Dataset Information

Gill developmental program in the teleost mandibular arch.

ABSTRACT: Whereas no known living vertebrate possesses gills derived from the jaw-forming mandibular arch, it has been proposed that the jaw arose through modifications of an ancestral mandibular gill. Here, we show that the zebrafish pseudobranch, which regulates blood pressure in the eye, develops from mandibular arch mesenchyme and first pouch epithelia and shares gene expression, enhancer utilization, and developmental gata3 dependence with the gills. Combined with work in chondrichthyans, our findings in a teleost fish point to the presence of a mandibular pseudobranch with serial homology to gills in the last common ancestor of jawed vertebrates, consistent with a gill origin of vertebrate jaws.

SUBMITTER: Thiruppathy M

PROVIDER: S-EPMC9239679 | biostudies-literature | 2022 Jun

REPOSITORIES: biostudies-literature

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Gill developmental program in the teleost mandibular arch.

Thiruppathy Mathi M Fabian Peter P Gillis J Andrew JA Crump J Gage JG

eLife 20220628

Whereas no known living vertebrate possesses gills derived from the jaw-forming mandibular arch, it has been proposed that the jaw arose through modifications of an ancestral mandibular gill. Here, we show that the zebrafish pseudobranch, which regulates blood pressure in the eye, develops from mandibular arch mesenchyme and first pouch epithelia and shares gene expression, enhancer utilization, and developmental <i>gata3</i> dependence with the gills. Combined with work in chondrichthyans, our ...[more]

PMID: 35762575

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Project description:Recent advances in sequencing methods have greatly expanded the knowledge of teleost-associated microorganisms. While fish-gut microbiomes are comparatively well studied, less attention has gone toward other, external organ-microbiome associations. Gills are particularly interesting to investigate due to their functions in gas exchange, osmoregulation, and nitrogen excretion. We recently discovered a branchial symbiosis between nitrogen-cycling bacteria and teleosts (zebrafish and carp), in which ammonia-oxidizing Nitrosomonas and denitrifying bacteria together convert toxic ammonia excreted by the fish into harmless dinitrogen (N2) gas. This symbiosis can function as a "natural biofilter" in fish gills and can potentially occur in all ammonotelic fish species, but it remains unknown how widespread this symbiosis is. In this study, we analyzed all publicly available gill microbiome data sets and checked for the presence of Nitrosomonas. We discovered that more than half of the described fish gill microbiomes contain 16S rRNA gene sequences of ammonia-oxidizing bacteria (AOB). The presence of gill-specific AOB was shown in both wild and aquacultured fish, as well as in marine and freshwater fish species. Based on these findings, we propose that ammonia oxidizers are widespread in teleost fish gills. These gill-associated AOB can significantly affect fish nitrogen excretion, and the widespread nature of this association suggests that the gill-associated AOB can have similar impacts on more fish species. Future research should address the contribution of these microorganisms to fish nitrogen metabolism and the fundamental characteristics of this novel symbiosis.IMPORTANCERecent advances in sequencing have increased our knowledge of teleost-associated microbiota, but the gill microbiome has received comparatively little attention. We recently discovered a consortium of nitrogen-cycling bacteria in the gills of common carp and zebrafish, which are able to convert (toxic) ammonia into harmless dinitrogen gas. These microorganisms thus function as a natural nitrogen biofilter. We analyzed all available gill microbiome data sets to determine how widespread gill-associated ammonia-oxidizing bacteria (AOB) are. More than half of the data sets contained AOB, representing both aquacultured and wild fish from freshwater and marine habitats. In total, 182 amplicon sequencing variants were obtained, of which 115 were found specifically in the gills and not the environmental microbiomes. As gill-associated AOB are apparently widespread in teleost fish, it is important to study their impact on host nitrogen excretion and the potential to reduce ammonia accumulation in (recirculating) aquaculture of relevant fish species.

Dataset Information

Gill developmental program in the teleost mandibular arch.

Publications

Gill developmental program in the teleost mandibular arch.

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