Microbial colonization is required for normal neurobehavioral development in zebrafish

Phelps, Drake; Brinkman, Nichole E.; Keely, Scott P.; Anneken, Emily M.; Catron, Tara R.; Betancourt, Doris; Wood, Charles E.; Espenschied, Scott T.; Rawls, John F.; Tal, Tamara

doi:10.1038/s41598-017-10517-5

Cited by 103 publications

(96 citation statements)

References 59 publications

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“…Like Vibrio, Aeromonas species are abundant members of the zebrafish intestinal microbiota [35]. Previous studies suggest that these 2 genera naturally compete against one another within complex intestinal communities [39]. In addition, we have shown that Vibrio is capable of invading and displacing established Aeromonas populations in gnotobiotic animals [32].…”

Section: Loss Of Swimming Motility or Chemotaxis Attenuates Intestinamentioning

confidence: 81%

Swimming motility of a gut bacterial symbiont promotes resistance to intestinal expulsion and enhances inflammation

et al. 2020

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Some of the densest microbial ecosystems in nature thrive within the intestines of humans and other animals. To protect mucosal tissues and maintain immune tolerance, animal hosts actively sequester bacteria within the intestinal lumen. In response, numerous bacterial pathogens and pathobionts have evolved strategies to subvert spatial restrictions, thereby undermining immune homeostasis. However, in many cases, it is unclear how escaping host spatial control benefits gut bacteria and how changes in intestinal biogeography are connected to inflammation. A better understanding of these processes could uncover new targets for treating microbiome-mediated inflammatory diseases. To this end, we investigated the spatial organization and dynamics of bacterial populations within the intestine using larval zebrafish and live imaging. We discovered that a proinflammatory Vibrio symbiont native to zebrafish governs its own spatial organization using swimming motility and chemotaxis. Surprisingly, we found that Vibrio's motile behavior does not enhance its growth rate but rather promotes its persistence by enabling it to counter intestinal flow. In contrast, Vibrio mutants lacking motility traits surrender to host spatial control, becoming aggregated and entrapped within the lumen. Consequently, nonmotile and nonchemotactic mutants are susceptible to intestinal expulsion and experience large fluctuations in absolute abundance. Further, we found that motile Vibrio cells induce expression of the proinflammatory cytokine tumor necrosis factor alpha (TNFα) in gut-associated macrophages and the liver. Using inducible genetic switches, we demonstrate that swimming motility can be manipulated in situ to modulate the spatial organization, persistence, and inflammatory activity of gut bacterial populations. Together, our findings suggest that host spatial control over resident microbiota plays a broader role in regulating the abundance and persistence of gut bacteria than simply protecting mucosal tissues. Moreover, we show that intestinal flow and bacterial motility are potential targets for therapeutically managing bacterial spatial organization and inflammatory activity within the gut. PLOS BIOLOGYPLOS Biology | https://doi.

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Section: Loss Of Swimming Motility or Chemotaxis Attenuates Intestinamentioning

confidence: 81%

Swimming motility of a gut bacterial symbiont promotes resistance to intestinal expulsion and enhances inflammation

et al. 2020

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“…Several tumors in humans are strongly associated with pathogenicity of a single bacterium, such as Helicobacter pylori [60], or are likely caused by interactions between two commensal bacteria, like Bacteroides fragilis and Escherichia coli [12]. Additionally, there is an accumulating evidence that commensal bacteria may support tissue homeostasis by, for instance, stimulating neurogenesis [61,62]. These observations point to the evolutionary conserved role of the host-associated bacteria in maintaining host tissue homeostasis.…”

Section: Discussionmentioning

confidence: 99%

Dynamic interactions within the host-associated microbiota cause tumor formation in the basal metazoan Hydra

et al. 2020

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The extent to which disturbances in the resident microbiota can compromise an animal's health is poorly understood. Hydra is one of the evolutionary oldest animals with naturally occurring tumors. Here, we found a causal relationship between an environmental spirochete (Turneriella spec.) and tumorigenesis in Hydra. Unexpectedly, virulence of this pathogen requires the presence of Pseudomonas spec., a member of Hydra´s beneficial microbiome indicating that dynamic interactions between a resident bacterium and a pathogen cause tumor formation. The observation points to the crucial role of commensal bacteria in maintaining tissue homeostasis and adds support to the view that microbial community interactions are essential for disease. These findings in an organism that shares deep evolutionary connections with all animals have implications for our understanding of cancer.

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“…As an alternative, orally administered, non-absorbable antimicrobials have been used to alter the gut microbiome in rodents (neomycin, bacitracin, and pimaricin) [4][5][6] as well as in zebrafish (amphotericin, kanamycin, and ampicillin). 7 Behavioral changes similar to GF animals are reported with oral but not intraperitoneal 4 treatment particularly related to stress-associated and anxiety-associated phenotypes. Oral antibiotics have also been used to examine the contribution of the maternal gut microbiota during pregnancy to offspring behavior by maternal treatment either preconception (non-absorbable sulfonamide) 5 or early in gestation (neomycin, pimaricin, bacitracin).…”

Section: Behavioral Alterations In Animal Modelsmentioning

confidence: 90%

The contribution of the gut microbiome to neurodevelopment and neuropsychiatric disorders

2018

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Bidirectional communication between the gut and brain is well recognized, with data now accruing for a specific role of the gut microbiota in that link, referred to as the microbiome-gut-brain axis. This review will discuss the emerging role of the gut microbiota in brain development and behavior. Animal studies have clearly demonstrated effects of the gut microbiota on gene expression and neurochemical metabolism impacting behavior and performance. Based on these changes, a modulating role of the gut microbiota has been demonstrated for a variety of neuropsychiatric disorders, including depression, anxiety, and movement including Parkinson's, and importantly for the pediatric population autism. Critical developmental windows that influence early behavioral outcomes have been identified that include both the prenatal environment and early postnatal colonization periods. The clearest data regarding the role of the gut microbiota on neurodevelopment and psychiatric disorders is from animal studies; however, human data have begun to emerge, including an association between early colonization patterns and cognition. The importance of understanding the contribution of the gut microbiota to the development and functioning of the nervous system lies in the potential to intervene using novel microbial-based approaches to treating neurologic conditions. While pathways of communication between the gut and brain are well established, the gut microbiome is a new component of this axis. The way in which organisms that live in the gut influence the central nervous system (CNS) and host behavior is likely to be multifactorial in origin. This includes immunologic, endocrine, and metabolic mechanisms, all of which are pathways used for other microbial-host interactions. Germ-free (GF) mice are an important model system for understanding the impact of gut microbes on development and function of the nervous system. Alternative animal model systems have further clarified the role of the gut microbiota, including antibiotic treatment, fecal transplantation, and selective gut colonization with specific microbial organisms. Recently, researchers have started to examine the human host as well. This review will examine the components of the CNS potentially influenced by the gut microbiota, and the mechanisms mediating these effects. Links between gut microbial colonization patterns and host behavior relevant to a pediatric population will be examined, highlighting important developmental windows in utero or early in development.

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Microbial colonization is required for normal neurobehavioral development in zebrafish

Cited by 103 publications

References 59 publications

Swimming motility of a gut bacterial symbiont promotes resistance to intestinal expulsion and enhances inflammation

Swimming motility of a gut bacterial symbiont promotes resistance to intestinal expulsion and enhances inflammation

Dynamic interactions within the host-associated microbiota cause tumor formation in the basal metazoan Hydra

The contribution of the gut microbiome to neurodevelopment and neuropsychiatric disorders

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