Dataset Information

Genomic Blueprint of Glycine Betaine Metabolism in Coral Metaorganisms and Their Contribution to Reef Nitrogen Budgets.

ABSTRACT: The osmolyte glycine betaine (GB) ranks among the few widespread biomolecules in all three domains of life. In corals, tissue concentrations of GB are substantially higher than in the ambient seawater. However, the synthetic routes remain unresolved, questioning whether intracellular GB originates from de novo synthesis or heterotrophic input. Here we show that the genomic blueprint of coral metaorganisms encode the biosynthetic and degradation machinery for GB. Member organisms also adopted the prokaryotic high-affinity carrier-mediated uptake of exogenous GB, rendering coral reefs potential sinks of marine dissolved GB. The machinery metabolizing GB is highly expressed in the coral model Aiptasia and its microalgal symbionts, signifying GB's role in the cnidarian-dinoflagellate symbiosis. We estimate that corals store between 106-109 grams of GB globally, representing about 16% of their nitrogen biomass. Our findings provide a framework for further mechanistic studies addressing GB's role in coral biology and reef ecosystem nitrogen cycling.

SUBMITTER: Ngugi DK

PROVIDER: S-EPMC7240134 | biostudies-literature | 2020 May

REPOSITORIES: biostudies-literature

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Genomic Blueprint of Glycine Betaine Metabolism in Coral Metaorganisms and Their Contribution to Reef Nitrogen Budgets.

Ngugi David K DK Ziegler Maren M Duarte Carlos M CM Voolstra Christian R CR

iScience 20200430 5

The osmolyte glycine betaine (GB) ranks among the few widespread biomolecules in all three domains of life. In corals, tissue concentrations of GB are substantially higher than in the ambient seawater. However, the synthetic routes remain unresolved, questioning whether intracellular GB originates from de novo synthesis or heterotrophic input. Here we show that the genomic blueprint of coral metaorganisms encode the biosynthetic and degradation machinery for GB. Member organisms also adopted the ...[more]

PMID: 32438323

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Project description:BACKGROUND:Accumulating evidence is supporting the protective effect of whole grains against several chronic diseases. Simultaneously, our knowledge is increasing on the impact of gut microbiota on our health and on how diet can modify the composition of our bacterial cohabitants. Herein, we studied C57BL/6?J mice fed with diets enriched with rye bran and wheat aleurone, conventional and germ-free C57BL/6NTac mice on a basal diet, and the colonic fermentation of rye bran in an in vitro model of the human gastrointestinal system. We performed 16S rRNA gene sequencing and metabolomics on the study samples to determine the effect of bran-enriched diets on the gut microbial composition and the potential contribution of microbiota to the metabolism of a novel group of betainized compounds. RESULTS:The bran-enriched study diets elevated the levels of betainized compounds in the colon contents of C57BL/6?J mice. The composition of microbiota changed, and the bran-enriched diets induced an increase in the relative abundance of several bacterial taxa, including Akkermansia, Bifidobacterium, Coriobacteriaceae, Lactobacillus, Parasutterella, and Ruminococcus, many of which are associated with improved health status or the metabolism of plant-based molecules. The levels of betainized compounds in the gut tissues of germ-free mice were significantly lower compared to conventional mice. In the in vitro model of the human gut, the production of betainized compounds was observed throughout the incubation, while the levels of glycine betaine decreased. In cereal samples, only low levels or trace amounts of other betaines than glycine betaine were observed. CONCLUSIONS:Our findings provide evidence that the bacterial taxa increased in relative abundance by the bran-based diet are also involved in the metabolism of glycine betaine into other betainized compounds, adding another potential compound group acting as a mediator of the synergistic metabolic effect of diet and colonic microbiota.

Project description:Benthic primary producers in tropical reef ecosystems can alter biogeochemical cycling and microbial processes in the surrounding seawater. In order to quantify these influences, we measured rates of photosynthesis, respiration, and dissolved organic carbon (DOC) exudate release by the dominant benthic primary producers (calcifying and non-calcifying macroalgae, turf-algae and corals) on reefs of Mo'orea French Polynesia. Subsequently, we examined planktonic and benthic microbial community response to these dissolved exudates by measuring bacterial growth rates and oxygen and DOC fluxes in dark and daylight incubation experiments. All benthic primary producers exuded significant quantities of DOC (roughly 10% of their daily fixed carbon) into the surrounding water over a diurnal cycle. The microbial community responses were dependent upon the source of the exudates and whether the inoculum of microbes included planktonic or planktonic plus benthic communities. The planktonic and benthic microbial communities in the unamended control treatments exhibited opposing influences on DO concentration where respiration dominated in treatments comprised solely of plankton and autotrophy dominated in treatments with benthic plus plankon microbial communities. Coral exudates (and associated inorganic nutrients) caused a shift towards a net autotrophic microbial metabolism by increasing the net production of oxygen by the benthic and decreasing the net consumption of oxygen by the planktonic microbial community. In contrast, the addition of algal exudates decreased the net primary production by the benthic communities and increased the net consumption of oxygen by the planktonic microbial community thereby resulting in a shift towards net heterotrophic community metabolism. When scaled up to the reef habitat, exudate-induced effects on microbial respiration did not outweigh the high oxygen production rates of benthic algae, such that reef areas dominated with benthic primary producers were always estimated to be net autotrophic. However, estimates of microbial consumption of DOC at the reef scale surpassed the DOC exudation rates suggesting net consumption of DOC at the reef-scale. In situ mesocosm experiments using custom-made benthic chambers placed over different types of benthic communities exhibited identical trends to those found in incubation experiments. Here we provide the first comprehensive dataset examining direct primary producer-induced, and indirect microbially mediated alterations of elemental cycling in both benthic and planktonic reef environments over diurnal cycles. Our results highlight the variability of the influence of different benthic primary producers on microbial metabolism in reef ecosystems and the potential implications for energy transfer to higher trophic levels during shifts from coral to algal dominance on reefs.

Dataset Information

Genomic Blueprint of Glycine Betaine Metabolism in Coral Metaorganisms and Their Contribution to Reef Nitrogen Budgets.

Publications

Genomic Blueprint of Glycine Betaine Metabolism in Coral Metaorganisms and Their Contribution to Reef Nitrogen Budgets.

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