Animal biosynthesis of complex polyketides in a photosynthetic partnership

Torres, Joshua P.; Lin, Zhenjian; Winter, Jaclyn M.; Krug, Patrick J.; Schmidt, Eric W.

doi:10.1101/764225

“…Polypropionates with different carbon skeleton were also described from genus Siphonaria (Gastropoda: Tectipleura) such as Siphonaria baconi Reeve, 1856 (now accepted as Siphonaria zelandica Quoy and Gaimard, 1833) 43 , and Siphonaria diemenensis Quoy and Gaimard, 1833 44 . Moreover, other marine molluscs, like photosynthetic members of the order Sacoglossa, harbor a big complex of different polypropionates acting as photoprotectants and antioxidants within the slugs 45 , 46 . These compounds seem to be common within the Onchidiidae and are reported from various localities, including China, Hawaii, and Australia 18 , 44 , 47 .…”

Section: Discussionmentioning

confidence: 99%

From Persian Gulf to Indonesia: interrelated phylogeographic distance and chemistry within the genus Peronia (Onchidiidae, Gastropoda, Mollusca)

Maniei

¹

,

Moghaddam

²

,

Crüsemann

³

et al. 2020

Sci Rep

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the knowledge of relationships between taxa is essential to understand and explain the chemical diversity of the respective groups. Here, twelve individuals of the panpulmonate slug Peronia persiae from two localities in persian Gulf, and one animal of P. verruculata from Bangka island, indonesia, were analyzed in a phylogenetic and chemotaxonomic framework. Based on the ABGD test and haplotype networking using coi gene sequences of Peronia specimens, nine well-supported clades were found. Haplotype network analysis highlighted a considerable distance between the specimens of P. persiae and other clades. Metabolomic analysis of both species using tandem mass spectrometrybased GnpS molecular networking revealed a large chemical diversity within Peronia of different clades and localities. While P. persiae from different localities showed a highly similar metabolome, only few identical chemical features were found across the clades. the main common metabolites in both Peronia species were assigned as polypropionate esters of onchitriols and ilikonapyrones, and osmoprotectant amino acid-betaine compounds. On the other hand, the isoflavonoids genistein and daidzein were exclusively detected in P. persiae, while cholesterol and conjugated chenodeoxycholic acids were only found in P. verruculata. flavonoids, bile acids, and amino acid-betaine compounds were not reported before from onchidiidae, some are even new for panpulmonates. our chemical analyses indicate a close chemotaxonomic relation between phylogeographically distant Peronia species. Peronia Fleming, 1822, a panpulmonate slug genus, is typically distributed in tropical and subtropical regions of the Indo-Pacific ocean 1. The genus Peronia, with ten acknowledged species, has been reported from many localities ranging from the Indo-Pacific to the East Coast of Africa and to Hawaii 2-4. Due to undetected cryptic speciation, species diversity is often underestimated while the widespread distributions attributed to species is often overestimated 5. The integration of molecular and morphological methods has led to numerous discoveries of cryptic species complexes 6. This is also true for the genus Peronia, as was shown by Maniei et al. 3. To date, only three Peronia species are well investigated by molecular and/or morphology data, i.e.

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“…[7] However, ar ecent study by Schmidt and co-workers excluded ab acterial origin and demonstrated that the gene EcPKS1-found in the animal genome but not in the sequestered algal chloroplast-was responsible for the biosynthesis of pyrone polyenes,a fter heterologous expression in yeast. [8] Theg ene is present in Elysia chlorotica,w hile homologues were found in Placobranchuso cellatus.…”

Section: Introductionmentioning

confidence: 99%

Complex Polypropionates from a South China Sea Photosynthetic Mollusk: Isolation and Biomimetic Synthesis Highlighting Novel Rearrangements

Wu

¹

,

Li

²

,

Xu

³

et al. 2020

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Placobranchus ocellatus, regarded as a "solar-powered" sacoglossan mollusk, is well known to produce diverse and complex γ-pyrone polypropionates. Unexpectedly, in this study, the chemical investigation of P. ocellatus from the South China Sea led to the discovery of ocellatusones A−D, a series of racemic non-γpyrone polyketides with novel skeletons, characterized by a bicyclo[3.2.1]octane (1, 2), a bicyclo[3.3.1]nonane (3) or a mesitylene-substituted dimethylfuran-3(2H)-one core (4). Extensive spectroscopic analysis, quantum chemical computation, chemical synthesis, and/or X-ray diffraction analysis were used to determine the structure and absolute configuration of the new compounds, including each enantiomer of racemic compounds 1−4 after chiral HPLC resolution. An important array of new and diversitygenerating rearrangements is proposed to explain the biosynthesis of these unusual compounds based on careful structural analysis and comparison with six known co-occurring γ-pyrones (5−10). Furthermore, the successful biomimetic synthesis of ocellatusone A (1) from its γ-pyrone precursor (5) confirmed the biosynthetic relationship of these two compounds and the proposed rearrangement through an unprecedented acid promoted cascade reaction. Besides, an initially untargeted semisynthetic product, polycyclic lactone 11 with another novel carbocyclic skeleton was proved to be naturally occurring in the mollusk by comparative LC-MS/MS analysis, which provides a strategy to fish a vast number of novel trace components in Nature.

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“…7 However, a recent study by Schmidt and coworkers excluded a bacterial origin and demonstrated that the gene EcPKS1found in the animal genome but not in the sequestered algal chloroplast-was responsible for the biosynthesis of pyrone polyenes, after heterologous expression in yeast. 8 The gene is present in Elysia chlorotica, while homologues were found in Placobranchus ocellatus. Structurally, the sacoglossan polypropionates show a characteristic γ-pyrone connected to a variety of complex cyclic systems and/or unsaturated side chains (skeletons I-IV, Figure 1).…”

mentioning

confidence: 99%

“…The polypropionate nature of the novel compounds ocellatusones A-D (1-4) was deduced from their co-occurrence with the well documented tridachiahydropyrone (5), phototridachiahydropyrone (6), tridachiahydropyrones B (7) and C (8). All are biosynthetically related, sharing common structural features such as an isoamyl moiety and the presence of 1,3-positionned methyl substituents.…”

mentioning

confidence: 99%

Complex Polypropionates from a South China Sea Photosynthetic Mollusk: Isolation and Biomimetic Synthesis Highlighting Novel Rearrangements

Wu

¹

,

Li

²

,

Xu

³

et al. 2020

View full text Add to dashboard Cite

Placobranchus ocellatus, regarded as a "solar-powered" sacoglossan mollusk, is well known to produce diverse and complex γ-pyrone polypropionates. Unexpectedly, in this study, the chemical investigation of P. ocellatus from the South China Sea led to the discovery of ocellatusones A−D, a series of racemic non-γpyrone polyketides with novel skeletons, characterized by a bicyclo[3.2.1]octane (1, 2), a bicyclo[3.3.1]nonane (3) or a mesitylene-substituted dimethylfuran-3(2H)-one core (4). Extensive spectroscopic analysis, quantum chemical computation, chemical synthesis, and/or X-ray diffraction analysis were used to determine the structure and absolute configuration of the new compounds, including each enantiomer of racemic compounds 1−4 after chiral HPLC resolution. An important array of new and diversitygenerating rearrangements is proposed to explain the biosynthesis of these unusual compounds based on careful structural analysis and comparison with six known co-occurring γ-pyrones (5−10). Furthermore, the successful biomimetic synthesis of ocellatusone A (1) from its γ-pyrone precursor (5) confirmed the biosynthetic relationship of these two compounds and the proposed rearrangement through an unprecedented acid promoted cascade reaction. Besides, an initially untargeted semisynthetic product, polycyclic lactone 11 with another novel carbocyclic skeleton was proved to be naturally occurring in the mollusk by comparative LC-MS/MS analysis, which provides a strategy to fish a vast number of novel trace components in Nature.

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Animal biosynthesis of complex polyketides in a photosynthetic partnership

Abstract: 7

Cited by 13 publications

References 63 publications

From Persian Gulf to Indonesia: interrelated phylogeographic distance and chemistry within the genus Peronia (Onchidiidae, Gastropoda, Mollusca)

From Persian Gulf to Indonesia: interrelated phylogeographic distance and chemistry within the genus Peronia (Onchidiidae, Gastropoda, Mollusca)

Complex Polypropionates from a South China Sea Photosynthetic Mollusk: Isolation and Biomimetic Synthesis Highlighting Novel Rearrangements

Complex Polypropionates from a South China Sea Photosynthetic Mollusk: Isolation and Biomimetic Synthesis Highlighting Novel Rearrangements

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