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Transcriptomic analyses highlight the likely metabolic consequences of colonization of a cnidarian host by native or non-native Symbiodinium species.

ABSTRACT: Reef-building corals and some other cnidarians form symbiotic relationships with members of the dinoflagellate family Symbiodinaceae. As Symbiodinaceae is a highly diverse taxon, the physiological interactions between its members and their hosts are assumed to differ between associations. The presence of different symbiont types is known to affect expression levels of specific host genes, but knowledge of the effects on the transcriptome more broadly remains limited. In the present study, transcriptome profiling was conducted on the tropical corallimorpharian, Ricordea yuma, following the establishment of symbiosis with either the 'homologous' symbiont Symbiodinium goreaui (also known as Cladocopium goreaui; ITS2 type C1) or 'heterologous' symbionts (predominantly S. trenchii, which is also known as Durusdinium trenchii; ITS2 type D1a) isolated from a different corallimorpharian host (Rhodactis indosinensis). Transcriptomic analyses showed that genes encoding host glycogen biosynthesis pathway components are more highly induced during colonization by the homologous symbiont than by the heterologous symbiont. Similar patterns were also observed for several other genes thought to facilitate symbiotic nutrient exchange, including those involved in lipid translocation/storage and metabolite transport. The gene expression results presented here imply that colonization by homologous or heterologous Symbiodinium types may have very different metabolic consequences for the Ricordea host, supporting the notion that even though some cnidarians may be able to form novel symbioses after bleaching, the metabolic performance of these may be compromised.This article has an associated First Person interview with the first author of the paper.

SUBMITTER: Lin MF

PROVIDER: S-EPMC6451341 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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Transcriptomic analyses highlight the likely metabolic consequences of colonization of a cnidarian host by native or non-native Symbiodinium species.

Lin Mei-Fang MF Takahashi Shunichi S Forêt Sylvain S Davy Simon K SK Miller David J DJ

Biology open 20190327 3

Reef-building corals and some other cnidarians form symbiotic relationships with members of the dinoflagellate family Symbiodinaceae. As Symbiodinaceae is a highly diverse taxon, the physiological interactions between its members and their hosts are assumed to differ between associations. The presence of different symbiont types is known to affect expression levels of specific host genes, but knowledge of the effects on the transcriptome more broadly remains limited. In the present ...[more]

PMID: 30814067

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Project description:UnlabelledThe gut microbiota enhances the host's metabolic capacity for processing nutrients and drugs and modulate the activities of multiple pathways in a variety of organ systems. We have probed the systemic metabolic adaptation to gut colonization for 20 days following exposure of axenic mice (n = 35) to a typical environmental microbial background using high-resolution (1)H nuclear magnetic resonance (NMR) spectroscopy to analyze urine, plasma, liver, kidney, and colon (5 time points) metabolic profiles. Acquisition of the gut microbiota was associated with rapid increase in body weight (4%) over the first 5 days of colonization with parallel changes in multiple pathways in all compartments analyzed. The colonization process stimulated glycogenesis in the liver prior to triggering increases in hepatic triglyceride synthesis. These changes were associated with modifications of hepatic Cyp8b1 expression and the subsequent alteration of bile acid metabolites, including taurocholate and tauromuricholate, which are essential regulators of lipid absorption. Expression and activity of major drug-metabolizing enzymes (Cyp3a11 and Cyp2c29) were also significantly stimulated. Remarkably, statistical modeling of the interactions between hepatic metabolic profiles and microbial composition analyzed by 16S rRNA gene pyrosequencing revealed strong associations of the Coriobacteriaceae family with both the hepatic triglyceride, glucose, and glycogen levels and the metabolism of xenobiotics. These data demonstrate the importance of microbial activity in metabolic phenotype development, indicating that microbiota manipulation is a useful tool for beneficially modulating xenobiotic metabolism and pharmacokinetics in personalized health care.ImportanceGut bacteria have been associated with various essential biological functions in humans such as energy harvest and regulation of blood pressure. Furthermore, gut microbial colonization occurs after birth in parallel with other critical processes such as immune and cognitive development. Thus, it is essential to understand the bidirectional interaction between the host metabolism and its symbionts. Here, we describe the first evidence of an in vivo association between a family of bacteria and hepatic lipid metabolism. These results provide new insights into the fundamental mechanisms that regulate host-gut microbiota interactions and are thus of wide interest to microbiological, nutrition, metabolic, systems biology, and pharmaceutical research communities. This work will also contribute to developing novel strategies in the alteration of host-gut microbiota relationships which can in turn beneficially modulate the host metabolism.

Project description:BACKGROUND: The algal endosymbionts (genus Symbiodinium) associated with scleractinian corals (and other reef invertebrates) have received a lot of research attention in the past decade, particularly as certain host-symbiont associations appear more affected by increasing seawater temperatures than others. With the rapid accumulation of information on the diversity of Symbiodinium, it is becoming increasingly difficult to compare newly acquired Symbiodinium data with existing data to detect patterns of host-symbiont specificity on broader spatial scales. The lack of a general consensus on the classification of Symbiodinium species coupled with the variety of different markers used to identify the genus Symbiodinium (ITS1, ITS2, LSU D1/D2, chloroplast 23S rDNA and psbA minicircle) further complicate direct comparison. DESCRIPTION: The SymbioGBR database compiles all currently available Symbiodinium sequences and associated host information of data collected from the Great Barrier Reef into a single relational database that is accessible via a user-friendly, searchable web-based application (http://www.SymbioGBR.org). SymbioGBR allows users to query Symbiodinium types or sequences sourced from various genetic markers (e.g. ITS1, ITS2, LSU D1/D2 and chloroplast 23S) and invertebrate host species to explore their reported associations. In addition, as the database includes sequence information of multiple genetic markers, it allows cross-referencing between conventional (e.g. ITS2 region) and novel markers that exhibit low intragenomic variability (e.g. psbA region). Finally, the database is based on the collection details of individual specimens. Such host-symbiont associations can be assessed quantitatively and viewed in relation to their environmental and geographic context. CONCLUSIONS: The SymbioGBR database provides a comprehensive overview of Symbiodinium diversity and host-associations on the Great Barrier Reef. It provides a quick, user-friendly means to compare newly acquired data on Symbiodinium (e.g. raw sequences or characterized Symbiodinium types) with previous data on the diversity of invertebrate host-symbiont associations on the GBR. The inclusion of psbAncr sequence information allows for validation of widely used ITS1/ITS2 markers and their ability to accurately identify relevant sequences. Most importantly, centralization of sequence information from multiple genetic markers will aid the classification of Symbiodinium species diversity and allow researchers to easily compare patterns of host-Symbiodinium associations.

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Transcriptomic analyses highlight the likely metabolic consequences of colonization of a cnidarian host by native or non-native Symbiodinium species.

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Transcriptomic analyses highlight the likely metabolic consequences of colonization of a cnidarian host by native or non-native <i>Symbiodinium</i> species.

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