Presence of Bromotyrosine Alkaloids in Marine Sponges Is Independent of Metabolomic and Microbiome Architectures

ABSTRACT Marine sponge holobionts are prolific sources of natural products. One of the most geographically widespread classes of sponge-derived natural products is the bromotyrosine alkaloids. A distinguishing feature of bromotyrosine alkaloids is that they are present in phylogenetically disparate...

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Autores principales:	Ipsita Mohanty, Subhasish Tapadar, Samuel G. Moore, Jason S. Biggs, Christopher J. Freeman, David A. Gaul, Neha Garg, Vinayak Agarwal
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	marine sponge metabolomics mass spectrometry microbiome natural products Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/4e78252f7ad4462f95127cfd195f05bd
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spelling	oai:doaj.org-article:4e78252f7ad4462f95127cfd195f05bd2021-12-02T19:22:27ZPresence of Bromotyrosine Alkaloids in Marine Sponges Is Independent of Metabolomic and Microbiome Architectures10.1128/mSystems.01387-202379-5077https://doaj.org/article/4e78252f7ad4462f95127cfd195f05bd2021-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.01387-20https://doaj.org/toc/2379-5077ABSTRACT Marine sponge holobionts are prolific sources of natural products. One of the most geographically widespread classes of sponge-derived natural products is the bromotyrosine alkaloids. A distinguishing feature of bromotyrosine alkaloids is that they are present in phylogenetically disparate sponges. In this study, using sponge specimens collected from Guam, the Solomon Islands, the Florida Keys, and Puerto Rico, we queried whether the presence of bromotyrosine alkaloids potentiates metabolomic and microbiome conservation among geographically distant and phylogenetically different marine sponges. A multi-omic characterization of sponge holobionts revealed vastly different metabolomic and microbiome architectures among different bromotyrosine alkaloid-harboring sponges. However, we find statistically significant correlations between the microbiomes and metabolomes, signifying that the microbiome plays an important role in shaping the overall metabolome, even in low-microbial-abundance sponges. Molecules mined from the polar metabolomes of these sponges revealed conservation of biosynthetic logic between bromotyrosine alkaloids and brominated pyrrole-imidazole alkaloids, another class of marine sponge-derived natural products. In light of prior findings postulating the sponge host itself to be the biosynthetic source of bromotyrosine alkaloids, our data now set the stage for investigating the causal relationships that dictate the microbiome-metabolome interconnectedness for marine sponges in which the microbiome may not contribute to natural product biogenesis. IMPORTANCE Our work demonstrates that phylogenetically and geographically distant sponges with very different microbiomes can harbor natural product chemical classes that are united in their core chemical structures and biosynthetic logic. Furthermore, we show that independent of geographical dispersion, natural product chemistry, and microbial abundance, overall sponge metabolomes tightly correlate with their microbiomes.Ipsita MohantySubhasish TapadarSamuel G. MooreJason S. BiggsChristopher J. FreemanDavid A. GaulNeha GargVinayak AgarwalAmerican Society for Microbiologyarticlemarine spongemetabolomicsmass spectrometrymicrobiomenatural productsMicrobiologyQR1-502ENmSystems, Vol 6, Iss 2 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	marine sponge metabolomics mass spectrometry microbiome natural products Microbiology QR1-502
spellingShingle	marine sponge metabolomics mass spectrometry microbiome natural products Microbiology QR1-502 Ipsita Mohanty Subhasish Tapadar Samuel G. Moore Jason S. Biggs Christopher J. Freeman David A. Gaul Neha Garg Vinayak Agarwal Presence of Bromotyrosine Alkaloids in Marine Sponges Is Independent of Metabolomic and Microbiome Architectures
description	ABSTRACT Marine sponge holobionts are prolific sources of natural products. One of the most geographically widespread classes of sponge-derived natural products is the bromotyrosine alkaloids. A distinguishing feature of bromotyrosine alkaloids is that they are present in phylogenetically disparate sponges. In this study, using sponge specimens collected from Guam, the Solomon Islands, the Florida Keys, and Puerto Rico, we queried whether the presence of bromotyrosine alkaloids potentiates metabolomic and microbiome conservation among geographically distant and phylogenetically different marine sponges. A multi-omic characterization of sponge holobionts revealed vastly different metabolomic and microbiome architectures among different bromotyrosine alkaloid-harboring sponges. However, we find statistically significant correlations between the microbiomes and metabolomes, signifying that the microbiome plays an important role in shaping the overall metabolome, even in low-microbial-abundance sponges. Molecules mined from the polar metabolomes of these sponges revealed conservation of biosynthetic logic between bromotyrosine alkaloids and brominated pyrrole-imidazole alkaloids, another class of marine sponge-derived natural products. In light of prior findings postulating the sponge host itself to be the biosynthetic source of bromotyrosine alkaloids, our data now set the stage for investigating the causal relationships that dictate the microbiome-metabolome interconnectedness for marine sponges in which the microbiome may not contribute to natural product biogenesis. IMPORTANCE Our work demonstrates that phylogenetically and geographically distant sponges with very different microbiomes can harbor natural product chemical classes that are united in their core chemical structures and biosynthetic logic. Furthermore, we show that independent of geographical dispersion, natural product chemistry, and microbial abundance, overall sponge metabolomes tightly correlate with their microbiomes.
format	article
author	Ipsita Mohanty Subhasish Tapadar Samuel G. Moore Jason S. Biggs Christopher J. Freeman David A. Gaul Neha Garg Vinayak Agarwal
author_facet	Ipsita Mohanty Subhasish Tapadar Samuel G. Moore Jason S. Biggs Christopher J. Freeman David A. Gaul Neha Garg Vinayak Agarwal
author_sort	Ipsita Mohanty
title	Presence of Bromotyrosine Alkaloids in Marine Sponges Is Independent of Metabolomic and Microbiome Architectures
title_short	Presence of Bromotyrosine Alkaloids in Marine Sponges Is Independent of Metabolomic and Microbiome Architectures
title_full	Presence of Bromotyrosine Alkaloids in Marine Sponges Is Independent of Metabolomic and Microbiome Architectures
title_fullStr	Presence of Bromotyrosine Alkaloids in Marine Sponges Is Independent of Metabolomic and Microbiome Architectures
title_full_unstemmed	Presence of Bromotyrosine Alkaloids in Marine Sponges Is Independent of Metabolomic and Microbiome Architectures
title_sort	presence of bromotyrosine alkaloids in marine sponges is independent of metabolomic and microbiome architectures
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/4e78252f7ad4462f95127cfd195f05bd
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Presence of Bromotyrosine Alkaloids in Marine Sponges Is Independent of Metabolomic and Microbiome Architectures

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