Gut microbiome remodeling induces depressive-like behaviors through a pathway mediated by the host’s metabolism
Abstract
Major depressive disorder (MDD) is the result of complex gene-environment interactions. According to the World Health Organization, MDD is the leading cause of disability worldwide, and it is a major contributor to the overall global burden of disease. However, the definitive environmental mechanisms underlying the pathophysiology of MDD remain elusive. The gut microbiome is an increasingly recognized environmental factor that can shape the brain through the microbiota-gut-brain axis. We show here that the absence of gut microbiota in germ-free (GF) mice resulted in decreased immobility time in the forced swimming test relative to conventionally raised healthy control mice. Moreover, from clinical sampling, the gut microbiotic compositions of MDD patients and healthy controls were significantly different with MDD patients characterized by significant changes in the relative abundance of Firmicutes, Actinobacteria and Bacteroidetes. Fecal microbiota transplantation of GF mice with 'depression microbiota' derived from MDD patients resulted in depression-like behaviors compared with colonization with 'healthy microbiota' derived from healthy control individuals. Mice harboring 'depression microbiota' primarily exhibited disturbances of microbial genes and host metabolites involved in carbohydrate and amino acid metabolism. This study demonstrates that dysbiosis of the gut microbiome may have a causal role in the development of depressive-like behaviors, in a pathway that is mediated through the host's metabolism.
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These taxa may interface with conserved aspects of mammalian neurophysiology.
“These associations also exist in human clinical populations—for example, members of the Lachnospiraceae are frequently associated with diagnoses of major depressive disorder across studies60–63—suggesting that these taxa may interface with conserved aspects of mammalian neurophysiology.”
From Integrated analysis of behavioral, epigenetic, and gut microbiome analyses in AppNL-G-F, AppNL-F, and wild type mice (2021) · cites this paper as [61]
Members of the Lachnospiraceae are frequently associated with diagnoses of major depressive disorder across studies.
“These associations also exist in human clinical populations—for example, members of the Lachnospiraceae are frequently associated with diagnoses of major depressive disorder across studies60–63—suggesting that these taxa may interface with conserved aspects of mammalian neurophysiology.”
From Integrated analysis of behavioral, epigenetic, and gut microbiome analyses in AppNL-G-F, AppNL-F, and wild type mice (2021) · cites this paper as [61]
Differences in the composition of the gut microbiota in patients with depression compared with healthy individuals have been demonstrated.
“Differences in the composition of the gut microbiota in patients with depression compared with healthy individuals have been demonstrated (134).”
From Vagus Nerve as Modulator of the Brain–Gut Axis in Psychiatric and Inflammatory Disorders (2018) · cites this paper as [134]
Alteration of composition of bacterial communities in the gut caused by different stress has the potential to affect various metabolic pathways which may be involved in the development of depressive states.
“It is widely accepted that the alteration of composition of bacterial communities in the gut caused by different stress have the potential to affect various metabolic pathways which may be involved in the development of depressive states [96,97].”
From Circular RNAs in depression: Biogenesis, function, expression, and therapeutic potential (2021) · cites this paper as [96]
Gut microbiota can also influence neural metabolism.
“Recent work indicates gut microbiota can also influence neural metabolism [198].”
From The molecular and cellular mechanisms of depression: a focus on reward circuitry (2019) · cites this paper as [198]
Psychiatric and neurodevelopmental illnesses, including major depressive disorder, autism spectrum disorder, and multiple sclerosis, are consistently associated with a state of dysbiosis.
“Psychiatric and neurodevelopmental illnesses, including major depressive disorder [49,50], autism spectrum disorder [51], and multiple sclerosis [26], are consistently associated with a state of dysbiosis.”
Germ-free mice receiving cecal content transplant express behavioral phenotypes that mimic the donors, and mice receiving fecal transplant from patients with major depressive disorder display more depression-like behaviors than those colonized with microbiota from healthy controls.
“Further, germ-free mice receiving cecal content transplant expressed behavioral phenotypes that mimicked the donors [54], and those that had fecal transplant from patients with major depressive disorder also displayed more depression-like behaviors, as compared to those colonized with microbiota from healthy controls [50].”
Absence of microbiota or depletion of microbes by antibiotics in rodents leads to exaggerated HPA axis activation with elevated adrenocorticotrophic hormone and corticosterone levels in response to stress, accompanied by reduced anxiety.
“Absence of microbiota (germ-free [GF] status) or depletion of microbes by antibiotics in rodents leads to exaggerated activation of the HPA axis associated with elevated adrenocorticotrophic hormone and corticosterone levels in response to stress, accompanied with reduced anxiety (Sudo et al., 2004; Zheng et al., 2016; Diaz Heijtz et al., 2011; Huo et al., 2017).”
From Intestinal microbiota modulates adrenomedullary response through Nod1 sensing in chromaffin cells (2021) · cites this paper as Zheng et al., 2016
Patients with MDD have an altered gut microbiome when compared to healthy controls.
“There have been a number of recent studies demonstrating that patients with MDD have an altered gut microbiome when compared to healthy controls [62, 63]”
From Role of diet and its effects on the gut microbiome in the pathophysiology of mental disorders (2022) · cites this paper as [63]
The nature of dysbiosis in MDD varies across studies, no consistent microbial biomarker has been identified, and causality between gut dysbiosis and clinical symptoms of depression has not been established.
“although the nature of the dysbiosis in each of the studies varies, has not identified a consistent microbial biomarker, and causality between gut dysbiosis and clinical symptoms of depression has not been established.”
From Role of diet and its effects on the gut microbiome in the pathophysiology of mental disorders (2022) · cites this paper as [63]
The microbiota may play a causal role in the pathophysiology of depression.
“suggesting the possibility of a causal role for the microbiota in the pathophysiology of depression [63, 65].”
From Role of diet and its effects on the gut microbiome in the pathophysiology of mental disorders (2022) · cites this paper as [63]
Transferring the microbiome of a depressed individual into a healthy rodent can induce depressive-like behaviors in the murine recipient.
“Several studies have also shown that transferring the microbiome of a depressed individual into a healthy rodent (without or with suppressed gut microbiota) can induce depressive-like behaviors in the murine recipient”
From Role of diet and its effects on the gut microbiome in the pathophysiology of mental disorders (2022) · cites this paper as [63]
HPA axis and serotonergic system were altered in mice lacking microbiota.
“Previous studies had demonstrated that the HPA axis and serotonergic system were altered in mice lacking microbiota (Sudo et al., 2004; Clarke et al., 2013; Zheng et al., 2016).”
From Intestinal microbiota modulates adrenomedullary response through Nod1 sensing in chromaffin cells (2021) · cites this paper as Zheng et al., 2016
FMT from patients with depression to germ-free mice can result in depression-like behaviour in recipient mice.
“These four studies all support that FMT from patients with depression to GF mice can result in depression-like behaviour in the recipient mice.”
From Effect of fecal microbiota transplant on symptoms of psychiatric disorders: a systematic review (2020) · cites this paper as [35]
Three studies reported no significant differences in microbial diversity.
“While three studies reported no significant differences in microbial diversity [57,70,71], Jiang et al. (2015) reported greater microbial diversity in patients with MDD than in healthy individuals [56].”
From Flavonoid-rich orange juice intake and altered gut microbiome in young adults with depressive symptom: a randomized controlled study (2020) · cites this paper as [70]
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“…pathophysiology of MDD. 301 Because the interaction of bacteria of some taxa in the gut with peripheral in fl ammation with the brain may be related to depression pathophysiology, 302,303 regulating the gut-microbe-brain axis may be a therapeutic and preventive strategy for psychiatric disorders.”
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The gut microbiome and mental health: implications for anxiety- and trauma-related disorders
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Hassan, A. M., Mancano, G., Kashofer, K., Fröhlich, E. E., Matak, A., Mayerhofer, R., Reichmann, F., Olivares, M., Neyrinck, A. M., Delzenne, N. M., et al. (2019) · Nutritional Neuroscience · doi:10.1080/1028415x.2018.1465713 · Cited by 166 · see citing works
- Authors
- Zheng, P., Zeng, B., Zhou, C., Liu, M., Fang, Z., Xu, X., Zeng, L., Chen, J., Fan, S., Du, X., Zhang, X., Yang, D., Yang, Y., Meng, H., Li, W., Melgiri, N. D., Licinio, J., Wei, H., & Xie, P.
- Affiliations
- The Affiliated Yongchuan Hospital of Chongqing Medical University (CN)
- Army Medical University (CN)
- Chongqing Medical University (CN)
- Flinders University (AU)
- Corresponding author
- Licinio, J
- Wei, H
- Xie, P
- ORCID
- Venue
- Molecular Psychiatry
- Published
- 2016-04-12
- Volume
- 21
- Issue
- 6
- Pages
- 786-796
- ISSN
- 1359-4184 (ISSN-L)
- 1476-5578
- OpenAlex
- W2337492846
- Cited by
- 2,023
- References
- 70
- Citations by year
- 2026: 152 · 2025: 221 · 2024: 251 · 2023: 237 · 2022: 262 · 2021: 289 · 2020: 215 · 2019: 172 · 2018: 117 · 2017: 73 · 2016: 29 · 2015: 1 · 2013: 1
- FWCI
- 67.71
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Molecular Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- major depressive disorder, gut microbiota, microbiota-gut-brain axis, germ-free mice, fecal microbiota transplantation, depression-like behavior, dysbiosis, carbohydrate metabolism, amino acid metabolism, host metabolism, Firmicutes, actinobacteria, Bacteroidetes
- MeSH terms
- Gastrointestinal Microbiome, Animals, Depression, Major Depressive Disorder, Humans, Mice, Gene-Environment Interaction, Microbiota, Dysbiosis
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