The microbiome: stress, health and disease

Moloney, Rachel D.; Desbonnet, Lieve; Clarke, Gerard; Dinan, Timothy G.; Cryan, John F.

doi:10.1007/s00335-013-9488-5

Cited by 430Gut microbiota and healthGastrointestinal motility and disordersTryptophan and brain disorders

The microbiome: stress, health and disease

Moloney, Rachel D., Desbonnet, Lieve, Clarke, Gerard, Dinan, Timothy G., Cryan, John F.·2014·Mammalian Genome

DOI 10.1007/s00335-013-9488-5

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Abstract

Bacterial colonisation of the gut plays a major role in postnatal development and maturation of key systems that have the capacity to influence central nervous system (CNS) programming and signaling, including the immune and endocrine systems. Individually, these systems have been implicated in the neuropathology of many CNS disorders and collectively they form an important bidirectional pathway of communication between the microbiota and the brain in health and disease. Regulation of the microbiome-brain-gut axis is essential for maintaining homeostasis, including that of the CNS. Moreover, there is now expanding evidence for the view that commensal organisms within the gut play a role in early programming and later responsivity of the stress system. Research has focused on how the microbiota communicates with the CNS and thereby influences brain function. The routes of this communication are not fully elucidated but include neural, humoral, immune and metabolic pathways. This view is underpinned by studies in germ-free animals and in animals exposed to pathogenic bacterial infections, probiotic agents or antibiotics which indicate a role for the gut microbiota in the regulation of mood, cognition, pain and obesity. Thus, the concept of a microbiome-brain-gut axis is emerging which suggests that modulation of the gut microflora may be a tractable strategy for developing novel therapeutics for complex stress-related CNS disorders where there is a huge unmet medical need.

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Dysbiosis is implicated in diseases including obesity, type 2 diabetes, and depression.
“Dysbiosis, a pathogenic disruption of gut microbial composition or host-microbe interactions, is implicated in diseases including obesity, type 2 diabetes, and depression [73].”
From Biological embedding of childhood adversity: from physiological mechanisms to clinical implications (2017) · cites this paper as [73]
Various previous studies have suggested profound microbiome effects on neuroendocrine and immune function, such that dysbiosis could compound ELA-related changes including cortisol dysregulation and chronic inflammation.
“Various previous studies have suggested profound microbiome effects on neuroendocrine and immune function, such that dysbiosis could compound ELA-related changes including cortisol dysregulation and chronic inflammation [73–77].”
From Biological embedding of childhood adversity: from physiological mechanisms to clinical implications (2017) · cites this paper as [73]
The gut microbiota modulates excitatory and inhibitory neurotransmitters (serotonin, GABA and dopamine) and neurotransmitter-like substances, especially in response to physical and emotional stress.
“Evidence shows that the gut microbiota also modulates excitatory and inhibitory neurotransmitters (i.e. serotonin, GABA and dopamine) and neurotransmitter-like substances, especially in response to physical and emotional stress (reviewed by Clarke et al. [21] and Moloney et al [22]).”
From Exercise-induced stress behavior, gut-microbiota-brain axis and diet: a systematic review for athletes (2016) · cites this paper as [22]
The GM influences the stress system, behavior, and cognition in animals.
“Studies in animals have demonstrated the effect that the GM has on neural development and neurochemistry in the host, influencing the stress system, behavior, and cognition (42–47).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [43]
Many risk factors of functional constipation including age, diet, obesity, and stress have a large impact on the gut microbiota.
“many risk factors of FC including age, diet, obesity, and stress have a large impact on the gut microbiota [ 33–35 ]”
From Role of gut microbiota in functional constipation (2021) · cites this paper as [33]

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A controlled crossover study of the selective serotonin reuptake inhibitor citalopram in irritable bowel syndrome
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Commensal microbiota modulate murine behaviors in a strictly contamination-free environment confirmed by culture-based methods
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A Molecular Analysis of Fecal and Mucosal Bacterial Communities in Irritable Bowel Syndrome
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Comparative Metagenomics and Population Dynamics of the Gut Microbiota in Mother and Infant
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Cerebral low-molecular metabolites influenced by intestinal microbiota: a pilot study
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Review article: probiotics for the treatment of irritable bowel syndrome – focus on lactic acid bacteria
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Fish Oil Attenuates Omega-6 Polyunsaturated Fatty Acid-Induced Dysbiosis and Infectious Colitis but Impairs LPS Dephosphorylation Activity Causing Sepsis
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Pathways underlying the gut-to-brain connection in autism spectrum disorders as future targets for disease management
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Early-life stress and cognitive outcome
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Serotonergic dysfunction: Brain imaging and behavioral correlates
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Prebiotics Promote Good Health
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Does the Human Gut Microbiota Contribute to the Etiology of Autism Spectrum Disorders?
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Metagenomics and development of the gut microbiota in infants
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Relationship between the hypothalamic–pituitary–adrenal-axis and fatty acid metabolism in recurrent depression
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Diagnosing Latent Tuberculosis in High-Risk Individuals: Rising to the Challenge in High-Burden Areas
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The microbiome-gut-brain axis in health and disease
Dinan, T. G., & Cryan, J. F. (2017) · Gastroenterology Clinics of North America · doi:10.1016/j.gtc.2016.09.007 · Cited by 1,111 · see citing works
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Breaking down the barriers: the gut microbiome, intestinal permeability and stress-related psychiatric disorders
Kelly, J. R., Kennedy, P. J., Cryan, J. F., Dinan, T. G., Clarke, G., & Hyland, N. P. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00392 · Cited by 1,110 · see citing works
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Microbiota and neurodevelopmental windows: implications for brain disorders
Borre, Y. E., O’Keeffe, G. W., Clarke, G., Stanton, C., Dinan, T. G., & Cryan, J. F. (2014) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2014.05.002 · Cited by 1,089 · see citing works
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Gut microbes and the brain: paradigm shift in neuroscience
Mayer, E. A., Knight, R., Mazmanian, S. K., Cryan, J. F., & Tillisch, K. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.3299-14.2014 · Cited by 1,033 · see citing works
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Targeting the microbiota-gut-brain axis: prebiotics have anxiolytic and antidepressant-like effects and reverse the impact of chronic stress in mice
Burokas, A., Arboleya, S., Moloney, R. D., Peterson, V. L., Murphy, K., Clarke, G., Stanton, C., Dinan, T. G., & Cryan, J. F. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.12.031 · Cited by 952 · see citing works
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Gut instincts: microbiota as a key regulator of brain development, ageing and neurodegeneration
Dinan, T. G., & Cryan, J. F. (2017) · The Journal of Physiology · doi:10.1113/jp273106 · Cited by 813 · see citing works
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Biological embedding of childhood adversity: from physiological mechanisms to clinical implications
Berens, A. E., Jensen, S. K. G., & Nelson, C. A. (2017) · BMC Medicine · doi:10.1186/s12916-017-0895-4 · Cited by 657 · see citing works
“Dysbiosis, a pathogenic disruption of gut microbial composition or host-microbe interactions, is implicated in diseases including obesity, type 2 diabetes, and depression [73].”
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Administration of Lactobacillus helveticus NS8 improves behavioral, cognitive, and biochemical aberrations caused by chronic restraint stress
Liang, S., Wang, T., Hu, X., Luo, J., Li, W., Wu, X., Duan, Y., & Jin, F. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.09.033 · Cited by 651 · see citing works
Exercise-induced stress behavior, gut-microbiota-brain axis and diet: a systematic review for athletes
Clark, A., & Mach, N. (2016) · Journal of the International Society of Sports Nutrition · doi:10.1186/s12970-016-0155-6 · Cited by 583 · see citing works
“[21] and Moloney et al [22]).”
Anxiety, depression, and the microbiome: A role for gut peptides
Lach, G., Schellekens, H., Dinan, T. G., & Cryan, J. F. (2018) · Neurotherapeutics · doi:10.1007/s13311-017-0585-0 · Cited by 573 · see citing works
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Central nervous system control of gastrointestinal motility and secretion and modulation of gastrointestinal functions
Browning, K. N., & Travagli, R. A. (2014) · Comprehensive Physiology · doi:10.1002/cphy.c130055 · Cited by 541 · see citing works
The microbiome: a key regulator of stress and neuroinflammation
Rea, K., Dinan, T. G., & Cryan, J. F. (2016) · Neurobiology of Stress · doi:10.1016/j.ynstr.2016.03.001 · Cited by 508 · see citing works
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Microbiota-gut-brain axis: Modulator of host metabolism and appetite
van de Wouw, M., Schellekens, H., Dinan, T. G., & Cryan, J. F. (2017) · The Journal of Nutrition · doi:10.3945/jn.116.240481 · Cited by 461 · see citing works
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<scp>B</scp> ifidobacteria exert strain‐specific effects on stress‐related behavior and physiology in <scp>BALB</scp> /c mice
Savignac, H. M., Kiely, B., Dinan, T. G., & Cryan, J. F. (2014) · Neurogastroenterology & Motility · doi:10.1111/nmo.12427 · Cited by 418 · see citing works
Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis
Rusch, J. A., Layden, B. T., & Dugas, L. R. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1130689 · Cited by 415 · see citing works
The gut microbiome and diet in psychiatry: focus on depression
Dash, S., Clarke, G., Berk, M., & Jacka, F. N. (2015) · Current Opinion in Psychiatry · doi:10.1097/yco.0000000000000117 · Cited by 369 · see citing works
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Probiotics and the microbiota-gut-brain axis: Focus on psychiatry
Mörkl, S., Butler, M. I., Holl, A., Cryan, J. F., & Dinan, T. G. (2020) · Current Nutrition Reports · doi:10.1007/s13668-020-00313-5 · Cited by 337 · see citing works
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The neuroendocrinology of the microbiota-gut-brain axis: a behavioural perspective
Cussotto, S., Sandhu, K. V., Dinan, T. G., & Cryan, J. F. (2018) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2018.04.002 · Cited by 326 · see citing works
Gut reactions: Breaking down xenobiotic–microbiome interactions
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Modulation of Gut Microbiota–Brain Axis by Probiotics, Prebiotics, and Diet
Liu, X., Cao, S., & Zhang, X. (2015) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.5b02404 · Cited by 304 · see citing works
Microbiota regulation of the mammalian gut-brain axis
Burokas, A., Moloney, R. D., Dinan, T. G., & Cryan, J. F. (2015) · Advances in applied microbiology · doi:10.1016/bs.aambs.2015.02.001 · Cited by 300 · see citing works
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Interplay between the gut-brain axis, obesity and cognitive function
Agustí, A., García-Pardo, M. P., López-Almela, I., Campillo, I., Maes, M., Romaní-Pérez, M., & Sanz, Y. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00155 · Cited by 294 · see citing works
Disturbance of the gut microbiota in early-life selectively affects visceral pain in adulthood without impacting cognitive or anxiety-related behaviors in male rats
O’Mahony, S. M., Felice, V. D., Nally, K., Savignac, H. M., Claesson, M. J., Scully, P., Woznicki, J., Hyland, N. P., Shanahan, F., Quigley, E. M., et al. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.07.054 · Cited by 272 · see citing works
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Cross talk: the microbiota and neurodevelopmental disorders
Kelly, J. R., Minuto, C., Cryan, J. F., Clarke, G., & Dinan, T. G. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00490 · Cited by 271 · see citing works
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Alteration of behavior and monoamine levels attributable to Lactobacillus plantarum PS128 in germ-free mice
Liu, W.-H., Chuang, H.-L., Huang, Y.-T., Wu, C.-C., Chou, G.-T., Wang, S., & Tsai, Y.-C. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.10.046 · Cited by 269 · see citing works
N-3 Polyunsaturated Fatty Acids (PUFAs) Reverse the Impact of Early-Life Stress on the Gut Microbiota
Pusceddu, M. M., El Aidy, S., Crispie, F., O’Sullivan, O., Cotter, P., Stanton, C., Kelly, P., Cryan, J. F., & Dinan, T. G. (2015) · PLOS ONE · doi:10.1371/journal.pone.0139721 · Cited by 214 · see citing works
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Early-life adversity and brain development: Is the microbiome a missing piece of the puzzle?
O’Mahony, S. M., Clarke, G., Dinan, T. G., & Cryan, J. F. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2015.09.068 · Cited by 203 · see citing works
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Gastrointestinal inflammation by gut microbiota disturbance induces memory impairment in mice
Jang, S.-E., Lim, S.-M., Jeong, J.-J., Jang, H.-M., Lee, H.-J., Han, M. J., & Kim, D.-H. (2018) · Mucosal Immunology · doi:10.1038/mi.2017.49 · Cited by 190 · see citing works
Brain structure and response to emotional stimuli as related to gut microbial profiles in healthy women
Tillisch, K., Mayer, E. A., Gupta, A., Gill, Z., Brazeilles, R., Le Nevé, B., van Hylckama Vlieg, J. E. T., Guyonnet, D., Derrien, M., & Labus, J. S. (2017) · Psychosomatic Medicine · doi:10.1097/psy.0000000000000493 · Cited by 185 · see citing works
Role of gut microbiota in functional constipation
Zhang, S., Wang, R., Li, D., Zhao, L., & Zhu, L. (2021) · Gastroenterology Report · doi:10.1093/gastro/goab035 · Cited by 175 · see citing works
The gut microbiome and mental health: implications for anxiety- and trauma-related disorders
Malan-Muller, S., Valles-Colomer, M., Raes, J., Lowry, C. A., Seedat, S., & Hemmings, S. M. J. (2018) · OMICS: A Journal of Integrative Biology · doi:10.1089/omi.2017.0077 · Cited by 161 · see citing works
Gutted! Unraveling the Role of the Microbiome in Major Depressive Disorder
Bastiaanssen, T. F. S., Cussotto, S., Claesson, M. J., Clarke, G., Dinan, T. G., & Cryan, J. F. (2020) · Harvard Review of Psychiatry · doi:10.1097/hrp.0000000000000243 · Cited by 159 · see citing works
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Identification of a Signaling Mechanism by Which the Microbiome Regulates Th17 Cell-Mediated Depressive-Like Behaviors in Mice
Medina-Rodriguez, E. M., Madorma, D., O’Connor, G., Mason, B. L., Han, D., Deo, S. K., Oppenheimer, M., Nemeroff, C. B., Trivedi, M. H., Daunert, S., et al. (2020) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2020.19090960 · Cited by 110 · see citing works
Feeding melancholic microbes: MyNewGut recommendations on diet and mood
Dinan, T. G., Stanton, C., Long-Smith, C., Kennedy, P., Cryan, J. F., Cowan, C. S. M., Cenit, M. C., van der Kamp, J.-W., & Sanz, Y. (2019) · Clinical Nutrition · doi:10.1016/j.clnu.2018.11.010 · Cited by 95 · see citing works
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Of microbes and minds: A narrative review on the second brain aging
Calvani, R., Picca, A., Lo Monaco, M. R., Landi, F., Bernabei, R., & Marzetti, E. (2018) · Frontiers in Medicine · doi:10.3389/fmed.2018.00053 · Cited by 92 · see citing works
Exploration of the association between dietary fiber intake and depressive symptoms in adults
Xu, H., Li, S., Song, X., Li, Z., & Zhang, D. (2018) · Nutrition · doi:10.1016/j.nut.2018.03.009 · Cited by 76 · see citing works
Resilience priming: Translational models for understanding resiliency and adaptation to early life adversity
Kentner, A. C., Cryan, J. F., & Brummelte, S. (2019) · Developmental Psychobiology · doi:10.1002/dev.21775 · Cited by 64 · see citing works
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Proteomic analysis of olfactory bulb suggests CACNA1E as a promoter of CREB signaling in microbiota-induced depression
Huang, C., Yang, X., Zeng, B., Zeng, L., Gong, X., Zhou, C., Xia, J., Lian, B., Qin, Y., Yang, L., et al. (2019) · Journal of Proteomics · doi:10.1016/j.jprot.2018.11.023 · Cited by 54 · see citing works
Daily Interpersonal Stress, Sleep Duration, and Gene Regulation during Late Adolescence
Chiang, J. J., Cole, S. W., Bower, J. E., Irwin, M. R., Taylor, S. E., Arevalo, J., & Fuligni, A. J. (2019) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.11.026 · Cited by 44 · see citing works
Biological underpinnings from psychosocial stress towards appetite and obesity during youth: research implications towards metagenomics, epigenomics and metabolomics
Michels, N. (2019) · Nutrition Research Reviews · doi:10.1017/s0954422419000143 · Cited by 35 · see citing works
Potential lineage transmission within the active microbiota of the eggs and the nauplii of the shrimp Litopenaeus stylirostris : possible influence of the rearing water and more
Giraud, C., Callac, N., Beauvais, M., Mailliez, J.-R., Ansquer, D., Selmaoui-Folcher, N., Pham, D., Wabete, N., & Boulo, V. (2021) · PeerJ · doi:10.7717/peerj.12241 · Cited by 23 · see citing works
Absence of gut microbial colonization attenuates the sympathoadrenal response to hypoglycemic stress in mice: implications for human neonates
Giri, P., Hu, F., La Gamma, E. F., & Nankova, B. B. (2019) · Pediatric Research · doi:10.1038/s41390-018-0270-y · Cited by 15 · see citing works
Genome to Phenome: A Systems Biology Approach to PTSD Using an Animal Model
Chakraborty, N., Meyerhoff, J., Jett, M., & Hammamieh, R. (2017) · Methods in Molecular Biology · doi:10.1007/978-1-4939-6952-4_6 · Cited by 14 · see citing works

Gut hormones in microbiota-gut-brain cross-talk
Sun, L.-J., Li, J.-N., & Nie, Y.-Z. (2020) · Chinese Medical Journal · doi:10.1097/cm9.0000000000000706 · Cited by 145 · see citing works
The potential of human milk oligosaccharides to impact the microbiota-gut-brain axis through modulation of the gut microbiota
Al-Khafaji, A. H., Jepsen, S. D., Christensen, K. R., & Vigsnæs, L. K. (2020) · Journal of Functional Foods · doi:10.1016/j.jff.2020.104176 · Cited by 59 · see citing works
The role of gut microbiota in the gut-brain axis: current challenges and perspectives
Chen, X., D’Souza, R., & Hong, S. (2013) · Protein & Cell · doi:10.1007/s13238-013-3017-x · Cited by 153 · see citing works
The Role of the Gut Microbiota in the Gut–Brain Axis in Obesity: Mechanisms and Future Implications
van Son, J., Koekkoek, L. L., la Fleur, S. E., Serlie, M. J. M., & Nieuwdorp, M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22062993 · Cited by 82 · see citing works
Role of gut microbiota via the gut-liver-brain axis in digestive diseases
Ding, J., Jin, Z., Yang, X., Lou, J., Shan, W., Hu, Y., Du, Q., Liao, Q., Xie, R., & Xu, J. (2020) · World Journal of Gastroenterology · doi:10.3748/wjg.v26.i40.6141 · Cited by 172 · see citing works

Authors: Moloney, R. D., Desbonnet, L., Clarke, G., Dinan, T. G., & Cryan, J. F.
Affiliations: University College Cork (IE)
Corresponding author: Cryan, John F.
ORCID: Moloney, Rachel D.
Desbonnet, Lieve
Clarke, Gerard
Dinan, Timothy G.
Cryan, John F.
Venue: Mammalian Genome
Publisher: Springer Science and Business Media LLC
Published: 2013-11-27
Volume: 25
Issue: 1-2
Pages: 49-74
ISSN: 0938-8990 (ISSN-L)
1432-1777
DOI: 10.1007/s00335-013-9488-5
OpenAlex: W2031136972
Cited by: 430
References: 222
Citations by year: 2026: 23 · 2025: 26 · 2024: 22 · 2023: 18 · 2022: 39 · 2021: 32 · 2020: 49 · 2019: 56 · 2018: 37 · 2017: 43 · 2016: 33 · 2015: 31 · 2014: 20 · 2013: 1
FWCI: 2.66
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Mammalian Genome (publishedVersion)
PubMed (publishedVersion)
ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (submittedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Keywords: gut microbiota, stress, central nervous system, postnatal development, immune system, endocrine system, stress system, mood, cognition, pain, obesity, probiotics, antibiotics, germ-free animals, bacterial infection, central nervous system disorders, therapeutics
MeSH terms: Animals, Behavior, Mental Disorders, Brain, Humans, Stress, Physiological, Stress, Psychological, Signal Transduction, Gastrointestinal Tract, Microbiota

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