Bioconversion of 13C-labeled microalgal phytosterols to cholesterol by the Northern Bay scallop, Argopecten irradians irradians

Giner, José‐Luis; Zhao, Hui; Dixon, Mark S.; Wikfors, Gary H.

doi:10.1016/j.cbpb.2015.11.003

Cited by 11 publications

(3 citation statements)

References 37 publications

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“…Among animals, some (e.g., mammals) can de novo synthesize cholesterol from low molecular weight precursors such as acetate, whereas others (e.g., insects) exclusively depend on dietary sterols due to the complete or partial absence of a cholesterol biosynthetic pathway. Several bivalve species, including mussels, have been suggested to be of the latter type based on radioisotope tracer experiments (Goad 1981; Knauer et al 1998): it is considered that bivalves produce cholesterol by modification of exogenous sterols derived from dietary sources, such as microalgae, as shown by Giner et al (2016). The genome sequence data of the Pacific oyster Crassostrea gigas reported by Zhang et al (2012) also supports these findings: there are no genes encoding enzymes associated with upstream steps of the cholesterol biosynthesis pathway, including squalene monooxygenase and oxidosqualene cyclase, whereas genes for downstream steps of the pathway are present in this bivalve.…”

Section: Discussionmentioning

confidence: 99%

Genomic Evidence that Methanotrophic Endosymbionts Likely Provide Deep-Sea Bathymodiolus Mussels with a Sterol Intermediate in Cholesterol Biosynthesis

Takishita

Takaki

Chikaraishi

et al. 2017

Genome Biology and Evolution

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Sterols are key cyclic triterpenoid lipid components of eukaryotic cellular membranes, which are synthesized through complex multi-enzyme pathways. Similar to most animals, Bathymodiolus mussels, which inhabit deep-sea chemosynthetic ecosystems and harbor methanotrophic and/or thiotrophic bacterial endosymbionts, possess cholesterol as their main sterol. Based on the stable carbon isotope analyses, it has been suggested that host Bathymodiolus mussels synthesize cholesterol using a sterol intermediate derived from the methanotrophic endosymbionts. To test this hypothesis, we sequenced the genome of the methanotrophic endosymbiont in Bathymodiolus platifrons. The genome sequence data demonstrated that the endosymbiont potentially generates up to 4,4-dimethyl-cholesta-8,14,24-trienol, a sterol intermediate in cholesterol biosynthesis, from methane. In addition, transcripts for a subset of the enzymes of the biosynthetic pathway to cholesterol downstream from a sterol intermediate derived from methanotroph endosymbionts were detected in our transcriptome data for B. platifrons. These findings suggest that this mussel can de novo synthesize cholesterol from methane in cooperation with the symbionts. By in situ hybridization analyses, we showed that genes associated with cholesterol biosynthesis from both host and endosymbionts were expressed exclusively in the gill epithelial bacteriocytes containing endosymbionts. Thus, cholesterol production is probably localized within these specialized cells of the gill. Considering that the host mussel cannot de novo synthesize cholesterol and depends largely on endosymbionts for nutrition, the capacity of endosymbionts to synthesize sterols may be important in establishing symbiont–host relationships in these chemosynthetic mussels.

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Section: Discussionmentioning

confidence: 99%

Genomic Evidence that Methanotrophic Endosymbionts Likely Provide Deep-Sea Bathymodiolus Mussels with a Sterol Intermediate in Cholesterol Biosynthesis

Takishita

Takaki

Chikaraishi

et al. 2017

Genome Biology and Evolution

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“…Mammals synthesize squalene and various sterols from low-molecular-weight precursors such as acetate via mevalonate. However, other animals exclusively depend on dietary sterols due to the complete or partial absence of a cholesterol biosynthetic pathway, such as insects, nematodes [ 49 , 50 ], the annelid Lumbricus terrestris [ 51 , 52 ], and some marine invertebrate crustaceans [ 53 – 56 ]. For example, C. elegans expresses predicted homologues of the enzymes that produce the initial intermediates of the mammalian sterol biosynthetic pathway up to farnesyl diphosphate but cannot synthesize either squalene or lanosterol [ 49 ].…”

Section: Resultsmentioning

confidence: 99%

Sulfur, sterol and trehalose metabolism in the deep-sea hydrocarbon seep tubeworm Lamellibrachia luymesi

et al. 2023

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Background Lamellibrachia luymesi dominates cold sulfide-hydrocarbon seeps and is known for its ability to consume bacteria for energy. The symbiotic relationship between tubeworms and bacteria with particular adaptations to chemosynthetic environments has received attention. However, metabolic studies have primarily focused on the mechanisms and pathways of the bacterial symbionts, while studies on the animal hosts are limited. Results Here, we sequenced the transcriptome of L. luymesi and generated a transcriptomic database containing 79,464 transcript sequences. Based on GO and KEGG annotations, we identified transcripts related to sulfur metabolism, sterol biosynthesis, trehalose synthesis, and hydrolysis. Our in-depth analysis identified sulfation pathways in L. luymesi, and sulfate activation might be an important detoxification pathway for promoting sulfur cycling, reducing byproducts of sulfide metabolism, and converting sulfur compounds to sulfur-containing organics, which are essential for symbiotic survival. Moreover, sulfide can serve directly as a sulfur source for cysteine synthesis in L. luymesi. The existence of two pathways for cysteine synthesis might ensure its participation in the formation of proteins, heavy metal detoxification, and the sulfide-binding function of haemoglobin. Furthermore, our data suggested that cold-seep tubeworm is capable of de novo sterol biosynthesis, as well as incorporation and transformation of cycloartenol and lanosterol into unconventional sterols, and the critical enzyme involved in this process might have properties similar to those in the enzymes from plants or fungi. Finally, trehalose synthesis in L. luymesi occurs via the trehalose-6-phosphate synthase (TPS) and trehalose-6-phosphate phosphatase (TPP) pathways. The TPP gene has not been identified, whereas the TPS gene encodes a protein harbouring conserved TPS/OtsA and TPP/OtsB domains. The presence of multiple trehalases that catalyse trehalose hydrolysis could indicate the different roles of trehalase in cold-seep tubeworms. Conclusions We elucidated several molecular pathways of sulfate activation, cysteine and cholesterol synthesis, and trehalose metabolism. Contrary to the previous analysis, two pathways for cysteine synthesis and the cycloartenol-C-24-methyltransferase gene were identified in animals for the first time. The present study provides new insights into particular adaptations to chemosynthetic environments in L. luymesi and can serve as the basis for future molecular studies on host-symbiont interactions and biological evolution.

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“…They were more likely to dealkylate side chains possessing 24-ethyl groups. The only 24-methyl sterols dealkylated by A. irradians contained a Δ 24(28) olefin (i.e., 24-methylene, rather than 24-methyl) [ 55 ].…”

Section: Phylogenic and Ecological Insightsmentioning

confidence: 99%

Microbial Sterolomics as a Chemical Biology Tool

Haubrich

2018

Molecules

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Metabolomics has become a powerful tool in chemical biology. Profiling the human sterolome has resulted in the discovery of noncanonical sterols, including oxysterols and meiosis-activating sterols. They are important to immune responses and development, and have been reviewed extensively. The triterpenoid metabolite fusidic acid has developed clinical relevance, and many steroidal metabolites from microbial sources possess varying bioactivities. Beyond the prospect of pharmacognostical agents, the profiling of minor metabolites can provide insight into an organism’s biosynthesis and phylogeny, as well as inform drug discovery about infectious diseases. This review aims to highlight recent discoveries from detailed sterolomic profiling in microorganisms and their phylogenic and pharmacological implications.

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Bioconversion of 13C-labeled microalgal phytosterols to cholesterol by the Northern Bay scallop, Argopecten irradians irradians

Cited by 11 publications

References 37 publications

Genomic Evidence that Methanotrophic Endosymbionts Likely Provide Deep-Sea Bathymodiolus Mussels with a Sterol Intermediate in Cholesterol Biosynthesis

Genomic Evidence that Methanotrophic Endosymbionts Likely Provide Deep-Sea Bathymodiolus Mussels with a Sterol Intermediate in Cholesterol Biosynthesis

Sulfur, sterol and trehalose metabolism in the deep-sea hydrocarbon seep tubeworm Lamellibrachia luymesi

Microbial Sterolomics as a Chemical Biology Tool

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