Commensal Microbiota Regulate Vertebrate Innate Immunity-Insights From the Zebrafish

Abstract

Microbial communities populate the mucosal surfaces of all animals. Metazoans have co-evolved with these microorganisms, forming symbioses that affect the molecular and cellular underpinnings of animal physiology. These microorganisms, collectively referred to as the microbiota, are found on many distinct body sites (including the skin, nasal cavity, and urogenital tract), however the most densely colonized host tissue is the intestinal tract. Although spatially confined within the intestinal lumen, the microbiota and associated products shape the development and function of the host immune system. Studies comparing gnotobiotic animals devoid of any microbes (germ free) with counterparts colonized with selected microbial communities have demonstrated that commensal microorganisms are required for the proper development and function of the immune system at homeostasis and following infectious challenge or injury. Animal model systems have been essential for defining microbiota-dependent shifts in innate immune cell function and intestinal physiology during infection and disease. In particular, the zebrafish has emerged as a powerful vertebrate model organism with unparalleled capacity for in vivo imaging, a full complement of genetic approaches, and facile methods to experimentally manipulate microbial communities. Here we review key insights afforded by the zebrafish into the impact of microbiota on innate immunity, including evidence that the perception of and response to the microbiota is evolutionarily conserved. We also highlight opportunities to strengthen the zebrafish model system, and to gain new insights into microbiota-innate immune interactions that would be difficult to achieve in mammalian models.

The relationship between the gut microbiome and host gene expression: a review

“…While we highlight mouse models above, many additional organisms serve as powerful laboratory systems to reveal insights into the relationship between the microbiome and host transcription. Studies conducted in zebrafish (Murdoch and Rawls 2019), C. elegans (Dirksen et al 2020;Yang et al 2019), and Drosophila melanogaster (Broderick et al 2014;Douglas 2018;Elya et al 2016) for example, all have revealed the impact of the microbiome on immunity, metabolism, and developmental gene regulation.…”

QTL Mapping of Intestinal Neutrophil Variation in Threespine Stickleback Reveals Possible Gene Targets Connecting Intestinal Inflammation and Systemic Health

“…These cells exist throughout the body and are recruited from the blood stream to sites of inflammation, including the gut (Borregaard 2010;Fournier and Parkos 2012;Wera et al 2016). While intestinal neutrophil recruitment often occurs due to the presence of pathogens, resulting from acute inflammation, such recruitment can also occur chronically due to aberrant interactions between the immune system and the gut microbiota (Foell et al 2003;Wera et al 2016;Mortaz et al 2018;Rosales 2018;Murdoch and Rawls 2019).…”

Microbiota Modulates the Immunomodulatory Effects of Filifolinone on Atlantic Salmon

“…If a similar mechanism exists in fish, it can be supposed that intramuscular filifolinone can modify microbiota by being excreted to the gastrointestinal tract. Although there is no report that directly addresses the role of microbiota in the Atlantic salmon immune system, an experiment with gnotobiotic zebrafish showed that microbiota is necessary to induce the expression of more than 200 genes related to innate immunity [ 63 , 64 ]. Moreover, experiments using probiotics have shown that yeast and lactic acid bacteria can improve the function of the Atlantic salmon immune system [ 65 , 66 , 67 ] and other fish [ 68 ].…”