Uncovering the Core Microbiome and Distribution of Palmerolide in <i>Synoicum adareanum</i> Across the Anvers Island Archipelago, Antarctica
Polar marine ecosystems hold the potential for bioactive compound biodiscovery, based on their untapped macro- and microorganism diversity. Characterization of polar benthic marine invertebrate-associated microbiomes is limited to few studies. This study was motivated by our interest in better under...
| Main Authors: | , , , , , , , , , , , , , |
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| Format: | Article |
| Sprog: | English |
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MDPI AG
2020-06-01
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| Serier: | Marine Drugs |
| Fag: | |
| Online adgang: | https://www.mdpi.com/1660-3397/18/6/298 |
| _version_ | 1827715697035182080 |
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| author | Alison E. Murray Nicole E. Avalon Lucas Bishop Karen W. Davenport Erwan Delage Armand E.K. Dichosa Damien Eveillard Mary L. Higham Sofia Kokkaliari Chien-Chi Lo Christian S. Riesenfeld Ryan M. Young Patrick S.G. Chain Bill J. Baker |
| author_facet | Alison E. Murray Nicole E. Avalon Lucas Bishop Karen W. Davenport Erwan Delage Armand E.K. Dichosa Damien Eveillard Mary L. Higham Sofia Kokkaliari Chien-Chi Lo Christian S. Riesenfeld Ryan M. Young Patrick S.G. Chain Bill J. Baker |
| author_sort | Alison E. Murray |
| collection | DOAJ |
| description | Polar marine ecosystems hold the potential for bioactive compound biodiscovery, based on their untapped macro- and microorganism diversity. Characterization of polar benthic marine invertebrate-associated microbiomes is limited to few studies. This study was motivated by our interest in better understanding the microbiome structure and composition of the ascidian, <i>Synoicum adareanum</i>, in which palmerolide A (PalA), a bioactive macrolide with specificity against melanoma, was isolated. PalA bears structural resemblance to a hybrid nonribosomal peptide-polyketide that has similarities to microbially-produced macrolides. We conducted a spatial survey to assess both PalA levels and microbiome composition in <i>S. adareanum</i> in a region of the Antarctic Peninsula near Anvers Island (64°46′ S, 64°03′ W). PalA was ubiquitous and abundant across a collection of 21 ascidians (3 subsamples each) sampled from seven sites across the Anvers Island Archipelago. The microbiome composition (V3–V4 16S rRNA gene sequence variants) of these 63 samples revealed a core suite of 21 bacterial amplicon sequence variants (ASVs)—20 of which were distinct from regional bacterioplankton. ASV co-occurrence analysis across all 63 samples yielded subgroups of taxa that may be interacting biologically (interacting subsystems) and, although the levels of PalA detected were not found to correlate with specific sequence variants, the core members appeared to occur in a preferred optimum and tolerance range of PalA levels. These results, together with an analysis of the biosynthetic potential of related microbiome taxa, describe a conserved, high-latitude core microbiome with unique composition and substantial promise for natural product biosynthesis that likely influences the ecology of the holobiont. |
| first_indexed | 2024-03-10T19:24:31Z |
| format | Article |
| id | doaj.art-2b8a2c2fe5d3479582a5a8baf73e92d3 |
| institution | Directory Open Access Journal |
| issn | 1660-3397 |
| language | English |
| last_indexed | 2024-03-10T19:24:31Z |
| publishDate | 2020-06-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Marine Drugs |
| spelling | doaj.art-2b8a2c2fe5d3479582a5a8baf73e92d32023-11-20T02:38:53ZengMDPI AGMarine Drugs1660-33972020-06-0118629810.3390/md18060298Uncovering the Core Microbiome and Distribution of Palmerolide in <i>Synoicum adareanum</i> Across the Anvers Island Archipelago, AntarcticaAlison E. Murray0Nicole E. Avalon1Lucas Bishop2Karen W. Davenport3Erwan Delage4Armand E.K. Dichosa5Damien Eveillard6Mary L. Higham7Sofia Kokkaliari8Chien-Chi Lo9Christian S. Riesenfeld10Ryan M. Young11Patrick S.G. Chain12Bill J. Baker13Division of Earth and Ecosystem Science, Desert Research Institute, Reno, NV 89512, USADepartment of Chemistry, University of South Florida, Tampa, FL 33620, USADivision of Earth and Ecosystem Science, Desert Research Institute, Reno, NV 89512, USABioscience Division, Los Alamos National Laboratory, Los Alamos, NM 87545, USALS2N, Université de Nantes, CNRS, 44322 Nantes, FranceBioscience Division, Los Alamos National Laboratory, Los Alamos, NM 87545, USALS2N, Université de Nantes, CNRS, 44322 Nantes, FranceDivision of Earth and Ecosystem Science, Desert Research Institute, Reno, NV 89512, USADepartment of Chemistry, University of South Florida, Tampa, FL 33620, USABioscience Division, Los Alamos National Laboratory, Los Alamos, NM 87545, USADivision of Earth and Ecosystem Science, Desert Research Institute, Reno, NV 89512, USADepartment of Chemistry, University of South Florida, Tampa, FL 33620, USABioscience Division, Los Alamos National Laboratory, Los Alamos, NM 87545, USADepartment of Chemistry, University of South Florida, Tampa, FL 33620, USAPolar marine ecosystems hold the potential for bioactive compound biodiscovery, based on their untapped macro- and microorganism diversity. Characterization of polar benthic marine invertebrate-associated microbiomes is limited to few studies. This study was motivated by our interest in better understanding the microbiome structure and composition of the ascidian, <i>Synoicum adareanum</i>, in which palmerolide A (PalA), a bioactive macrolide with specificity against melanoma, was isolated. PalA bears structural resemblance to a hybrid nonribosomal peptide-polyketide that has similarities to microbially-produced macrolides. We conducted a spatial survey to assess both PalA levels and microbiome composition in <i>S. adareanum</i> in a region of the Antarctic Peninsula near Anvers Island (64°46′ S, 64°03′ W). PalA was ubiquitous and abundant across a collection of 21 ascidians (3 subsamples each) sampled from seven sites across the Anvers Island Archipelago. The microbiome composition (V3–V4 16S rRNA gene sequence variants) of these 63 samples revealed a core suite of 21 bacterial amplicon sequence variants (ASVs)—20 of which were distinct from regional bacterioplankton. ASV co-occurrence analysis across all 63 samples yielded subgroups of taxa that may be interacting biologically (interacting subsystems) and, although the levels of PalA detected were not found to correlate with specific sequence variants, the core members appeared to occur in a preferred optimum and tolerance range of PalA levels. These results, together with an analysis of the biosynthetic potential of related microbiome taxa, describe a conserved, high-latitude core microbiome with unique composition and substantial promise for natural product biosynthesis that likely influences the ecology of the holobiont.https://www.mdpi.com/1660-3397/18/6/298Antarcticaascidianmicrobiomemicrobial diversitypalmerolide Aco-occurrence |
| spellingShingle | Alison E. Murray Nicole E. Avalon Lucas Bishop Karen W. Davenport Erwan Delage Armand E.K. Dichosa Damien Eveillard Mary L. Higham Sofia Kokkaliari Chien-Chi Lo Christian S. Riesenfeld Ryan M. Young Patrick S.G. Chain Bill J. Baker Uncovering the Core Microbiome and Distribution of Palmerolide in <i>Synoicum adareanum</i> Across the Anvers Island Archipelago, Antarctica Marine Drugs Antarctica ascidian microbiome microbial diversity palmerolide A co-occurrence |
| title | Uncovering the Core Microbiome and Distribution of Palmerolide in <i>Synoicum adareanum</i> Across the Anvers Island Archipelago, Antarctica |
| title_full | Uncovering the Core Microbiome and Distribution of Palmerolide in <i>Synoicum adareanum</i> Across the Anvers Island Archipelago, Antarctica |
| title_fullStr | Uncovering the Core Microbiome and Distribution of Palmerolide in <i>Synoicum adareanum</i> Across the Anvers Island Archipelago, Antarctica |
| title_full_unstemmed | Uncovering the Core Microbiome and Distribution of Palmerolide in <i>Synoicum adareanum</i> Across the Anvers Island Archipelago, Antarctica |
| title_short | Uncovering the Core Microbiome and Distribution of Palmerolide in <i>Synoicum adareanum</i> Across the Anvers Island Archipelago, Antarctica |
| title_sort | uncovering the core microbiome and distribution of palmerolide in i synoicum adareanum i across the anvers island archipelago antarctica |
| topic | Antarctica ascidian microbiome microbial diversity palmerolide A co-occurrence |
| url | https://www.mdpi.com/1660-3397/18/6/298 |
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