Sequestration and Cyanobacterial Diet Preferences in the Opisthobranch Molluscs Dolabrifera nicaraguana and Stylocheilus rickettsi

A multidisciplinary approach was used to assess chemical ecological dietary interactions between marine organisms as a tool to isolate novel ecologically relevant compounds with biotechnological potential. First, laboratory-based feeding preference assays of the sea hare Dolabrifera nicaraguana (pre...

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Autores principales: Kasey E. Clark, Angela Capper, Wei-Ting Liu, Amanda M. Fenner, Alejandro Almanza, Gina Della Togna, Liuris Herrera, Timothy Johns, Valerie J. Paul, Pieter C. Dorrestein, Todd L. Capson, Marcy J. Balunas
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Publicado: Frontiers Media S.A. 2021
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spelling oai:doaj.org-article:27810dcad59e49959f71378abcc901902021-11-10T06:20:41ZSequestration and Cyanobacterial Diet Preferences in the Opisthobranch Molluscs Dolabrifera nicaraguana and Stylocheilus rickettsi2296-774510.3389/fmars.2021.766282https://doaj.org/article/27810dcad59e49959f71378abcc901902021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fmars.2021.766282/fullhttps://doaj.org/toc/2296-7745A multidisciplinary approach was used to assess chemical ecological dietary interactions between marine organisms as a tool to isolate novel ecologically relevant compounds with biotechnological potential. First, laboratory-based feeding preference assays of the sea hare Dolabrifera nicaraguana (previously known as D. dolabrifera), an anaspidean mollusc, were conducted by simultaneously offering six food options collected from nearby tidal pools in the Coiba National Park in the Tropical Eastern Pacific of Panama. An evaluation of preferred dietary repertoire revealed D. nicaraguana significantly preferred cf. Lyngbya sp. over the cyanobacterium Symploca sp., green alga Chaetomorpha sp., and red alga Spyridia sp. A no-choice feeding assay using cf. Lyngbya sp. or green alga Cladophora sp. supported this finding. Secondly, we conducted bioactivity-guided fractionation using the preferred food source of D. nicaraguana, the ‘hair-like” cf. Lyngbya sp. from which we also isolated and elucidated two new depsipeptide compounds, veraguamide M (1) and veraguamide N (2). Veraguamides M (1) and N (2) showed in vitro activity toward the malaria-causing parasite Plasmodium falciparum with GI50 values of 4.2 and 4.3 μM, respectively, and therapeutic windows of 7.0–8.0 (based on moderate cytotoxicities to mammalian Vero cells with GI50 values of 29.3 and 34.1 μM, respectively). Veraguamide N (2) was also active against Leishmania donovani, the causative agent of visceral leishmaniasis, with a GI50 value of 6.9 μM. We then evaluated sequestration of these new compounds by D. nicaraguana used in the feeding assays and found trace amounts of the dietary sequestered compounds. Finally, we evaluated sequestration of these new compounds by the sea hare Stylocheilus rickettsi (previously known as S. striatus) that were grazing on the cf. Lyngbya sp. used in the feeding assays and found both to be sequestered. This study is the first example whereby compounds with significant activity against tropical parasites have been found in both the sea hare S. rickettsi and its cyanobacterial food source. These results suggest that chemical ecological studies involving sea hares and cyanobacteria continue to provide a diverse source of bioactive compounds with biotechnological potential.Kasey E. ClarkKasey E. ClarkAngela CapperWei-Ting LiuAmanda M. FennerAlejandro AlmanzaAlejandro AlmanzaGina Della TognaLiuris HerreraTimothy JohnsValerie J. PaulPieter C. DorresteinTodd L. CapsonTodd L. CapsonMarcy J. BalunasMarcy J. BalunasMarcy J. BalunasFrontiers Media S.A.articlemarine chemical ecologysea hares and cyanobacteriacf. Lyngbya sp. (formerly Lyngbya majuscula)Dolabrifera nicaraguana (formerly D. dolabrifera)Stylocheilus rickettsi (formerly S. striatus)bioactive secondary metabolitesScienceQGeneral. Including nature conservation, geographical distributionQH1-199.5ENFrontiers in Marine Science, Vol 8 (2021)
institution DOAJ
collection DOAJ
language EN
topic marine chemical ecology
sea hares and cyanobacteria
cf. Lyngbya sp. (formerly Lyngbya majuscula)
Dolabrifera nicaraguana (formerly D. dolabrifera)
Stylocheilus rickettsi (formerly S. striatus)
bioactive secondary metabolites
Science
Q
General. Including nature conservation, geographical distribution
QH1-199.5
spellingShingle marine chemical ecology
sea hares and cyanobacteria
cf. Lyngbya sp. (formerly Lyngbya majuscula)
Dolabrifera nicaraguana (formerly D. dolabrifera)
Stylocheilus rickettsi (formerly S. striatus)
bioactive secondary metabolites
Science
Q
General. Including nature conservation, geographical distribution
QH1-199.5
Kasey E. Clark
Kasey E. Clark
Angela Capper
Wei-Ting Liu
Amanda M. Fenner
Alejandro Almanza
Alejandro Almanza
Gina Della Togna
Liuris Herrera
Timothy Johns
Valerie J. Paul
Pieter C. Dorrestein
Todd L. Capson
Todd L. Capson
Marcy J. Balunas
Marcy J. Balunas
Marcy J. Balunas
Sequestration and Cyanobacterial Diet Preferences in the Opisthobranch Molluscs Dolabrifera nicaraguana and Stylocheilus rickettsi
description A multidisciplinary approach was used to assess chemical ecological dietary interactions between marine organisms as a tool to isolate novel ecologically relevant compounds with biotechnological potential. First, laboratory-based feeding preference assays of the sea hare Dolabrifera nicaraguana (previously known as D. dolabrifera), an anaspidean mollusc, were conducted by simultaneously offering six food options collected from nearby tidal pools in the Coiba National Park in the Tropical Eastern Pacific of Panama. An evaluation of preferred dietary repertoire revealed D. nicaraguana significantly preferred cf. Lyngbya sp. over the cyanobacterium Symploca sp., green alga Chaetomorpha sp., and red alga Spyridia sp. A no-choice feeding assay using cf. Lyngbya sp. or green alga Cladophora sp. supported this finding. Secondly, we conducted bioactivity-guided fractionation using the preferred food source of D. nicaraguana, the ‘hair-like” cf. Lyngbya sp. from which we also isolated and elucidated two new depsipeptide compounds, veraguamide M (1) and veraguamide N (2). Veraguamides M (1) and N (2) showed in vitro activity toward the malaria-causing parasite Plasmodium falciparum with GI50 values of 4.2 and 4.3 μM, respectively, and therapeutic windows of 7.0–8.0 (based on moderate cytotoxicities to mammalian Vero cells with GI50 values of 29.3 and 34.1 μM, respectively). Veraguamide N (2) was also active against Leishmania donovani, the causative agent of visceral leishmaniasis, with a GI50 value of 6.9 μM. We then evaluated sequestration of these new compounds by D. nicaraguana used in the feeding assays and found trace amounts of the dietary sequestered compounds. Finally, we evaluated sequestration of these new compounds by the sea hare Stylocheilus rickettsi (previously known as S. striatus) that were grazing on the cf. Lyngbya sp. used in the feeding assays and found both to be sequestered. This study is the first example whereby compounds with significant activity against tropical parasites have been found in both the sea hare S. rickettsi and its cyanobacterial food source. These results suggest that chemical ecological studies involving sea hares and cyanobacteria continue to provide a diverse source of bioactive compounds with biotechnological potential.
format article
author Kasey E. Clark
Kasey E. Clark
Angela Capper
Wei-Ting Liu
Amanda M. Fenner
Alejandro Almanza
Alejandro Almanza
Gina Della Togna
Liuris Herrera
Timothy Johns
Valerie J. Paul
Pieter C. Dorrestein
Todd L. Capson
Todd L. Capson
Marcy J. Balunas
Marcy J. Balunas
Marcy J. Balunas
author_facet Kasey E. Clark
Kasey E. Clark
Angela Capper
Wei-Ting Liu
Amanda M. Fenner
Alejandro Almanza
Alejandro Almanza
Gina Della Togna
Liuris Herrera
Timothy Johns
Valerie J. Paul
Pieter C. Dorrestein
Todd L. Capson
Todd L. Capson
Marcy J. Balunas
Marcy J. Balunas
Marcy J. Balunas
author_sort Kasey E. Clark
title Sequestration and Cyanobacterial Diet Preferences in the Opisthobranch Molluscs Dolabrifera nicaraguana and Stylocheilus rickettsi
title_short Sequestration and Cyanobacterial Diet Preferences in the Opisthobranch Molluscs Dolabrifera nicaraguana and Stylocheilus rickettsi
title_full Sequestration and Cyanobacterial Diet Preferences in the Opisthobranch Molluscs Dolabrifera nicaraguana and Stylocheilus rickettsi
title_fullStr Sequestration and Cyanobacterial Diet Preferences in the Opisthobranch Molluscs Dolabrifera nicaraguana and Stylocheilus rickettsi
title_full_unstemmed Sequestration and Cyanobacterial Diet Preferences in the Opisthobranch Molluscs Dolabrifera nicaraguana and Stylocheilus rickettsi
title_sort sequestration and cyanobacterial diet preferences in the opisthobranch molluscs dolabrifera nicaraguana and stylocheilus rickettsi
publisher Frontiers Media S.A.
publishDate 2021
url https://doaj.org/article/27810dcad59e49959f71378abcc90190
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