Gene family expansion and functional diversification of chitinase and chitin synthase genes in Atlantic salmon (Salmo salar)

Abstract

Background: Chitin is one of the most abundant polysaccharides in nature, forming important structures in insects, crustaceans, and fungal cell walls. Vertebrates on the other hand are generally considered "non-chitinous" organisms, despite having highly conserved chitin metabolism associated genes. Recent work has revealed that the largest group of vertebrates, the teleosts, have the potential to both synthesize and degrade endogenous chitin. Yet little is still known about the genes and proteins responsible for these dynamic processes. Here we used comparative genomics, transcriptomics, and chromatin accessibility data to characterize the repertoire, evolution, and regulation of genes involved in chitin-metabolism in teleosts, with a particular focus on Atlantic salmon. Results: Reconstruction of gene family phylogenies provide evidence for an expansion of teleost and salmonid chitinase and chitin synthase genes after multiple whole-genome duplications. Analyses of multi-tissue gene expression data demonstrated a strong bias of gastrointestinal tract expression for chitin metabolism genes, but with different spatial and temporal tissue specificities. Finally, we integrated transcriptomes from a developmental time series of the gastrointestinal tract with chromatin accessibility data to identify putative transcription factors responsible for regulating chitin-metabolism gene expression (CDX1 and CDX2) as well as tissue-specific divergence in the regulation of gene duplicates (FOXJ2). These transcription factors are also potential regulators of multiple glycosyltransferases being co-expressed with the chitin remodeling genes. Conclusion: The findings presented here add support to the hypothesis that chitin metabolism genes in teleosts play a role in developing and maintaining a chitin-based barrier in the teleost gut and provide a basis for further investigations into the molecular basis of this barrier.

The Salmon Microbial Genome Atlas enables novel insights into bacteria-host interactions via functional mapping

“…Chitin is a common carbohydrate found in the natural diet of Atlantic salmon as a component of the exoskeleton of insects and crustaceans 12 . While Atlantic salmon possess endogenous chitinases that have some level of activity for use and exploitation of this dietary component 44,45 , our findings show that gut Gammaproteobacteria (P. phosphoreum, S. liquefaciens and Pseudomonas) can efficiently degrade chitin in pure culture while in vivo they express chitinases and are inferred as active degraders that contribute towards break-down of this polymer (Fig. 4).…”

“…Chitin is a common carbohydrate found in the natural diet of Atlantic salmon as a component of the exoskeleton of insects and crustaceans 12 . While Atlantic salmon possess endogenous chitinases that have some level of activity for use and exploitation of this dietary component 44,45 , our findings show that gut Gammaproteobacteria (P. phosphoreum, S. liquefaciens and Pseudomonas) can efficiently degrade chitin in pure culture while in vivo they express chitinases and are inferred as active degraders that contribute towards break-down of this polymer (Fig. approach provides a community overview but does not discriminate between metabolically active and inactive populations in the gut (including carry-over of microbial DNA from abundant microbial populations in the feed); as a consequence of this, the observed changes in microbiome composition may not directly translate into functional alterations that impact host's metabolism.…”

The gastric mucosa of Atlantic salmon (Salmo salar) is abundant in highly active chitinases

“…The Atlantic salmon genome encodes 10 chitinase-like genes according to the NCBI RefSeq annotation (GCF_000233375.1; release 100) that all belong to family 18 of the glycoside hydrolases, as classified by the carbohydrate active enzyme (CAZy) database 18 . Three of these chitinase genes (hereby named chia.3, chia.4 , and chia.7 ; proteins named Chia.3, Chia.4, and Chia.7, respectively) have shown stomach-specific expression 17 . The sequence identity of the amino acid sequences of the chitinases range from 60-95% when aligned with each other and 61-65% when aligned with the ortholog human acidic mammalian chitinase, AMCase (Table 1).…”

“…Wild Atlantic salmon ( Salmo salar ) is known to prey on chitinous organisms such amphipods, euphausiids, shrimp, and insects 15,16 and possess 10 genes encoding family GH18 chitinases 17 . A better understanding of the biological functions of these proteins may be of value to the salmon industry as it searches for new, alternative feed sources.…”