Cell-type-specific responses to the microbiota across all tissues of the larval zebrafish

Massaquoi, Michelle S.; Kong, Garth; Chilin‐Fuentes, Daisy R.; Ngo, Julia; Horve, Patrick F.; Melançon, Ellie; Hamilton, M. Kristina; Eisen, Judith S; Guillemin, Karen

doi:10.1016/j.celrep.2023.112095

Cited by 5 publications

(3 citation statements)

References 87 publications

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“…As such, it is important to provide a timely overview of the GRN underlying zebrafish enteric neuron development, which I have synthesized from numerous studies and depicted using the GRN Biotapestry model [ 78 ] ( Figure 2 ). Additionally, many recent transcriptomic studies have expanded our knowledge of the genes expressed within developing zebrafish ENS cells [ 36 , 40–42 , 79 , 80 ]. Looking to the future, it will be essential to validate connections between gene nodes within the GRN and incorporate how other newly discovered factors affect ENS ontogenesis.…”

Section: Discussionmentioning

confidence: 99%

Genetic regulation of enteric nervous system development in zebrafish

Uribe

2024

Biochemical Society Transactions

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The enteric nervous system (ENS) is a complex series of interconnected neurons and glia that reside within and along the entire length of the gastrointestinal tract. ENS functions are vital to gut homeostasis and digestion, including local control of peristalsis, water balance, and intestinal cell barrier function. How the ENS develops during embryological development is a topic of great concern, as defects in ENS development can result in various diseases, the most common being Hirschsprung disease, in which variable regions of the infant gut lack ENS, with the distal colon most affected. Deciphering how the ENS forms from its progenitor cells, enteric neural crest cells, is an active area of research across various animal models. The vertebrate animal model, zebrafish, has been increasingly leveraged to understand early ENS formation, and over the past 20 years has contributed to our knowledge of the genetic regulation that underlies enteric development. In this review, I summarize our knowledge regarding the genetic regulation of zebrafish enteric neuronal development, and based on the most current literature, present a gene regulatory network inferred to underlie its construction. I also provide perspectives on areas for future zebrafish ENS research.

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Section: Discussionmentioning

confidence: 99%

Genetic regulation of enteric nervous system development in zebrafish

Uribe

2024

Biochemical Society Transactions

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“…Many of these pathways have been studied previously in the context of microbial regulation during post-embryonic development, including calcium and neurotransmitter signaling, synaptic plasticity, visual development, axonogenesis, and HPA/HPI axis activation (Davis et al, 2016; Heijtz et al, 2011; Kaur et al, 2023; Massaquoi et al, 2023; Rea et al, 2022; Vuong et al, 2020). However, less is known regarding the microbial regulation of these pathways during embryonic development.…”

Section: Discussionmentioning

confidence: 99%

The External Microbiome Communicates with the Developing Zebrafish (Danio rerio) Embryo Through the Protective Chorion and Influences Developmental Trajectory

Green,

Harishchandra,

Ranasinghe

et al. 2024

Preprint

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The commensal microbiome plays a significant role in shaping host physiological processes including energy metabolism and neurobiology. However, current knowledge on host-microbiome interactions is limited to effects of the microbiome during post-embryonic development. Elucidating mechanisms and consequences of host-microbe communication during embryonic development, particularly in oviparous organisms is a notable gap. Protected from the chorionic fluid and considered to be sterile, embryonic development in oviparous organisms is typically considered to be independent of the influence of the microbiome. Here, we tested the hypothesis that the external microbiome influences embryonic development in oviparous organisms despite lack of physical contact. We utilized zebrafish (Danio rerio) reared germ-free (GF) and conventionalized with microbes (CV) at different times during embryonic development to examine changes in the embryonic transcriptome, proteome, and physiology during embryogenesis at 32 hours post-fertilization. Our results contrast the conventional notion that zebrafish embryos are shielded from the external microbial environment by their protective chorion until hatching. We demonstrate the external microbial community influences embryonic transcript and protein abundance associated with critical developmental processes including energy metabolism and neurodevelopment. While these pathways are previously identified to be influence by microbes duringpost-embryonic stages, here, we reveal a significant role of the surrounding aquatic microbial community in regulating these processes as early as embryogenesis. Furthermore, we demonstrate the external microbial community differentially regulates cytochrome P450 driven xenobiotic metabolism and associated bioenergetic and behavioral responses following exposure to a CYP1A activator during embryogenesis. These findings transform our interpretation and consideration of embryonic development as a function of microbial cues and genetic blueprints, enhance knowledge of fundamental processes governing vertebrate embryonic development, and expand comprehension of host-microbe communication.

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“…Recent scRNA-seq studies suggested that the gut microbiome affects the transcriptome of LREs and other ileal cell types in zebrafish by upregulating expression of immune markers ( Willms et al 2022 ; Massaquoi et al 2023 ; Jones et al 2023 ). Our dataset also showed that microbes upregulated expression of immune markers in LREs.…”

Section: Discussionmentioning

confidence: 99%

Protein absorption in the zebrafish gut is regulated by interactions between lysosome rich enterocytes and the microbiome

Childers,

Park,

Wang

et al. 2024

Preprint

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Dietary protein absorption in neonatal mammals and fishes relies on the function of a specialized and conserved population of highly absorptive lysosome rich enterocytes (LREs). The gut microbiome has been shown to enhance absorption of nutrients, such as lipids, by intestinal epithelial cells. However, whether protein absorption is also affected by the gut microbiome is poorly understood. Here, we investigate connections between protein absorption and microbes in the zebrafish gut. Using live microscopy-based quantitative assays, we find that microbes slow the pace of protein uptake and degradation in LREs. While microbes do not affect the number of absorbing LRE cells, microbes lower the expression of endocytic and protein digestion machinery in LREs. Using transgene assisted cell isolation and single cell RNA-sequencing, we characterize all intestinal cells that take up dietary protein. We find that microbes affect expression of bacteria-sensing and metabolic pathways in LREs, and that some secretory cell types also take up protein and share components of protein uptake and digestion machinery with LREs. Using custom-formulated diets, we investigated the influence of diet and LRE activity on the gut microbiome. Impaired protein uptake activity in LREs, along with a protein-deficient diet, alters the microbial community and leads to increased abundance of bacterial genera that have the capacity to reduce protein uptake in LREs. Together, these results reveal that diet-dependent reciprocal interactions between LREs and the gut microbiome regulate protein absorption.

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Cell-type-specific responses to the microbiota across all tissues of the larval zebrafish

Cited by 5 publications

References 87 publications

Genetic regulation of enteric nervous system development in zebrafish

Genetic regulation of enteric nervous system development in zebrafish

The External Microbiome Communicates with the Developing Zebrafish (Danio rerio) Embryo Through the Protective Chorion and Influences Developmental Trajectory

Protein absorption in the zebrafish gut is regulated by interactions between lysosome rich enterocytes and the microbiome

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