Chitin-based barrier immunity and its loss predated mucus-colonization by indigenous gut microbiota

Nakashima, Keisuke; Kimura, Satoshi; Ogawa, Yu; Watanabe, Shinji; Soma, Satoshi; Kaneko, Toyoji; Yamada, Lixy; Sawada, Hitoshi; Tung, Che‐Huang; Lu, Tsai-Ming; Yu, Jr-Kai; Villar‐Briones, Alejandro; Kikuchi, Sakura; Satoh, Noriyuki

doi:10.1038/s41467-018-05884-0

Cited by 71 publications

(67 citation statements)

References 64 publications

(85 reference statements)

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“…Genes encoding chitin synthase enzymes were found in the genomes of a number of fishes and amphibians and shown to be correspondingly expressed at the sites where chitin was localized [1,2]. In this report, we show that chitin is prevalent within the specialized electrosensory organs of cartilaginous fishes (Chondrichthyes).…”

Section: Introductionmentioning

confidence: 62%

Evidence of Chitin in the Ampullae of Lorenzini of Chondrichthyan Fishes

Phillips

Tang

Hassan³

et al. 2019

Preprint

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Chitin is produced by a variety of organisms using enzymes called chitin synthases and was recently discovered in certain vertebrates. In our ongoing investigations into the presence of vertebrate chitin, we unexpectedly found it within the electrosensory organs, known as Ampullae of Lorenzini, of diverse cartilaginous fishes. We used histochemical reagents, chemical analyses, and enzymatic digestions to confirm our findings. Further, in situ hybridization with a sequence from the little skate (Leucoraja erinacea) revealed that chitin synthase expression is localized to cells inside the organs. These findings indicate that cartilaginous fishes endogenously synthesize chitin and beg further investigation into the function of chitin in the electrosensory system.

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Section: Introductionmentioning

confidence: 62%

Evidence of Chitin in the Ampullae of Lorenzini of Chondrichthyan Fishes

Phillips

Tang

Hassan³

et al. 2019

Preprint

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“…One trait hagfish share with invertebrates, but which is lacking in all but a few vertebrates, is the presence of a peritrophic membrane (PM) (Adam, 1966;Nakashima et al, 2018). This is essentially a chitin-based mesh 'bag' which encapsulates the food bolus and, at least in invertebrates, has roles in digestion (e.g.…”

Section: Y X I N E G L U T I N O S a E P T A T R E T U S S T O U Tmentioning

confidence: 99%

“…However, such conclusions are usually only able to be drawn by comparative analysis of a given trait in hagfishes, other chordates and advanced invertebrates (e.g. Nakashima et al, 2018). To date, very few such studies exist.…”

Section: Introductionmentioning

confidence: 99%

The good, the bad and the slimy: experimental studies of hagfish digestive and nutritional physiology

Glover

Weinrauch

2019

Journal of Experimental Biology

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The hagfishes provide valuable insight into the physiology of feeding, digestion and nutrient absorption by virtue of unusual and unique features of their biology. For example, members of this group undergo long periods of fasting, and are the only vertebrates known to absorb organic nutrients across their epidermal surface. Such properties engender significant attention from researchers interested in feeding and feeding-related processes; however, the practical realities of employing the hagfish as an experimental organism can be challenging. Many of the key tools of the experimental biologist are compromised by a species that does not readily feed in captivity, is difficult to instrument and which produces copious quantities of slime. This Commentary provides critical insight into the key aspects of hagfish feeding and digestive processes, and highlights the pitfalls of this group as experimental organisms. We also suggest key research gaps that, if filled, will lead to better understanding of hagfishes, and we consider how this group may advance our knowledge of feeding, digestion and nutrient absorption processes.

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“…In ascidians, the gut space is compartmentalized into a luminal part by envelope membranes. The membranes con ned microbes to the luminal space and maintained the ciliated epithelium free of microbes [26]. The geographically disparate C. intestinalis was found to harbor a core microbiota in the gut [27].…”

Section: Introductionmentioning

confidence: 99%

Seasonal Dynamics and Starvation Impact on the Gut Microbiome of Urochordate Ascidian Halocynthia roretzi

Wei

Gao²,

Yang

et al. 2020

Preprint

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Background Gut microbiota plays important roles in host animal metabolism, homeostasis and environmental adaptation. However, the interplay between the gut microbiome and urochordate ascidian, the most closet relative of vertebrate, remains less explored. In this study, we characterized the gut microbial communities of urochordate ascidian ( Halocynthia roretzi ) across the changes of season and starvation stress using a comprehensive set of omic approaches including 16S rRNA gene amplicon sequencing, shotgun metagenomics, metabolomic profiling, and transcriptome sequencing. Results The 16S rRNA gene amplicon profiling revealed that ascidians harbor indigenous gut microbiota distinctly different to the marine microbial community and significant variations in composition and abundance of gut bacteria, with predominant bacterial orders representing each season. Depressed alpha-diversities of gut microbiota were observed across starvation stress when compared to the communities in aquafarm condition. Synechococcales involving photosynthesis and its related biosynthesis was reduced in abundance while the enrichments of Xanthomonadales and Legionellales may facilitate bile acid biosynthesis during starvation. Metabolomics analysis found that long chain fatty acids, linolenic acid,cyanoamino acid, and pigments derived from gut bacteria were upregulated, suggesting a beneficial contribution of the gut microbiome to the ascidian under starvation stress. Conclusions Our findings revealed seasonal variation of ascidian gut microbiota. Defense and energy-associated metabolites derived from gut microbiome may provide an adaptive interplay between gut microbiome and ascidian host that maintains a beneficial metabolic system across season and starvation stress. The diversity-generating metabolisms from both microbiota and host might lead to the co-evolution and environmental adaptation.

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Chitin-based barrier immunity and its loss predated mucus-colonization by indigenous gut microbiota

Cited by 71 publications

References 64 publications

Evidence of Chitin in the Ampullae of Lorenzini of Chondrichthyan Fishes

Evidence of Chitin in the Ampullae of Lorenzini of Chondrichthyan Fishes

The good, the bad and the slimy: experimental studies of hagfish digestive and nutritional physiology

Seasonal Dynamics and Starvation Impact on the Gut Microbiome of Urochordate Ascidian Halocynthia roretzi

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