied and Environmental Microbiology, Vol. 74, Issue 5
Akkermansia muciniphila induces gut microbiota remodelling and controls islet autoimmunity in NOD mice
journal, December 2017
- Hänninen, Arno; Toivonen, Raine; Pöysti, Sakari
- Gut, Vol. 67, Issue 8
An SHR–SCR module specifies legume cortical cell fate to enable nodulation
journal, December 2020
- Dong, Wentao; Zhu, Yayun; Chang, Huizhong
- Nature, Vol. 589, Issue 7843
Bacterial Community Variation in Human Body Habitats Across Space and Time
journal, November 2009
- Costello, E. K.; Lauber, C. L.; Hamady, M.
- Science, Vol. 326, Issue 5960
Shifting the genomic gold standard for the prokaryotic species definition
journal, October 2009
- Richter, Michael; Rosselló-Móra, Ramon
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 45
Quality control and preprocessing of metagenomic datasets
journal, January 2011
- Schmieder, R.; Edwards, R.
- Bioinformatics, Vol. 27, Issue 6
Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes
journal, February 2014
- Kim, M.; Oh, H. -S.; Park, S. -C.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 64, Issue Pt 2
Next-Generation Beneficial Microbes: The Case of Akkermansia muciniphila
journal, September 2017
- Cani, Patrice D.; de Vos, Willem M.
- Frontiers in Microbiology, Vol. 8
Microbiota-Produced Succinate Improves Glucose Homeostasis via Intestinal Gluconeogenesis
journal, July 2016
- De Vadder, Filipe; Kovatcheva-Datchary, Petia; Zitoun, Carine
- Cell Metabolism, Vol. 24, Issue 1
Investigating Deep Phylogenetic Relationships among Cyanobacteria and Plastids by Small Subunit rRNA Sequence Analysis
journal, July 1999
- Turner, SeÁN; Pryer, Kathleen M.; Miao, Vivian P. W.
- The Journal of Eukaryotic Microbiology, Vol. 46, Issue 4
CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice
journal, January 1994
- Thompson, Julie D.; Higgins, Desmond G.; Gibson, Toby J.
- Nucleic Acids Research, Vol. 22, Issue 22, p. 4673-4680
Detection of Succinate by Intestinal Tuft Cells Triggers a Type 2 Innate Immune Circuit
journal, July 2018
- Nadjsombati, Marija S.; McGinty, John W.; Lyons-Cohen, Miranda R.
- Immunity, Vol. 49, Issue 1
Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants the Keio collection
journal, February 2006
- Baba, Tomoya; Ara, Takeshi; Hasegawa, Miki
- Molecular Systems Biology, Vol. 2, Article No. 2006.0008
Alterations in the Abundance and Co-occurrence of Akkermansia muciniphila and Faecalibacterium prausnitzii in the Colonic Mucosa of Inflammatory Bowel Disease Subjects
journal, September 2018
- Lopez-Siles, Mireia; Enrich-Capó, Núria; Aldeguer, Xavier
- Frontiers in Cellular and Infection Microbiology, Vol. 8
Faecal levels of Bifidobacterium and Clostridium coccoides but not plasma lipopolysaccharide are inversely related to insulin and HOMA index in women
journal, December 2013
- F. S. Teixeira, T.; Grześkowiak, Łukasz M.; Salminen, Seppo
- Clinical Nutrition, Vol. 32, Issue 6
Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014
- Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern
- Bioinformatics, Vol. 30, Issue 15
From Dietary Fiber to Host Physiology: Short-Chain Fatty Acids as Key Bacterial Metabolites
journal, June 2016
- Koh, Ara; De Vadder, Filipe; Kovatcheva-Datchary, Petia
- Cell, Vol. 165, Issue 6
Genomics and taxonomy in diagnostics for food security: soft-rotting enterobacterial plant pathogens
journal, January 2016
- Pritchard, Leighton; Glover, Rachel H.; Humphris, Sonia
- Analytical Methods, Vol. 8, Issue 1
Mucolytic Bacteria With Increased Prevalence in IBD Mucosa Augment In Vitro Utilization of Mucin by Other Bacteria
journal, January 2010
- Png, Chin Wen; Lindén, Sara K.; Gilshenan, Kristen S.
- American Journal of Gastroenterology, Vol. 105, Issue 11
Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample
journal, June 2010
- Caporaso, J. G.; Lauber, C. L.; Walters, W. A.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010
- Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P.
- PLoS ONE, Vol. 5, Issue 3
IMG: the integrated microbial genomes database and comparative analysis system
journal, December 2011
- Markowitz, V. M.; Chen, I. -M. A.; Palaniappan, K.
- Nucleic Acids Research, Vol. 40, Issue D1
MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities
journal, January 2015
- Kang, Dongwan D.; Froula, Jeff; Egan, Rob
- PeerJ, Vol. 3
Prodigal: prokaryotic gene recognition and translation initiation site identification
journal, March 2010
- Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F.
- BMC Bioinformatics, Vol. 11, Issue 1
Characterization and functional analysis of phytoene synthase gene family in tobacco
journal, January 2021
- Wang, Zhaojun; Zhang, Lin; Dong, Chen
- BMC Plant Biology, Vol. 21, Issue 1
Uneven distribution of cobamide biosynthesis and dependence in bacteria predicted by comparative genomics
journal, November 2018
- Shelton, Amanda N.; Seth, Erica C.; Mok, Kenny C.
- The ISME Journal, Vol. 13, Issue 3
Microbial Metabolic Networks at the Mucus Layer Lead to Diet-Independent Butyrate and Vitamin B 12 Production by Intestinal Symbionts
journal, September 2017
- Belzer, Clara; Chia, Loo Wee; Aalvink, Steven
- mBio, Vol. 8, Issue 5
Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: relationship with gut microbiome richness and ecology
journal, June 2015
- Dao, Maria Carlota; Everard, Amandine; Aron-Wisnewsky, Judith
- Gut, Vol. 65, Issue 3
Phylogenetic Analysis of Dysbiosis in Ulcerative Colitis During Remission
journal, January 2013
- Rajilić-Stojanović, Mirjana; Shanahan, Fergus; Guarner, Francisco
- Inflammatory Bowel Diseases, Vol. 19, Issue 3
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes
journal, May 2015
- Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T.
- Genome Research, Vol. 25, Issue 7
Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium
journal, September 2004
- Derrien, M.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 54, Issue 5
Vitamin B 12 as a Modulator of Gut Microbial Ecology
journal, November 2014
- Degnan, Patrick H.; Taga, Michiko E.; Goodman, Andrew L.
- Cell Metabolism, Vol. 20, Issue 5
Intestinal Integrity and Akkermansia muciniphila, a Mucin-Degrading Member of the Intestinal Microbiota Present in Infants, Adults, and the Elderly
journal, October 2007
- Collado, M. C.; Derrien, M.; Isolauri, E.
- Applied and Environmental Microbiology, Vol. 73, Issue 23
UGA is an additional glycine codon in uncultured SR1 bacteria from the human microbiota
journal, March 2013
- Campbell, J. H.; O'Donoghue, P.; Campbell, A. G.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 14, p. 5540-5545
Effect of Different Extraction Methods on Vitamin B12 from Blue Green Algae, Spirulina Platensis
journal, January 2015
- Kumudha, Anantharajappa
- Pharmaceutica Analytica Acta, Vol. 06, Issue 02
Dietary Habits of 2- to 9-Year-Old American Children Are Associated with Gut Microbiome Composition
journal, April 2020
- Herman, Dena R.; Rhoades, Nicholas; Mercado, Jasmine
- Journal of the Academy of Nutrition and Dietetics, Vol. 120, Issue 4
Pili-like proteins of Akkermansia muciniphila modulate host immune responses and gut barrier function
journal, March 2017
- Ottman, Noora; Reunanen, Justus; Meijerink, Marjolein
- PLOS ONE, Vol. 12, Issue 3
Temporal variability is a personalized feature of the human microbiome
journal, December 2014
- Flores, Gilberto E.; Caporaso, J. Gregory; Henley, Jessica B.
- Genome Biology, Vol. 15, Issue 12
Moving pictures of the human microbiome
journal, January 2011
- Caporaso, J. Gregory; Lauber, Christian L.; Costello, Elizabeth K.
- Genome Biology, Vol. 12, Issue 5
Expanded microbial genome coverage and improved protein family annotation in the COG database
journal, November 2014
- Galperin, Michael Y.; Makarova, Kira S.; Wolf, Yuri I.
- Nucleic Acids Research, Vol. 43, Issue D1
The Genome of Akkermansia muciniphila, a Dedicated Intestinal Mucin Degrader, and Its Use in Exploring Intestinal Metagenomes
journal, March 2011
- van Passel, Mark W. J.; Kant, Ravi; Zoetendal, Erwin G.
- PLoS ONE, Vol. 6, Issue 3
Isolation and Characterization of an H2-Oxidizing Thermophilic Methanogen
journal, January 1983
- Ferguson, Thomas J.; Mah, Robert A.
- Applied and Environmental Microbiology, Vol. 45, Issue 1
ARB: a software environment for sequence data
journal, February 2004
- Ludwig, W.
- Nucleic Acids Research, Vol. 32, Issue 4
Fast Identification and Removal of Sequence Contamination from Genomic and Metagenomic Datasets
journal, March 2011
- Schmieder, Robert; Edwards, Robert
- PLoS ONE, Vol. 6, Issue 3
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing
journal, May 2012
- Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry
- Journal of Computational Biology, Vol. 19, Issue 5
The Microbiota of the Gut in Preschool Children With Normal and Excessive Body Weight
journal, November 2012
- Karlsson, Caroline L. J.; Önnerfält, Jenny; Xu, Jie
- Obesity, Vol. 20, Issue 11
Linking pangenomes and metagenomes: the Prochlorococcus metapangenome
journal, January 2018
- Delmont, Tom O.; Eren, A. Murat
- PeerJ, Vol. 6
Tissue-specific transcriptomics and proteomics of a filarial nematode and its Wolbachia endosymbiont
journal, November 2015
- Luck, Ashley N.; Anderson, Kathryn G.; McClung, Colleen M.
- BMC Genomics, Vol. 16, Issue 1
Adaptation of Akkermansia muciniphila to the Oxic-Anoxic Interface of the Mucus Layer
journal, September 2016
- Ouwerkerk, Janneke P.; van der Ark, Kees C. H.; Davids, Mark
- Applied and Environmental Microbiology, Vol. 82, Issue 23
Effects of targeted delivery of propionate to the human colon on appetite regulation, body weight maintenance and adiposity in overweight adults
journal, December 2014
- Chambers, Edward S.; Viardot, Alexander; Psichas, Arianna
- Gut, Vol. 64, Issue 11
ITEP: An integrated toolkit for exploration of microbial pan-genomes
journal, January 2014
- Benedict, Matthew N.; Henriksen, James R.; Metcalf, William W.
- BMC Genomics, Vol. 15, Issue 1
Short-chain fatty acids in control of energy metabolism
journal, June 2017
- Hu, Jiamiao; Lin, Shaoling; Zheng, Baodong
- Critical Reviews in Food Science and Nutrition, Vol. 58, Issue 8
MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets
journal, March 2016
- Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro
- Molecular Biology and Evolution, Vol. 33, Issue 7
Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity
journal, May 2013
- Everard, A.; Belzer, C.; Geurts, L.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 22
Cobalamin-Dependent Methionine Synthase Is a Modular Protein with Distinct Regions for Binding Homocysteine, Methyltetrahydrofolate, Cobalamin, and Adenosylmethionine †
journal, July 1997
- Goulding, Celia W.; Postigo, Dellma; Matthews, Rowena G.
- Biochemistry, Vol. 36, Issue 26
Human Gut Microbes Use Multiple Transporters to Distinguish Vitamin B12 Analogs and Compete in the Gut
journal, January 2014
- Degnan, Patrick H.; Barry, Natasha A.; Mok, Kenny C.
- Cell Host & Microbe, Vol. 15, Issue 1
Effects of short chain fatty acids on gut morphology and function.
journal, January 1994
- Scheppach, W.
- Gut, Vol. 35, Issue 1 Suppl
Genome sequencing of 39 Akkermansia muciniphila isolates reveals its population structure, genomic and functional diverisity, and global distribution in mammalian gut microbiotas
journal, October 2017
- Guo, Xianfeng; Li, Shenghui; Zhang, Jiachun
- BMC Genomics, Vol. 18, Issue 1
Deciphering the trophic interaction between Akkermansia muciniphila and the butyrogenic gut commensal Anaerostipes caccae using a metatranscriptomic approach
journal, February 2018
- Chia, Loo Wee; Hornung, Bastian V. H.; Aalvink, Steven
- Antonie van Leeuwenhoek, Vol. 111, Issue 6
An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice
journal, June 2013
- Shin, Na-Ri; Lee, June-Chul; Lee, Hae-Youn
- Gut, Vol. 63, Issue 5
Identification and Characterization of a Novel FosA7 Member from Fosfomycin-Resistant Escherichia coli Clinical Isolates from Canadian Hospitals
journal, December 2020
- Milner, Kieran A.; Bay, Denice C.; Alexander, David
- Antimicrobial Agents and Chemotherapy, Vol. 65, Issue 1
The Microbial Genomes Atlas (MiGA) webserver: taxonomic and gene diversity analysis of Archaea and Bacteria at the whole genome level
journal, June 2018
- Rodriguez-R, Luis M.; Gunturu, Santosh; Harvey, William T.
- Nucleic Acids Research, Vol. 46, Issue W1
Library construction for next-generation sequencing: Overviews and challenges
journal, February 2014
- Head, Steven R.; Komori, H. Kiyomi; LaMere, Sarah A.
- BioTechniques, Vol. 56, Issue 2
IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes
journal, October 2018
- Chen, I-Min A.; Chu, Ken; Palaniappan, Krishna
- Nucleic Acids Research, Vol. 47, Issue D1
Akkermansia muciniphila in the Human Gastrointestinal Tract: When, Where, and How?
journal, July 2018
- Geerlings, Sharon; Kostopoulos, Ioannis; de Vos, Willem
- Microorganisms, Vol. 6, Issue 3
Genome-Scale Model and Omics Analysis of Metabolic Capacities of Akkermansia muciniphila Reveal a Preferential Mucin-Degrading Lifestyle
journal, July 2017
- Ottman, Noora; Davids, Mark; Suarez-Diez, Maria
- Applied and Environmental Microbiology, Vol. 83, Issue 18
Current IUBMB recommendations on enzyme nomenclature and kinetics
journal, May 2014
- Cornish-Bowden, Athel
- Perspectives in Science, Vol. 1, Issue 1-6
MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004
- Edgar, R. C.
- Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
Microbes inside—from diversity to function: the case of Akkermansia
journal, March 2012
- Belzer, Clara; de Vos, Willem M.
- The ISME Journal, Vol. 6, Issue 8
A next-generation beneficial microbe: Akkermansia muciniphila
journal, January 2018
- Naito, Yuji; Uchiyama, Kazuhiko; Takagi, Tomohisa
- Journal of Clinical Biochemistry and Nutrition, Vol. 63, Issue 1
Changes in Gut Microbiota Composition after Bariatric Surgery: a New Balance to Decode
journal, August 2019
- Palmisano, Silvia; Campisciano, Giuseppina; Silvestri, Marta
- Journal of Gastrointestinal Surgery, Vol. 24, Issue 8
Dark chocolate as a stable carrier of microencapsulated Akkermansia muciniphila and Lactobacillus casei .
journal, December 2018
- Marcial-Coba, Martín Sebastián; Saaby, Lasse; Knøchel, Susanne
- FEMS Microbiology Letters, Vol. 366, Issue 2
Characterization of Outer Membrane Proteome of Akkermansia muciniphila Reveals Sets of Novel Proteins Exposed to the Human Intestine
journal, July 2016
- Ottman, Noora; Huuskonen, Laura; Reunanen, Justus
- Frontiers in Microbiology, Vol. 7
A purified membrane protein from Akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice
journal, November 2016
- Plovier, Hubert; Everard, Amandine; Druart, Céline
- Nature Medicine, Vol. 23, Issue 1
Akkermansia glycaniphila sp. nov., an anaerobic mucin-degrading bacterium isolated from reticulated python faeces
journal, November 2016
- Ouwerkerk, Janneke P.; Aalvink, Steven; Belzer, Clara
- International Journal of Systematic and Evolutionary Microbiology, Vol. 66, Issue 11
Alcohol pretreatment of stools effect on culturomics
journal, March 2020
- Afouda, Pamela; Hocquart, Marie; Pham, Thi-Phuong-Thao
- Scientific Reports, Vol. 10, Issue 1
Akkermansia muciniphila and its role in regulating host functions
journal, May 2017
- Derrien, Muriel; Belzer, Clara; de Vos, Willem M.
- Microbial Pathogenesis, Vol. 106
Cohabiting family members share microbiota with one another and with their dogs
journal, April 2013
- Song, Se Jin; Lauber, Christian; Costello, Elizabeth K.
- eLife, Vol. 2
Purification and Properties of 5-Methyltetrahydropteroyltriglutamate-Homocysteine Transmethylase
journal, January 1970
- Whitfield, Carolyn D.; Steers, Edward J.; Weissbach, Herbert
- Journal of Biological Chemistry, Vol. 245, Issue 2
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
journal, August 1989
- Banerjee, R. V.; Johnston, N. L.; Sobeski, J. K.
- Journal of Biological Chemistry, Vol. 264, Issue 23
Dark chocolate as a stable carrier of microencapsulated Akkermansia muciniphila and Lactobacillus casei
journal, December 2018
- Marcial-Coba, Martín Sebastián; Saaby, Lasse; Knøchel, Susanne
- FEMS Microbiology Letters, Vol. 366, Issue Supplement_1
Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes
journal, May 2014
- Kim, M.; Oh, H. -S.; Park, S. -C.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 64, Issue Pt 5