Diet-Microbe Interactions in the Gut: Effects on Human Health and Disease

268 Pages·2014·11.29 MB·English

by  Kieran Tuohy

DIET-MICROBE INTERACTIONS
IN THE GUT
This pageintentionallyleftblank
DIET-MICROBE
INTERACTIONS
IN THE GUT
Effects on Human Health
and Disease
Edited by
K T
IERAN UOHY
DepartmentofFoodQualityandNutrition,ResearchandInnovationCentre,
FoundationEdmundMach(FEM),SanMicheleall’Adige,Trento,Italy
D D R
ANIELE EL IO
DepartmentofFoodScience,UniversityofParma,Parma,Italy
AMSTERDAM(cid:129)BOSTON(cid:129)HEIDELBERG(cid:129)LONDON
NEWYORK(cid:129)OXFORD(cid:129)PARIS(cid:129)SANDIEGO
SANFRANCISCO(cid:129)SINGAPORE(cid:129)SYDNEY(cid:129)TOKYO
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Contents
Foreword...................................................................................................................................................ix
Acknowledgements....................................................................................................................................xi
List of Contributors.................................................................................................................................xiii
1. The Microbiota of the Human Gastrointestinal Tract: A Molecular View..........................................1
KIERANM.TUOHYANDKARENP.SCOTT
Introduction................................................................................................................................................................................1
Gut Microbiota MetabolisminHealth and Disease.................................................................................................................1
Methodologies for Studying the Human Gut Microbiota.........................................................................................................3
Spatial Distribution ofthe Gut Microbiota andInteractionswith Diet..................................................................................6
Models toStudy Microbial Ecology.........................................................................................................................................10
Conclusions...............................................................................................................................................................................11
References.................................................................................................................................................................................11
2. A Nutritional Anthropology of the Human Gut Microbiota.............................................................17
CARLOTTADEFILIPPOANDKIERANM.TUOHY
Human Diet orMicrobiota,Which Came First?.....................................................................................................................17
Metagenomics and Cultivation-IndependentAssessment ofHumanGut Microbiota.........................................................18
MicrobiomeandHuman Nutritional Phenotype....................................................................................................................18
The Gut Microbiota inHuman Evolution..............................................................................................................................19
Population Metagenomic Variation within the Human Microbiota......................................................................................21
The Western Diet Metagenome Is Obesity Prone..................................................................................................................24
Conclusions...............................................................................................................................................................................25
References.................................................................................................................................................................................25
3. Probiotic Microorganisms for Shaping the Human Gut Microbiota (cid:1) Mechanisms
and Efficacy into the Future ......................................................................................................................27
LORENZOMORELLIANDVANIAPATRONE
Introduction..............................................................................................................................................................................27
Let’sStartWith the Definition ofProbiotics..........................................................................................................................27
Shaping the Microbiota............................................................................................................................................................28
The Neonatal Period................................................................................................................................................................29
Adult Lifeand the Proposed Enterotype Classification..........................................................................................................31
The Aged Period.......................................................................................................................................................................32
Mechanisms and Efficacy.........................................................................................................................................................33
Efficacy inHealthyPeople.......................................................................................................................................................33
Conclusions...............................................................................................................................................................................37
References.................................................................................................................................................................................37
4. Bifidobacteria of the Human Gut: Our Special Friends......................................................................41
MARCOVENTURA,FRANCESCATURRONIANDDOUWEVANSINDEREN
TaxonomyofBifidobacteria.....................................................................................................................................................41
Bifidobacterial Ecology.............................................................................................................................................................43
v
vi
CONTENTS
Bifidobacterial Populations inthe HumanGut......................................................................................................................43
Bifidobacteria as Probiotics......................................................................................................................................................44
Bifidobacterial Genomics.........................................................................................................................................................45
Comparative Genomics and Bifidobacteria.............................................................................................................................46
Interaction Between Bifidobacteriaand TheirHosts.............................................................................................................47
Conclusions...............................................................................................................................................................................48
References.................................................................................................................................................................................49
5. Shaping the Human Microbiome with Prebiotic Foods (cid:1) Current Perspectives
for Continued Development......................................................................................................................53
KIERANM.TUOHY,DUNCANT.BROWN,ANNETTKLINDER,ADELECOSTABILEANDFRANCESCAFAVA
Introduction..............................................................................................................................................................................53
Linking Microbiome Structure and Function..........................................................................................................................54
Probiotics...................................................................................................................................................................................55
Prebiotics...................................................................................................................................................................................56
Testing Prebiotics......................................................................................................................................................................59
Conclusion................................................................................................................................................................................65
References.................................................................................................................................................................................66
6. Bioactivation of High-Molecular-Weight Polyphenols by the Gut Microbiome...............................73
PEDROMENA,LUCACALANI,RENATOBRUNIANDDANIELEDELRIO
Introduction..............................................................................................................................................................................73
Proanthocyanidins....................................................................................................................................................................73
Hydrolyzable Tannins (Gallotannins andEllagitannins)........................................................................................................85
Conclusions...............................................................................................................................................................................98
References.................................................................................................................................................................................98
7. Gut Microbial Metabolism of Plant Lignans: Influence on Human Health.....................................103
SETHC.YODER,SAMUELM.LANCASTER,MEREDITHA.J.HULLARANDJOHANNAW.LAMPE
Introduction............................................................................................................................................................................103
ConversionofPlant Lignans toEnterolignans byGut Bacteria..........................................................................................104
Associations Between Lignan Exposureand Human Health...............................................................................................107
Interindividual Differences inLignan Metabolism...............................................................................................................110
Conclusions.............................................................................................................................................................................114
Acknowledgements.................................................................................................................................................................114
References...............................................................................................................................................................................114
8. Gut Microbiome Modulates Dietary Xenobiotic Toxicity: The Case of DON
and Its Derivatives....................................................................................................................................119
MARTINACIRLINI,RENATOBRUNIANDCHIARADALL’ASTA
Introduction............................................................................................................................................................................119
Gastric Stability ofDON Derivatives....................................................................................................................................121
Bacterial Transformation andIntestinal Absorptionof DON and Its Derivatives..............................................................121
DON and DON-ConjugatesImpact onthe Human Gut.....................................................................................................123
References...............................................................................................................................................................................124
9. Gut Microbiota(cid:1)Immune System Crosstalk: Implications for Metabolic Disease...........................127
FRANCESCAFAVA
GutMicrobial Recognition by the Immune System.............................................................................................................127
Intestinal Barrier,Gut Permeability and Metabolic Inflammation......................................................................................129
vii
CONTENTS
Effects ofIntestinal Bacterial Short-Chain Fatty Acids (SCFAs)on Inflammation and Metabolism...............................130
Dietary Fat Metabolism,Bile Acids andGut Microbiota.....................................................................................................131
Diet, TMAO, Gut Microbiota and Atherosclerosis..............................................................................................................132
Immune Versus Metabolic Functions inIntestinal Epithelial Cells Gene Networks..........................................................133
Conclusion..............................................................................................................................................................................134
References...............................................................................................................................................................................135
10. The Interplay of Epigenetics and Epidemiology in Autoimmune Diseases:
Time for Geoepigenetics.......................................................................................................................... 139
CARLOSELMIANDANGELACERIBELLI
The Etiologyand Pathogenesis ofAutoimmune Disease......................................................................................................139
The Rationale for Geoepigenetics.........................................................................................................................................140
GeoepigeneticsofSystemic Lupus Erythematosus (SLE).....................................................................................................141
GeoepigeneticsofRheumatoid Arthritis(RA).....................................................................................................................143
GeoepigeneticsofSystemic Sclerosis.....................................................................................................................................144
Conclusions.............................................................................................................................................................................145
References...............................................................................................................................................................................145
11. Obesity-Associated Gut Microbiota: Characterization and Dietary Modulation...........................149
QINGSHENANDVATSALAMAITIN
The Obesity Pandemic...........................................................................................................................................................149
Genetic Determinants ofObesity..........................................................................................................................................149
Obesity AssociatedGut Microbiota.......................................................................................................................................150
Interactionsbetween Gut Microbesand Obesity: “TheEnergy Extraction Theory”..........................................................154
Interactionsbetween Gut Microbesand Obesity: “TheAppetite Control Theory”...........................................................157
Interactionsbetween Gut Microbesand Obesity: “TheInflammation Theory”.................................................................158
Gut Microbiota as aTherapeuticTargetofProbiotics, Prebiotics and Synbiotics..............................................................161
Conclusions.............................................................................................................................................................................166
References...............................................................................................................................................................................166
12. An Apple a Day Keeps the Doctor Away (cid:1) Inter-Relationship Between
Apple Consumption, the Gut Microbiota and Cardiometabolic Disease
Risk Reduction......................................................................................................................................... 173
ATHANASIOSKOUTSOSANDJULIEA.LOVEGROVE
Introduction............................................................................................................................................................................173
Apple Components.................................................................................................................................................................173
The Human Gut Microbiota..................................................................................................................................................178
CardiometabolicDisease Risk(cid:1)Epidemiological Studies...................................................................................................180
CardiometabolicRisk Factors................................................................................................................................................181
Diabetes Risk..........................................................................................................................................................................187
Conclusion..............................................................................................................................................................................187
References...............................................................................................................................................................................188
13. Whole Plant Foods and Colon Cancer Risk....................................................................................195
EMMAM.BROWN,IANROWLAND,NIGELG.TERNAN,PHILIPALLSOPP,GEOFFMCMULLANANDCHRISI.R.GILL
Introduction............................................................................................................................................................................195
Diet and Colorectal Cancer...................................................................................................................................................195
Biological Activity and Anticancer Properties ofWhole-Grain Cereals.............................................................................197
Biological Activity and Anticancer Properties ofBrassicaVegetables.................................................................................199
Human Studies........................................................................................................................................................................199
viii
CONTENTS
Biological Activity andAnticancer Properties ofBerry Fruits.............................................................................................201
Conclusion..............................................................................................................................................................................203
References...............................................................................................................................................................................204
14. Population Level Divergence from the Mediterranean Diet and the Risk of Cancer
and Metabolic Disease..............................................................................................................................209
GEORGEPOUNIS,MARIALAURABONACCIO,KIERANM.TUOHY,MARIABENEDETTADONATI,
GIOVANNIDEGAETANOANDLICIAIACOVIELLO
MediterraneanDiet as the Traditional Diet ofSouthern Europe.........................................................................................209
The Evidence-Based Health Protection by Mediterranean Diet..........................................................................................211
MediterraneanDiet as a Health Protection Model...............................................................................................................214
MediterraneanFoodConsumption andHumanGut Microbiota.........................................................................................216
References...............................................................................................................................................................................219
15. Diet and the Gut Microbiota (cid:1) How the Gut: Brain Axis Impacts on Autism............................225
KIERANM.TUOHY,PAOLAVENUTI,SIMONECUVA,CESAREFURLANELLO,MATTIAGASPEROTTI,
ANDREAMANCINI,FLORENCIACEPPA,DUCCIOCAVALIERI,CARLOTTADEFILIPPO,URSKAVRHOVSEK,
PEDROMENA,DANIELEDELRIOANDFRANCESCAFAVA
Background.............................................................................................................................................................................225
GutMicrobiota and ASD.......................................................................................................................................................226
Amino Acid Metabolism........................................................................................................................................................228
Lipid Metabolismand the Brain............................................................................................................................................230
Short-Chain Fatty Acids (SCFA) and the Brain..................................................................................................................231
GutMicrobiota and DigestiveFunction................................................................................................................................233
Probiotics, Gut MicrobiotaSuccessional Developmentand Brain Function.......................................................................237
Conclusions.............................................................................................................................................................................238
References...............................................................................................................................................................................238
Index......................................................................................................................................................247
Foreword
Recent metagenomic studies are confirming what pioneers in gut microbiology have been saying for a long
time, that diet:microbe interactions in the gut are critical for human health and disease. Overcoming the limita-
tions of culture based microbiology to study the ecology of the mainly anaerobic, culture recalcitrant and fastidi-
ous microorganisms present within the human gut, the post genomics technologies of metagenomics and
metabolomics are revealing the intricate relationship between microbiota species architecture and metabolic out-
put, and diverse host physiological functions linked to health and chronic non-communicable diseases. The gut
microbiota is now emerging as an important metabolic and immunological organ in its own right, rivalling (and
overcoming) the liver in metabolic diversity and activity, and playing a key role in immune education and
homeostasis. This newly recognised metabolic and immunologically paramount organ is closely linked to other
bodily systems, including adipose tissue, muscle, and even the brain, through the flux of metabolites produced
in, and absorbed from, the gut. Indeed, the gut:brain axis is currently receiving much attention not only for its
role in regulating satiety and whole body energy balance, but also for its involvement in regulating brain devel-
opment, neurological diseases including autism, depression and dementia, and even mood and sleep patterns.
We now know that aberrant microbiota profiles and/or metabolite production are associated with a range of
chronic diseases characterised by loss of metabolic homeostasis and unresolved systemic inflammation, including
the diseases of obesity, diabetes (type 1 and 2), metabolic syndrome, non-alcoholic fatty liver disease, as well as
some cancers, especially colon cancer, and many autoimmune diseases, where unresolved inflammation is
thought to contribute to autoantibody formation and trigger disease. While the gut microbiota have been impli-
cated in the production of toxic compounds or in the activation of pro-carginogens ingested with food (e.g.
cooked food mutagens, xenobiotics and mycotoxins), many microbial metabolites including breakdown products
derived by plant polyphenols, short chain fatty acids, deconjugated bile acids returning from the gut via the
enterohepatic circulation, and B vitamins produced by bifidobacteria are emerging as key beneficial mediators of
human cellular activity throughout the body. These metabolites, which comprise in large part the metabolic flux
from the colonic microbiota, have been implicated in regulating glucose and fat uptake and metabolism, energy
storage, thermogenesis, host hormone secretion, inflammatory molecule production, and epigenetic processes via
histone deacetylase inhibition on the one hand and acetylation and methylation, on the other. In this framework
of harmful or beneficial bio-activation of dietary components exerted by the gut microbiota, the emerging
remarkable variability in its composition helps explaining the parallel variability observed in the way we react to
food intake. Our ability to obtain the maximum benefit from a healthy diet derives not only from our genes, but
also from the presence or absence of specific microbial species in our gut. Moreover, it appears that our nutri-
tionalanthropology plays an important role in shaping not only the relative abundanceof the gut bacteria or also
apparently microbiota composition. Distinct microbiome profiles in distinct populations from diverse corners of
the world and accustomed to very different foods, diets and life-styles highlight the need to act quickly to pre-
serve the natural history of our gut microbiota before the onslaught of dietary globalization, bereft of safe micro-
bial “passengers” and denuded of fibers, prebiotics and plant polyphenols.
Indeed, processes within the gut or rather at the gut wall appear to play a critical role in the persistent low
grade systemic inflammation characteristic of many chronic human diseases, especially those associated with
modern diet and life-styles. Increased intestinal permeability leads to translocation of inflammatory molecules
such as lipopolysaccharide across the gut wall, which then act as continuous triggers for low level systemic
inflammation. This gut leakiness appears to be strongly influenced by diet, especially high fat - low fiber modern
or Western style at one extreme contributing to gut wall permeability, and ancestral or traditional dietary pat-
terns such as the Mediterranean diet, high in fermentable fiber, prebiotics, fruit and vegetables (and indeed cer-
tain probiotic or fermentative microorganisms) at the other, supporting gut barrier function. Bifidobacteria,
lactobacilli, SCFA and bile acid metabolism have been shown to regulate expression of tight junction proteins
between intestinal epithelial cells and reduce gut permeability. Similarly gut inflammation and oxidative damage
play their part and are intricately regulated by diet:microbe interactions within the intestine. Indeed, this process
strongly mirrors the gut leakiness and low grade chronic inflammation characteristic of old age, and at least in
ix