Microbial Metabolism Shifts Towards an Adverse Profile with Supplementary Iron in the TIM-2 In vitro Model of the Human Colon
Abstract
Oral iron administration in African children can increase the risk for infections. However, it remains unclear to what extent supplementary iron affects the intestinal microbiome. We here explored the impact of iron preparations on microbial growth and metabolism in the well-controlled TNO's in vitro model of the large intestine (TIM-2). The model was inoculated with a human microbiota, without supplementary iron, or with 50 or 250 μmol/L ferrous sulfate, 50 or 250 μmol/L ferric citrate, or 50 μmol/L hemin. High resolution responses of the microbiota were examined by 16S rDNA pyrosequencing, microarray analysis, and metagenomic sequencing. The metabolome was assessed by fatty acid quantification, gas chromatography-mass spectrometry (GC-MS), and 1H-NMR spectroscopy. Cultured intestinal epithelial Caco-2 cells were used to assess fecal water toxicity. Microbiome analysis showed, among others, that supplementary iron induced decreased levels of Bifidobacteriaceae and Lactobacillaceae, while it caused higher levels of Roseburia and Prevotella. Metagenomic analyses showed an enrichment of microbial motility-chemotaxis systems, while the metabolome markedly changed from a saccharolytic to a proteolytic profile in response to iron. Branched chain fatty acids and ammonia levels increased significantly, in particular with ferrous sulfate. Importantly, the metabolite-containing effluent from iron-rich conditions showed increased cytotoxicity to Caco-2 cells. Inmore »
- Authors:
-
- Radboud Univ., Nijmegen (Netherlands)
- Radboud Univ., Nijmegen (Netherlands); Univ. of Utrecht (Netherlands); Federal Univ. of Rio de Janeiro (Brazil)
- TNO Innovation for Life, Zeist (Netherlands)
- NIZO food research, Kernhemseweg Ede (Netherlands)
- Argonne National Lab. (ANL), Argonne, IL (United States); Univ. of Chicago, Lemont, IL (United States)
- Illumina Inc., Little Chesterford (United Kingdom); DNA digest, Future Business Centre, Cambridge (United Kingdom)
- Illumina Inc., Little Chesterford (United Kingdom)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1258646
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Microbiology
- Additional Journal Information:
- Journal Volume: 6; Journal ID: ISSN 1664-302X
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 60 APPLIED LIFE SCIENCES; in vitro fermentation; iron supplementation; gutmicrobiome; metabolome; metagenome; toxicity; SCFA; BCFA
Citation Formats
Kortman, Guus A. M., Dutilh, Bas E., Maathuis, Annet J. H., Engelke, Udo F., Boekhorst, Jos, Keegan, Kevin P., Nielsen, Fiona G. G., Betley, Jason, Weir, Jacqueline C., Kingsbury, Zoya, Kluijtmans, Leo A. J., Swinkels, Dorine W., Venema, Koen, and Tjalsma, Harold. Microbial Metabolism Shifts Towards an Adverse Profile with Supplementary Iron in the TIM-2 In vitro Model of the Human Colon. United States: N. p., 2016.
Web. doi:10.3389/fmicb.2015.01481.
Kortman, Guus A. M., Dutilh, Bas E., Maathuis, Annet J. H., Engelke, Udo F., Boekhorst, Jos, Keegan, Kevin P., Nielsen, Fiona G. G., Betley, Jason, Weir, Jacqueline C., Kingsbury, Zoya, Kluijtmans, Leo A. J., Swinkels, Dorine W., Venema, Koen, & Tjalsma, Harold. Microbial Metabolism Shifts Towards an Adverse Profile with Supplementary Iron in the TIM-2 In vitro Model of the Human Colon. United States. https://doi.org/10.3389/fmicb.2015.01481
Kortman, Guus A. M., Dutilh, Bas E., Maathuis, Annet J. H., Engelke, Udo F., Boekhorst, Jos, Keegan, Kevin P., Nielsen, Fiona G. G., Betley, Jason, Weir, Jacqueline C., Kingsbury, Zoya, Kluijtmans, Leo A. J., Swinkels, Dorine W., Venema, Koen, and Tjalsma, Harold. Wed .
"Microbial Metabolism Shifts Towards an Adverse Profile with Supplementary Iron in the TIM-2 In vitro Model of the Human Colon". United States. https://doi.org/10.3389/fmicb.2015.01481. https://www.osti.gov/servlets/purl/1258646.
@article{osti_1258646,
title = {Microbial Metabolism Shifts Towards an Adverse Profile with Supplementary Iron in the TIM-2 In vitro Model of the Human Colon},
author = {Kortman, Guus A. M. and Dutilh, Bas E. and Maathuis, Annet J. H. and Engelke, Udo F. and Boekhorst, Jos and Keegan, Kevin P. and Nielsen, Fiona G. G. and Betley, Jason and Weir, Jacqueline C. and Kingsbury, Zoya and Kluijtmans, Leo A. J. and Swinkels, Dorine W. and Venema, Koen and Tjalsma, Harold},
abstractNote = {Oral iron administration in African children can increase the risk for infections. However, it remains unclear to what extent supplementary iron affects the intestinal microbiome. We here explored the impact of iron preparations on microbial growth and metabolism in the well-controlled TNO's in vitro model of the large intestine (TIM-2). The model was inoculated with a human microbiota, without supplementary iron, or with 50 or 250 μmol/L ferrous sulfate, 50 or 250 μmol/L ferric citrate, or 50 μmol/L hemin. High resolution responses of the microbiota were examined by 16S rDNA pyrosequencing, microarray analysis, and metagenomic sequencing. The metabolome was assessed by fatty acid quantification, gas chromatography-mass spectrometry (GC-MS), and 1H-NMR spectroscopy. Cultured intestinal epithelial Caco-2 cells were used to assess fecal water toxicity. Microbiome analysis showed, among others, that supplementary iron induced decreased levels of Bifidobacteriaceae and Lactobacillaceae, while it caused higher levels of Roseburia and Prevotella. Metagenomic analyses showed an enrichment of microbial motility-chemotaxis systems, while the metabolome markedly changed from a saccharolytic to a proteolytic profile in response to iron. Branched chain fatty acids and ammonia levels increased significantly, in particular with ferrous sulfate. Importantly, the metabolite-containing effluent from iron-rich conditions showed increased cytotoxicity to Caco-2 cells. In conclusion, our explorations indicate that in the absence of host influences, iron induces a more hostile environment characterized by a reduction of microbes that are generally beneficial, and increased levels of bacterial metabolites that can impair the barrier function of a cultured intestinal epithelial monolayer.},
doi = {10.3389/fmicb.2015.01481},
journal = {Frontiers in Microbiology},
number = ,
volume = 6,
place = {United States},
year = {Wed Jan 06 00:00:00 EST 2016},
month = {Wed Jan 06 00:00:00 EST 2016}
}
Web of Science
Works referenced in this record:
A computer-controlled system to simulate conditions of the large intestine with peristaltic mixing, water absorption and absorption of fermentation products
journal, December 1999
- Minekus, M.; Smeets-Peeters, M.; Bernalier, A.
- Applied Microbiology and Biotechnology, Vol. 53, Issue 1
Acetogenesis and the Wood–Ljungdahl pathway of CO2 fixation
journal, December 2008
- Ragsdale, Stephen W.; Pierce, Elizabeth
- Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1784, Issue 12, p. 1873-1898
Gastrointestinal effects of single and repeated doses of ferrous sulphate in rats
journal, January 1993
- Benoni, G.; Cuzzolin, L.; Zambreri, D.
- Pharmacological Research, Vol. 27, Issue 1
Advances and perspectives in in vitro human gut fermentation modeling
journal, January 2012
- Payne, Amanda N.; Zihler, Annina; Chassard, Christophe
- Trends in Biotechnology, Vol. 30, Issue 1
Iron Availability Increases the Pathogenic Potential of Salmonella Typhimurium and Other Enteric Pathogens at the Intestinal Epithelial Interface
journal, January 2012
- Kortman, Guus A. M.; Boleij, Annemarie; Swinkels, Dorine W.
- PLoS ONE, Vol. 7, Issue 1
Effects of Different Complementary Feeding Regimens on Iron Status and Enteric Microbiota in Breastfed Infants
journal, August 2013
- Krebs, Nancy F.; Sherlock, Laurie G.; Westcott, Jamie
- The Journal of Pediatrics, Vol. 163, Issue 2
Depletion of luminal iron alters the gut microbiota and prevents Crohn's disease-like ileitis
journal, November 2010
- Werner, T.; Wagner, S. J.; Martinez, I.
- Gut, Vol. 60, Issue 3
Bacteria, Colonic Fermentation, and Gastrointestinal Health
journal, January 2012
- Macfarlane, George T.; Macfarlane, Sandra
- Journal of AOAC International, Vol. 95, Issue 1
Low iron availability in continuous in vitro colonic fermentations induces strong dysbiosis of the child gut microbial consortium and a decrease in main metabolites
journal, August 2012
- Dostal, Alexandra; Fehlbaum, Sophie; Chassard, Christophe
- FEMS Microbiology Ecology, Vol. 83, Issue 1
A human gut microbial gene catalogue established by metagenomic sequencing
journal, March 2010
- Qin, Junjie; Li, Ruiqiang; Raes, Jeroen
- Nature, Vol. 464, Issue 7285
Effect of iron supplementation on incidence of infectious illness in children: systematic review
journal, November 2002
- Gera, T.
- BMJ, Vol. 325, Issue 7373
Experimental models of the gut microbiome
journal, February 2013
- Venema, Koen; van den Abbeele, Pieter
- Best Practice & Research Clinical Gastroenterology, Vol. 27, Issue 1
Function of the microbiota
journal, February 2013
- Rajilić-Stojanović, Mirjana
- Best Practice & Research Clinical Gastroenterology, Vol. 27, Issue 1
Evaluating the microbial diversity of an in vitro model of the human large intestine by phylogenetic microarray analysis
journal, November 2010
- Rajilić-Stojanović, Mirjana; Maathuis, Annet; Heilig, Hans G. H. J.
- Microbiology, Vol. 156, Issue 11
Nutritional iron turned inside out: intestinal stress from a gut microbial perspective
journal, November 2014
- Kortman, Guus A. M.; Raffatellu, Manuela; Swinkels, Dorine W.
- FEMS Microbiology Reviews, Vol. 38, Issue 6
Evaluation of an optimal preparation of human standardized fecal inocula for in vitro fermentation studies
journal, October 2015
- Aguirre, Marisol; Eck, Anat; Koenen, Marjorie E.
- Journal of Microbiological Methods, Vol. 117
Effects of Dietary Iron Levels on Growth Performance, Hematological Status, Liver Mineral Concentration, Fecal Microflora, and Diarrhea Incidence in Weanling Pigs
journal, August 2008
- Lee, Seung Hyung; Shinde, Prashant; Choi, Jaeyong
- Biological Trace Element Research, Vol. 126, Issue S1
Iron fortification adversely affects the gut microbiome, increases pathogen abundance and induces intestinal inflammation in Kenyan infants
journal, August 2014
- Jaeggi, Tanja; Kortman, Guus A. M.; Moretti, Diego
- Gut, Vol. 64, Issue 5
Salmonella Adhesion, Invasion and Cellular Immune Responses Are Differentially Affected by Iron Concentrations in a Combined In Vitro Gut Fermentation-Cell Model
journal, March 2014
- Dostal, Alexandra; Gagnon, Mélanie; Chassard, Christophe
- PLoS ONE, Vol. 9, Issue 3
The effects of iron fortification on the gut microbiota in African children: a randomized controlled trial in Côte d'Ivoire
journal, October 2010
- Zimmermann, Michael B.; Chassard, Christophe; Rohner, Fabian
- The American Journal of Clinical Nutrition, Vol. 92, Issue 6
Faecal Microbiota and Short-Chain Fatty Acid Levels in Faeces from Infants with Cow‘s Milk Protein Allergy
journal, January 2011
- Thompson-Chagoyan, Oscar C.; Fallani, Matteo; Maldonado, José
- International Archives of Allergy and Immunology, Vol. 156, Issue 3
The Effect of the Undigested Fraction of Maize Products on the Activity and Composition of the Microbiota Determined in a Dynamic in Vitro Model of the Human Proximal Large Intestine
journal, December 2009
- Maathuis, Annet; Hoffman, Andrew; Evans, Annette
- Journal of the American College of Nutrition, Vol. 28, Issue 6
Nutritional immunity: transition metals at the pathogen–host interface
journal, July 2012
- Hood, M. Indriati; Skaar, Eric P.
- Nature Reviews Microbiology, Vol. 10, Issue 8
The dynamics of gut-associated microbial communities during inflammation
journal, March 2013
- Winter, Sebastian E.; Lopez, Christopher A.; Bäumler, Andreas J.
- EMBO reports, Vol. 14, Issue 4
Effect of Colonic Bacterial Metabolites on Caco-2 Cell Paracellular Permeability In Vitro
journal, March 2008
- Hughes, Roisin; Kurth, Mary Jo; McGilligan, Victoria
- Nutrition and Cancer, Vol. 60, Issue 2
Iron Depletion and Repletion with Ferrous Sulfate or Electrolytic Iron Modifies the Composition and Metabolic Activity of the Gut Microbiota in Rats
journal, December 2011
- Dostal, Alexandra; Chassard, Christophe; Hilty, Florentine M.
- The Journal of Nutrition, Vol. 142, Issue 2
The domain Archaea in human mucosal surfaces
journal, September 2012
- Matarazzo, F.; Ribeiro, A. C.; Faveri, M.
- Clinical Microbiology and Infection, Vol. 18, Issue 9
The Effect of Various Inulins and Clostridium difficile on the Metabolic Activity of the Human Colonic Microbiota in vitro
journal, November 2003
- van Nuenen, Marleen H. M. C.; Diederick Meyer, P.; Venema, Koen
- Microbial Ecology in Health and Disease, Vol. 15, Issue 2-3
Functions of Bacterial Flagella
journal, January 1996
- Moens, Sara; Vanderleyden, Jos
- Critical Reviews in Microbiology, Vol. 22, Issue 2
Gastrointestinal Tract: Intestinal Fatty Acid Metabolism and Implications for Health
book, January 2010
- Hoyles, L.; Wallace, R. J.
- Handbook of Hydrocarbon and Lipid Microbiology
Alpha-keto acids are novel siderophores in the genera Proteus, Providencia, and Morganella and are produced by amino acid deaminases.
journal, January 1993
- Drechsel, H.; Thieken, A.; Reissbrodt, R.
- Journal of Bacteriology, Vol. 175, Issue 9
Interactions Between the Microbiota and the Immune System
journal, June 2012
- Hooper, L. V.; Littman, D. R.; Macpherson, A. J.
- Science, Vol. 336, Issue 6086
The Global Hidden Hunger Indices and Maps: An Advocacy Tool for Action
journal, June 2013
- Muthayya, Sumithra; Rah, Jee Hyun; Sugimoto, Jonathan D.
- PLoS ONE, Vol. 8, Issue 6
Gut Microbial Activity, Implications for Health and Disease: The Potential Role of Metabolite Analysis
journal, October 2012
- Nyangale, Edna. P.; Mottram, Donald. S.; Gibson, Glenn. R.
- Journal of Proteome Research, Vol. 11, Issue 12
Major players on the microbial stage: why archaea are important
journal, February 2011
- Jarrell, K. F.; Walters, A. D.; Bochiwal, C.
- Microbiology, Vol. 157, Issue 4
Gut Microbiota in Health and Disease
journal, July 2010
- Sekirov, Inna; Russell, Shannon L.; Antunes, L. Caetano M.
- Physiological Reviews, Vol. 90, Issue 3
Linking phylogenetic identities of bacteria to starch fermentation in an in vitro model of the large intestine by RNA-based stable isotope probing
journal, April 2009
- Kovatcheva-Datchary, Petia; Egert, Markus; Maathuis, Annet
- Environmental Microbiology, Vol. 11, Issue 4
Diet and faecal flora in the newborn: iron.
journal, December 1991
- Balmer, S. E.; Wharton, B. A.
- Archives of Disease in Childhood, Vol. 66, Issue 12
Regulation of short-chain fatty acid production
journal, February 2003
- Macfarlane, Sandra; Macfarlane, George T.
- Proceedings of the Nutrition Society, Vol. 62, Issue 1
Effects of probiotics and antibiotics on the intestinal homeostasis in a computer controlled model of the large intestine
journal, January 2012
- Rehman, Ateequr; Heinsen, Femke-Anouska; Koenen, Marjorie E.
- BMC Microbiology, Vol. 12, Issue 1
Dissimilatory Amino Acid Metabolism in Human Colonic Bacteria
journal, October 1997
- Smith, E. A.; Macfarlane, G. T.
- Anaerobe, Vol. 3, Issue 5
Different Human Gut Models Reveal the Distinct Fermentation Patterns of Arabinoxylan versus Inulin
journal, October 2013
- Van den Abbeele, Pieter; Venema, Koen; Van de Wiele, Tom
- Journal of Agricultural and Food Chemistry, Vol. 61, Issue 41
Influence of dietary protein content and source on colonic fermentative activity in dogs differing in body size and digestive tolerance1
journal, August 2012
- Nery, J.; Goudez, R.; Biourge, V.
- Journal of Animal Science, Vol. 90, Issue 8
To pool or not to pool? Impact of the use of individual and pooled fecal samples for in vitro fermentation studies
journal, December 2014
- Aguirre, Marisol; Ramiro-Garcia, Javier; Koenen, Marjorie E.
- Journal of Microbiological Methods, Vol. 107
Iron and infection: the heart of the matter
journal, March 2005
- Bullen, John J.; Rogers, Henry J.; Spalding, Paul B.
- FEMS Immunology & Medical Microbiology, Vol. 43, Issue 3
Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine
journal, May 2009
- Louis, Petra; Flint, Harry J.
- FEMS Microbiology Letters, Vol. 294, Issue 1
Fermentation in the human large intestine and the available substrates
journal, May 1987
- Cummings, J. H.; Englyst, H. N.
- The American Journal of Clinical Nutrition, Vol. 45, Issue 5
Characterization of 2-ketoisovalerate ferredoxin oxidoreductase, a new and reversible coenzyme A-dependent enzyme involved in peptide fermentation by hyperthermophilic archaea.
journal, February 1996
- Heider, J.; Mai, X.; Adams, M. W.
- Journal of Bacteriology, Vol. 178, Issue 3
Galacto-Oligosaccharides Have Prebiotic Activity in a Dynamic In Vitro Colon Model Using a 13C-Labeling Technique
journal, May 2012
- Maathuis, Annet J. H.; van den Heuvel, Ellen G.; Schoterman, Margriet H. C.
- The Journal of Nutrition, Vol. 142, Issue 7
Diet and faecal flora in the newborn: lactoferrin.
journal, December 1989
- Balmer, S. E.; Scott, P. H.; Wharton, B. A.
- Archives of Disease in Childhood, Vol. 64, Issue 12
The Effects of Dietary Ferric Iron and Iron Deprivation on the Bacterial Composition of the Mouse Intestine
journal, January 2001
- Tompkins, Geoffrey R.; O'Dell, Norris L.; Bryson, Israel T.
- Current Microbiology, Vol. 43, Issue 1
Bacterial iron homeostasis
journal, June 2003
- Andrews, Simon C.; Robinson, Andrea K.; Rodríguez-Quiñones, Francisco
- FEMS Microbiology Reviews, Vol. 27, Issue 2-3
Iron supplementation promotes gut microbiota metabolic activity but not colitis markers in human gut microbiota-associated rats
journal, February 2014
- Dostal, Alexandra; Lacroix, Christophe; Pham, Van T.
- British Journal of Nutrition, Vol. 111, Issue 12
Iron bioavailability and dietary reference values
journal, March 2010
- Hurrell, Richard; Egli, Ines
- The American Journal of Clinical Nutrition, Vol. 91, Issue 5
Fermentation in the Human Large Intestine: Its Physiologic Consequences and the Potential Contribution of Prebiotics
journal, January 2011
- Macfarlane, George T.; Macfarlane, Sandra
- Journal of Clinical Gastroenterology, Vol. 45
Effect of iron on neonatal gut flora during the first three months of life
journal, June 1985
- Mevissen-Verhage, E. A. E.; Marcelis, J. H.; Harmsen-Van Amerongen, W. C. M.
- European Journal of Clinical Microbiology, Vol. 4, Issue 3
Bacteroides: the Good, the Bad, and the Nitty-Gritty
journal, October 2007
- Wexler, Hannah M.
- Clinical Microbiology Reviews, Vol. 20, Issue 4
Nutritional iron deficiency
journal, August 2007
- Zimmermann, Michael B.; Hurrell, Richard F.
- The Lancet, Vol. 370, Issue 9586
Low iron availability in continuous in vitro colonic fermentations induces strong dysbiosis of the child gut microbial consortium and a decrease in main metabolites
text, January 2013
- Dostal, Alexandra; Fehlbaum, Sophie; Chassard, Christophe
- ETH Zurich
Salmonella Adhesion, Invasion and Cellular Immune Responses Are Differentially Affected by Iron Concentrations in a Combined In Vitro Gut Fermentation-Cell Model
text, January 2014
- Alexandra, Dostal,; Mélanie, Gagnon,; Christophe, Chassard,
- ETH Zurich
Gastrointestinal Tract: Intestinal Fatty Acid Metabolism and Implications for Health
book, November 2018
- Hoyles, Lesley; John Wallace, R.
- Health Consequences of Microbial Interactions with Hydrocarbons, Oils, and Lipids
Iron supplementation promotes gut microbiota metabolic activity but not colitis markers in human gut microbiota-associated rats
text, January 2014
- Dostal, Alexandra; Lacroix, Christophe; Pham, Van T.
- ETH Zurich
Gastrointestinal Tract: Intestinal Fatty Acid Metabolism and Implications for Health
book, April 2020
- Hoyles, Lesley; John Wallace, R.
- Health Consequences of Microbial Interactions with Hydrocarbons, Oils, and Lipids
Salmonella adhesion, invasion and cellular immune responses are differentially affected by iron concentrations in a combined in vitro gut fermentation-cell model
text, January 2014
- Alexandra, Dostal,; Mélanie, Gagnon,; Christophe, Chassard,
- Public Library of Science (PLoS)
Dissimilatory Amino Acid Metabolism in Human Colonic Bacteria
journal, October 1997
- Smith, E. A.; Macfarlane, G. T.
- Anaerobe, Vol. 3, Issue 5
Gastrointestinal effects of single and repeated doses of ferrous sulphate in rats
journal, January 1993
- Benoni, G.; Cuzzolin, L.; Zambreri, D.
- Pharmacological Research, Vol. 27, Issue 1
Gastrointestinal Tract: Intestinal Fatty Acid Metabolism and Implications for Health
book, January 2010
- Hoyles, L.; Wallace, R. J.
- Handbook of Hydrocarbon and Lipid Microbiology
A computer-controlled system to simulate conditions of the large intestine with peristaltic mixing, water absorption and absorption of fermentation products
journal, December 1999
- Minekus, M.; Smeets-Peeters, M.; Bernalier, A.
- Applied Microbiology and Biotechnology, Vol. 53, Issue 1
The Effects of Dietary Ferric Iron and Iron Deprivation on the Bacterial Composition of the Mouse Intestine
journal, January 2001
- Tompkins, Geoffrey R.; O'Dell, Norris L.; Bryson, Israel T.
- Current Microbiology, Vol. 43, Issue 1
Acetogenesis and the Wood–Ljungdahl pathway of CO2 fixation
journal, December 2008
- Ragsdale, Stephen W.; Pierce, Elizabeth
- Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1784, Issue 12, p. 1873-1898
Experimental models of the gut microbiome
journal, February 2013
- Venema, Koen; van den Abbeele, Pieter
- Best Practice & Research Clinical Gastroenterology, Vol. 27, Issue 1
Iron and infection: the heart of the matter
journal, March 2005
- Bullen, John J.; Rogers, Henry J.; Spalding, Paul B.
- FEMS Immunology & Medical Microbiology, Vol. 43, Issue 3
Effects of Different Complementary Feeding Regimens on Iron Status and Enteric Microbiota in Breastfed Infants
journal, August 2013
- Krebs, Nancy F.; Sherlock, Laurie G.; Westcott, Jamie
- The Journal of Pediatrics, Vol. 163, Issue 2
To pool or not to pool? Impact of the use of individual and pooled fecal samples for in vitro fermentation studies
journal, December 2014
- Aguirre, Marisol; Ramiro-Garcia, Javier; Koenen, Marjorie E.
- Journal of Microbiological Methods, Vol. 107
Advances and perspectives in in vitro human gut fermentation modeling
journal, January 2012
- Payne, Amanda N.; Zihler, Annina; Chassard, Christophe
- Trends in Biotechnology, Vol. 30, Issue 1
Nutritional iron deficiency in patients with chronic illnesses
journal, December 2007
- Thum, Thomas; Anker, Stefan D.
- The Lancet, Vol. 370, Issue 9603
Different Human Gut Models Reveal the Distinct Fermentation Patterns of Arabinoxylan versus Inulin
journal, October 2013
- Van den Abbeele, Pieter; Venema, Koen; Van de Wiele, Tom
- Journal of Agricultural and Food Chemistry, Vol. 61, Issue 41
Gut Microbial Activity, Implications for Health and Disease: The Potential Role of Metabolite Analysis
journal, October 2012
- Nyangale, Edna. P.; Mottram, Donald. S.; Gibson, Glenn. R.
- Journal of Proteome Research, Vol. 11, Issue 12
A human gut microbial gene catalogue established by metagenomic sequencing
journal, March 2010
- Qin, Junjie; Li, Ruiqiang; Raes, Jeroen
- Nature, Vol. 464, Issue 7285
Nutritional immunity: transition metals at the pathogen–host interface
journal, July 2012
- Hood, M. Indriati; Skaar, Eric P.
- Nature Reviews Microbiology, Vol. 10, Issue 8
The Effect of the Undigested Fraction of Maize Products on the Activity and Composition of the Microbiota Determined in a Dynamic in Vitro Model of the Human Proximal Large Intestine
journal, December 2009
- Maathuis, Annet; Hoffman, Andrew; Evans, Annette
- Journal of the American College of Nutrition, Vol. 28, Issue 6
The Effect of Various Inulins and Clostridium difficile on the Metabolic Activity of the Human Colonic Microbiota in vitro
journal, November 2003
- van Nuenen, Marleen H. M. C.; Diederick Meyer, P.; Venema, Koen
- Microbial Ecology in Health and Disease, Vol. 15, Issue 2-3
Fermentation in the human large intestine and the available substrates
journal, May 1987
- Cummings, J. H.; Englyst, H. N.
- The American Journal of Clinical Nutrition, Vol. 45, Issue 5
Evaluating the microbial diversity of an in vitro model of the human large intestine by phylogenetic microarray analysis
journal, November 2010
- Rajilić-Stojanović, Mirjana; Maathuis, Annet; Heilig, Hans G. H. J.
- Microbiology, Vol. 156, Issue 11
Major players on the microbial stage: why archaea are important
journal, February 2011
- Jarrell, K. F.; Walters, A. D.; Bochiwal, C.
- Microbiology, Vol. 157, Issue 4
Nutritional iron turned inside out: intestinal stress from a gut microbial perspective
journal, November 2014
- Kortman, Guus A. M.; Raffatellu, Manuela; Swinkels, Dorine W.
- FEMS Microbiology Reviews, Vol. 38, Issue 6
Linking phylogenetic identities of bacteria to starch fermentation in an in vitro model of the large intestine by RNA-based stable isotope probing
journal, April 2009
- Kovatcheva-Datchary, Petia; Egert, Markus; Maathuis, Annet
- Environmental Microbiology, Vol. 11, Issue 4
The domain Archaea in human mucosal surfaces
journal, September 2012
- Matarazzo, F.; Ribeiro, A. C.; Faveri, M.
- Clinical Microbiology and Infection, Vol. 18, Issue 9
Low iron availability in continuous in vitro colonic fermentations induces strong dysbiosis of the child gut microbial consortium and a decrease in main metabolites
journal, August 2012
- Dostal, Alexandra; Fehlbaum, Sophie; Chassard, Christophe
- FEMS Microbiology Ecology, Vol. 83, Issue 1
Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine
journal, May 2009
- Louis, Petra; Flint, Harry J.
- FEMS Microbiology Letters, Vol. 294, Issue 1
Interactions Between the Microbiota and the Immune System
journal, June 2012
- Hooper, L. V.; Littman, D. R.; Macpherson, A. J.
- Science, Vol. 336, Issue 6086
Use of a three-stage continuous culture system to study the effect of mucin on dissimilatory sulfate reduction and methanogenesis by mixed populations of human gut bacteria.
journal, January 1988
- Gibson, G. R.; Cummings, J. H.; Macfarlane, G. T.
- Applied and Environmental Microbiology, Vol. 54, Issue 11
Alpha-keto acids are novel siderophores in the genera Proteus, Providencia, and Morganella and are produced by amino acid deaminases.
journal, January 1993
- Drechsel, H.; Thieken, A.; Reissbrodt, R.
- Journal of Bacteriology, Vol. 175, Issue 9
Characterization of 2-ketoisovalerate ferredoxin oxidoreductase, a new and reversible coenzyme A-dependent enzyme involved in peptide fermentation by hyperthermophilic archaea.
journal, February 1996
- Heider, J.; Mai, X.; Adams, M. W.
- Journal of Bacteriology, Vol. 178, Issue 3
Diet and faecal flora in the newborn: casein and whey proteins.
journal, December 1989
- Balmer, S. E.; Scott, P. H.; Wharton, B. A.
- Archives of Disease in Childhood, Vol. 64, Issue 12
Diet and faecal flora in the newborn: lactoferrin.
journal, December 1989
- Balmer, S. E.; Scott, P. H.; Wharton, B. A.
- Archives of Disease in Childhood, Vol. 64, Issue 12
Diet and faecal flora in the newborn: iron.
journal, December 1991
- Balmer, S. E.; Wharton, B. A.
- Archives of Disease in Childhood, Vol. 66, Issue 12
Effect of iron supplementation on incidence of infectious illness in children: systematic review
journal, November 2002
- Gera, T.
- BMJ, Vol. 325, Issue 7373
Depletion of luminal iron alters the gut microbiota and prevents Crohn's disease-like ileitis
journal, November 2010
- Werner, T.; Wagner, S. J.; Martinez, I.
- Gut, Vol. 60, Issue 3
Iron fortification adversely affects the gut microbiome, increases pathogen abundance and induces intestinal inflammation in Kenyan infants
journal, August 2014
- Jaeggi, Tanja; Kortman, Guus A. M.; Moretti, Diego
- Gut, Vol. 64, Issue 5
Gut Microbiota in Health and Disease
journal, July 2010
- Sekirov, Inna; Russell, Shannon L.; Antunes, L. Caetano M.
- Physiological Reviews, Vol. 90, Issue 3
Faecal Microbiota and Short-Chain Fatty Acid Levels in Faeces from Infants with Cow‘s Milk Protein Allergy
journal, January 2011
- Thompson-Chagoyan, Oscar C.; Fallani, Matteo; Maldonado, José
- International Archives of Allergy and Immunology, Vol. 156, Issue 3
Effects of probiotics and antibiotics on the intestinal homeostasis in a computer controlled model of the large intestine
journal, January 2012
- Rehman, Ateequr; Heinsen, Femke-Anouska; Koenen, Marjorie E.
- BMC Microbiology, Vol. 12, Issue 1
Iron Availability Increases the Pathogenic Potential of Salmonella Typhimurium and Other Enteric Pathogens at the Intestinal Epithelial Interface
journal, January 2012
- Kortman, Guus A. M.; Boleij, Annemarie; Swinkels, Dorine W.
- PLoS ONE, Vol. 7, Issue 1
The Global Hidden Hunger Indices and Maps: An Advocacy Tool for Action
journal, June 2013
- Muthayya, Sumithra; Rah, Jee Hyun; Sugimoto, Jonathan D.
- PLoS ONE, Vol. 8, Issue 6
Functions of Bacterial Flagella
journal, January 1996
- Moens, Sara; Vanderleyden, Jos
- Critical Reviews in Microbiology, Vol. 22, Issue 2
The effects of iron fortification on the gut microbiota in African children: a randomized controlled trial in Côte d'Ivoire
journal, October 2010
- Zimmermann, Michael B.; Chassard, Christophe; Rohner, Fabian
- The American Journal of Clinical Nutrition, Vol. 92, Issue 6
Galacto-Oligosaccharides Have Prebiotic Activity in a Dynamic In Vitro Colon Model Using a 13C-Labeling Technique
journal, May 2012
- Maathuis, Annet J. H.; van den Heuvel, Ellen G.; Schoterman, Margriet H. C.
- The Journal of Nutrition, Vol. 142, Issue 7
Bacteria, Colonic Fermentation, and Gastrointestinal Health
journal, January 2012
- Macfarlane, George T.; Macfarlane, Sandra
- Journal of AOAC International, Vol. 95, Issue 1
Works referencing / citing this record:
Constipation in chronic kidney disease: it is time to reconsider
journal, December 2019
- Ikee, Ryota; Yano, Kazuhiro; Tsuru, Tomomi
- Renal Replacement Therapy, Vol. 5, Issue 1
Association between the gut microbiota and mineral metabolism: Gut microbiota and mineral metabolism
journal, October 2017
- Skrypnik, Katarzyna; Suliburska, Joanna
- Journal of the Science of Food and Agriculture, Vol. 98, Issue 7
Dietary strategies for improving iron status: balancing safety and efficacy
journal, December 2016
- Prentice, Andrew M.; Mendoza, Yery A.; Pereira, Dora
- Nutrition Reviews, Vol. 75, Issue 1
Potential for enriching next-generation health-promoting gut bacteria through prebiotics and other dietary components
journal, May 2019
- Lordan, Cathy; Thapa, Dinesh; Ross, R. Paul
- Gut Microbes, Vol. 11, Issue 1
Divergent short-chain fatty acid production and succession of colonic microbiota arise in fermentation of variously-sized wheat bran fractions
journal, November 2018
- Tuncil, Yunus E.; Thakkar, Riya D.; Marcia, Arianna D. Romero
- Scientific Reports, Vol. 8, Issue 1
The Phosphate Binder Ferric Citrate Alters the Gut Microbiome in Rats with Chronic Kidney Disease
journal, October 2018
- Lau, Wei Ling; Vaziri, Nosratola D.; Nunes, Ane C. F.
- Journal of Pharmacology and Experimental Therapeutics, Vol. 367, Issue 3
Dietary strategies for improving iron status: balancing safety and efficacy
text, January 2017
- Jorg, Spieldenner,; Dora, Pereira,; Rita, Wegmuller,
- The University of North Carolina at Chapel Hill University Libraries
Dietary strategies for improving iron status: balancing safety and efficacy.
text, January 2017
- Prentice, Andrew M.; Mendoza, Yery A.; Pereira, Dora
- Apollo - University of Cambridge Repository
A decrease in iron availability to human gut microbiome reduces the growth of potentially pathogenic gut bacteria; an in vitro colonic fermentation study
journal, May 2019
- Parmanand, Bhavika A.; Kellingray, Lee; Le Gall, Gwenaelle
- The Journal of Nutritional Biochemistry, Vol. 67
Potential for enriching next-generation health-promoting gut bacteria through prebiotics and other dietary components
journal, May 2019
- Lordan, Cathy; Thapa, Dinesh; Ross, R. Paul
- Gut Microbes, Vol. 11, Issue 1
Iron Sequestration in Microbiota Biofilms As A Novel Strategy for Treating Inflammatory Bowel Disease
journal, May 2018
- Motta, Jean-Paul; Allain, Thibault; Green-Harrison, Luke E.
- Inflammatory Bowel Diseases, Vol. 24, Issue 7
Pathobiont release from dysbiotic gut microbiota biofilms in intestinal inflammatory diseases: a role for iron?
journal, January 2019
- Buret, Andre Gerald; Motta, Jean-Paul; Allain, Thibault
- Journal of Biomedical Science, Vol. 26, Issue 1
Dietary strategies for improving iron status: balancing safety and efficacy
text, January 2017
- Jorg, Spieldenner,; Dora, Pereira,; Rita, Wegmuller,
- The University of North Carolina at Chapel Hill University Libraries