Probiotic modulation of the microbiota-gut-brain axis and behaviour in zebrafish

Borrelli, Luca; Aceto, Serena; Agnisola, Claudio; Paolo, Sofia De; Dipineto, Ludovico; Stilling, Roman M.; Dinan, Timothy G.; Cryan, John F.; Menna, Lucia Francesca; Fioretti, Alessandro

doi:10.1038/srep30046

Cited by 172 publications

(158 citation statements)

References 67 publications

(102 reference statements)

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“…Indeed, the crosstalk between the gut and brain is predominately influenced by the gut bacteria67891011. It is well established that an imbalance in gut microbiota can cause an abnormal gut-microbiota-brain axis resulting in several neurological and psychiatric diseases6737.…”

Section: Discussionmentioning

confidence: 99%

“…Accumulating evidence suggests that the brain acts on gastrointestinal and immune functions that have inherent assistance in shaping the gut’s microbial composition89 and that gut microbes could affect host brain functions by producing and secreting substances consisting of neurotransmitters and metabolites101112. Recent advancements in the alleviation of psychiatric diseases by optimizing the composition of the gut microbiota have attracted attention1314.…”

mentioning

confidence: 99%

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Bifidobacterium in the gut microbiota confer resilience to chronic social defeat stress in mice

Yang

Fujita

Ren

et al. 2017

Sci Rep

146

104

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Accumulating evidence suggests that abnormalities in the composition of the gut microbiota may play a role in the pathogenesis of depression. Although approximately 30% mice are resilient to chronic social defeat stress (CSDS), the role of gut microbiota in this stress resilience is unknown. In this study, male C57BL/6 mice were exposed to a different CD1 aggressor mouse for 10 min on 10 consecutive days. A social interaction test was applied to distinguish between resilient and susceptible mice. Using 16S rRNA analysis, we examined the composition of gut microbiota in feces from control, resilient, and susceptible mice. The marked appearance of Bifidobacterium was detected in the resilient mice, whereas in the control and susceptible mice, Bifidobacterium were below the detection limit. Oral intake of Bifidobacterium significantly increased the number of resilient mice after CSDS compared with vehicle-treated mice. These findings suggest that Bifidobacterium may confer resilience to CSDS. Therefore, supplementation of Bifidobacterium may prevent the onset of depression from stress in humans. In addition, supplementation of Bifidobacterium may prevent or minimize relapse from remission induced by inflammation and/or stress in depressed patients.

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Bifidobacterium in the gut microbiota confer resilience to chronic social defeat stress in mice

Yang

Fujita

Ren

et al. 2017

Sci Rep

146

104

View full text Add to dashboard Cite

show abstract

“…Given the current interest on the gut-brain axis as a primary subject in the “start”of neurodegenerative disorders, such as Parkinson’s disease [39,40,73] and also the importance of microbiota in the gut-brain axis and serotonergic control [74], our research focused on and provides new information on crop contraction mechanisms (as a part of the gut) and the serotonergic control in this fly. In particular, our results point to a double brain-gut serotonergic circuitry, thus suggesting that not only the brain can affect gut functions, but the gut can also affect the central nervous system.…”

Section: Discussionmentioning

confidence: 99%

Opposite effects of 5-HT/AKH and octopamine on the crop contractions in adult Drosophila melanogaster: Evidence of a double brain-gut serotonergic circuitry

et al. 2017

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This study showed that in adult Drosophila melanogaster, the type of sugar—either present within the crop lumen or in the bathing solution of the crop—had no effect on crop muscle contraction. What is important, however, is the volume within the crop lumen. Electrophysiological recordings demonstrated that exogenous applications of serotonin on crop muscles increases both the amplitude and the frequency of crop contraction rate, while adipokinetic hormone mainly enhances the crop contraction frequency. Conversely, octopamine virtually silenced the overall crop activity. The present study reports for the first time an analysis of serotonin effects along the gut-brain axis in adult D. melanogaster. Injection of serotonin into the brain between the interocellar area shows that brain applications of serotonin decrease the frequency of crop activity. Based on our results, we propose that there are two different, opposite pathways for crop motility control governed by serotonin: excitatory when added in the abdomen (i.e., directly bathing the crop) and inhibitory when supplied within the brain (i.e., by injection). Finally, our results point to a double brain-gut serotonergic circuitry suggesting that not only the brain can affect gut functions, but the gut can also affect the central nervous system. On the basis of our results, and data in the literature, a possible mechanism for these two discrete serotonergic functions is suggested.

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“…Borrelli et al. () found similar increases in Firmicutes after 28 days of treatment in adult animals. Importantly, adult zebrafish treated with L. rhamnosus IMC 501 displayed less shoaling and increased brain‐derived neurotrophic factor (bdnf), mRNA in the brain, with upregulation of genes involved in the serotonergic system in the brain (tph1a, tph1b, tph2, htr1aa, slc6a4a and mao) and gut (tph1a; Borrelli et al., ).…”

Section: The Usefulness Of Fish Models To Study Microbiome–behaviour mentioning

confidence: 71%

Using fish models to investigate the links between microbiome and social behaviour: The next step for translational microbiome research?

et al. 2019

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Recent research has revealed surprisingly important connections between animals’ microbiome and social behaviour. Social interactions can affect the composition and function of the microbiome; conversely, the microbiome affects social communication by influencing the hosts’ central nervous system and peripheral chemical communication. These discoveries set the stage for novel research focusing on the evolution and physiology of animal social behaviour in relation to microbial transmission strategies. Here, we discuss the emerging roles of teleost fish models and their potential for advancing research fields, linked to sociality and microbial regulation. We argue that fish models, such as the zebrafish (Danio rerio, Cyprinidae), sticklebacks (‎Gasterosteidae), guppies (Poeciliidae) and cleaner–client dyads (e.g., obligate cleaner fish from the Labridae and Gobiidae families and their visiting clientele), will provide valuable insights into the roles of microbiome in shaping social behaviour and vice versa, while also being of direct relevance to the food and ornamental fish trades. The diversity of fish behaviour warrants more interdisciplinary research, including microbiome studies, which should have a strong ecological (field‐derived) approach, together with laboratory‐based cognitive and neurobiological experimentation. The implications of such integrated approaches may be of translational relevance, opening new avenues for future investigation using fish models.

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Probiotic modulation of the microbiota-gut-brain axis and behaviour in zebrafish

Cited by 172 publications

References 67 publications

Bifidobacterium in the gut microbiota confer resilience to chronic social defeat stress in mice

Bifidobacterium in the gut microbiota confer resilience to chronic social defeat stress in mice

Opposite effects of 5-HT/AKH and octopamine on the crop contractions in adult Drosophila melanogaster: Evidence of a double brain-gut serotonergic circuitry

Using fish models to investigate the links between microbiome and social behaviour: The next step for translational microbiome research?

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