Cargando…

Uncovering the Core Microbiome and Distribution of Palmerolide in Synoicum adareanum 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...

Descripción completa

Detalles Bibliográficos
Autores principales: Murray, Alison E., Avalon, Nicole E., Bishop, Lucas, Davenport, Karen W., Delage, Erwan, Dichosa, Armand E.K., Eveillard, Damien, Higham, Mary L., Kokkaliari, Sofia, Lo, Chien-Chi, Riesenfeld, Christian S., Young, Ryan M., Chain, Patrick S.G., Baker, Bill J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7345734/
https://www.ncbi.nlm.nih.gov/pubmed/32498449
http://dx.doi.org/10.3390/md18060298
_version_ 1783556252882698240
author Murray, Alison E.
Avalon, Nicole E.
Bishop, Lucas
Davenport, Karen W.
Delage, Erwan
Dichosa, Armand E.K.
Eveillard, Damien
Higham, Mary L.
Kokkaliari, Sofia
Lo, Chien-Chi
Riesenfeld, Christian S.
Young, Ryan M.
Chain, Patrick S.G.
Baker, Bill J.
author_facet Murray, Alison E.
Avalon, Nicole E.
Bishop, Lucas
Davenport, Karen W.
Delage, Erwan
Dichosa, Armand E.K.
Eveillard, Damien
Higham, Mary L.
Kokkaliari, Sofia
Lo, Chien-Chi
Riesenfeld, Christian S.
Young, Ryan M.
Chain, Patrick S.G.
Baker, Bill J.
author_sort Murray, Alison E.
collection PubMed
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, Synoicum adareanum, 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 S. adareanum 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.
format Online
Article
Text
id pubmed-7345734
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher MDPI
record_format MEDLINE/PubMed
spelling pubmed-73457342020-07-09 Uncovering the Core Microbiome and Distribution of Palmerolide in Synoicum adareanum Across the Anvers Island Archipelago, Antarctica Murray, Alison E. Avalon, Nicole E. Bishop, Lucas Davenport, Karen W. Delage, Erwan Dichosa, Armand E.K. Eveillard, Damien Higham, Mary L. Kokkaliari, Sofia Lo, Chien-Chi Riesenfeld, Christian S. Young, Ryan M. Chain, Patrick S.G. Baker, Bill J. Mar Drugs Article 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, Synoicum adareanum, 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 S. adareanum 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. MDPI 2020-06-02 /pmc/articles/PMC7345734/ /pubmed/32498449 http://dx.doi.org/10.3390/md18060298 Text en © 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Murray, Alison E.
Avalon, Nicole E.
Bishop, Lucas
Davenport, Karen W.
Delage, Erwan
Dichosa, Armand E.K.
Eveillard, Damien
Higham, Mary L.
Kokkaliari, Sofia
Lo, Chien-Chi
Riesenfeld, Christian S.
Young, Ryan M.
Chain, Patrick S.G.
Baker, Bill J.
Uncovering the Core Microbiome and Distribution of Palmerolide in Synoicum adareanum Across the Anvers Island Archipelago, Antarctica
title Uncovering the Core Microbiome and Distribution of Palmerolide in Synoicum adareanum Across the Anvers Island Archipelago, Antarctica
title_full Uncovering the Core Microbiome and Distribution of Palmerolide in Synoicum adareanum Across the Anvers Island Archipelago, Antarctica
title_fullStr Uncovering the Core Microbiome and Distribution of Palmerolide in Synoicum adareanum Across the Anvers Island Archipelago, Antarctica
title_full_unstemmed Uncovering the Core Microbiome and Distribution of Palmerolide in Synoicum adareanum Across the Anvers Island Archipelago, Antarctica
title_short Uncovering the Core Microbiome and Distribution of Palmerolide in Synoicum adareanum Across the Anvers Island Archipelago, Antarctica
title_sort uncovering the core microbiome and distribution of palmerolide in synoicum adareanum across the anvers island archipelago, antarctica
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7345734/
https://www.ncbi.nlm.nih.gov/pubmed/32498449
http://dx.doi.org/10.3390/md18060298
work_keys_str_mv AT murrayalisone uncoveringthecoremicrobiomeanddistributionofpalmerolideinsynoicumadareanumacrosstheanversislandarchipelagoantarctica
AT avalonnicolee uncoveringthecoremicrobiomeanddistributionofpalmerolideinsynoicumadareanumacrosstheanversislandarchipelagoantarctica
AT bishoplucas uncoveringthecoremicrobiomeanddistributionofpalmerolideinsynoicumadareanumacrosstheanversislandarchipelagoantarctica
AT davenportkarenw uncoveringthecoremicrobiomeanddistributionofpalmerolideinsynoicumadareanumacrosstheanversislandarchipelagoantarctica
AT delageerwan uncoveringthecoremicrobiomeanddistributionofpalmerolideinsynoicumadareanumacrosstheanversislandarchipelagoantarctica
AT dichosaarmandek uncoveringthecoremicrobiomeanddistributionofpalmerolideinsynoicumadareanumacrosstheanversislandarchipelagoantarctica
AT eveillarddamien uncoveringthecoremicrobiomeanddistributionofpalmerolideinsynoicumadareanumacrosstheanversislandarchipelagoantarctica
AT highammaryl uncoveringthecoremicrobiomeanddistributionofpalmerolideinsynoicumadareanumacrosstheanversislandarchipelagoantarctica
AT kokkaliarisofia uncoveringthecoremicrobiomeanddistributionofpalmerolideinsynoicumadareanumacrosstheanversislandarchipelagoantarctica
AT lochienchi uncoveringthecoremicrobiomeanddistributionofpalmerolideinsynoicumadareanumacrosstheanversislandarchipelagoantarctica
AT riesenfeldchristians uncoveringthecoremicrobiomeanddistributionofpalmerolideinsynoicumadareanumacrosstheanversislandarchipelagoantarctica
AT youngryanm uncoveringthecoremicrobiomeanddistributionofpalmerolideinsynoicumadareanumacrosstheanversislandarchipelagoantarctica
AT chainpatricksg uncoveringthecoremicrobiomeanddistributionofpalmerolideinsynoicumadareanumacrosstheanversislandarchipelagoantarctica
AT bakerbillj uncoveringthecoremicrobiomeanddistributionofpalmerolideinsynoicumadareanumacrosstheanversislandarchipelagoantarctica