Comparative Genomics Reveals Ecological and Evolutionary Insights into Sponge-Associated <italic toggle="yes">Thaumarchaeota</italic>

ABSTRACT Thaumarchaeota are frequently reported to associate with marine sponges (phylum Porifera); however, little is known about the features that distinguish them from their free-living thaumarchaeal counterparts. In this study, thaumarchaeal metagenome-assembled genomes (MAGs) were reconstructed...

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Autores principales:	Shan Zhang, Weizhi Song, Bernd Wemheuer, Julie Reveillaud, Nicole Webster, Torsten Thomas
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	evolution genetic features host associated sponge microbiome symbionts Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/79c42aec14294963970e0073f2e6fbae
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spelling	oai:doaj.org-article:79c42aec14294963970e0073f2e6fbae2021-12-02T19:47:38ZComparative Genomics Reveals Ecological and Evolutionary Insights into Sponge-Associated <italic toggle="yes">Thaumarchaeota</italic>10.1128/mSystems.00288-192379-5077https://doaj.org/article/79c42aec14294963970e0073f2e6fbae2019-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00288-19https://doaj.org/toc/2379-5077ABSTRACT Thaumarchaeota are frequently reported to associate with marine sponges (phylum Porifera); however, little is known about the features that distinguish them from their free-living thaumarchaeal counterparts. In this study, thaumarchaeal metagenome-assembled genomes (MAGs) were reconstructed from metagenomic data sets derived from the marine sponges Hexadella detritifera, Hexadella cf. detritifera, and Stylissa flabelliformis. Phylogenetic and taxonomic analyses revealed that the three thaumarchaeal MAGs represent two new species within the genus Nitrosopumilus and one novel genus, for which we propose the names “Candidatus UNitrosopumilus hexadellus,” “Candidatus UNitrosopumilus detritiferus,” and “Candidatus UCenporiarchaeum stylissum” (the U superscript indicates that the taxon is uncultured). Comparison of these genomes to data from the Sponge Earth Microbiome Project revealed that “Ca. UCenporiarchaeum stylissum” has been exclusively detected in sponges and can hence be classified as a specialist, while “Ca. UNitrosopumilus detritiferus” and “Ca. UNitrosopumilus hexadellus” are also detected outside the sponge holobiont and likely lead a generalist lifestyle. Comparison of the sponge-associated MAGs to genomes of free-living Thaumarchaeota revealed signatures that indicate functional features of a sponge-associated lifestyle, and these features were related to nutrient transport and metabolism, restriction-modification, defense mechanisms, and host interactions. Each species exhibited distinct functional traits, suggesting that they have reached different stages of evolutionary adaptation and/or occupy distinct ecological niches within their sponge hosts. Our study therefore offers new evolutionary and ecological insights into the symbiosis between sponges and their thaumarchaeal symbionts. IMPORTANCE Sponges represent ecologically important models to understand the evolution of symbiotic interactions of metazoans with microbial symbionts. Thaumarchaeota are commonly found in sponges, but their potential adaptations to a host-associated lifestyle are largely unknown. Here, we present three novel sponge-associated thaumarchaeal species and compare their genomic and predicted functional features with those of closely related free-living counterparts. We found different degrees of specialization of these thaumarchaeal species to the sponge environment that is reflected in their host distribution and their predicted molecular and metabolic properties. Our results indicate that Thaumarchaeota may have reached different stages of evolutionary adaptation in their symbiosis with sponges.Shan ZhangWeizhi SongBernd WemheuerJulie ReveillaudNicole WebsterTorsten ThomasAmerican Society for Microbiologyarticleevolutiongenetic featureshost associatedsponge microbiomesymbiontsMicrobiologyQR1-502ENmSystems, Vol 4, Iss 4 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	evolution genetic features host associated sponge microbiome symbionts Microbiology QR1-502
spellingShingle	evolution genetic features host associated sponge microbiome symbionts Microbiology QR1-502 Shan Zhang Weizhi Song Bernd Wemheuer Julie Reveillaud Nicole Webster Torsten Thomas Comparative Genomics Reveals Ecological and Evolutionary Insights into Sponge-Associated <italic toggle="yes">Thaumarchaeota</italic>
description	ABSTRACT Thaumarchaeota are frequently reported to associate with marine sponges (phylum Porifera); however, little is known about the features that distinguish them from their free-living thaumarchaeal counterparts. In this study, thaumarchaeal metagenome-assembled genomes (MAGs) were reconstructed from metagenomic data sets derived from the marine sponges Hexadella detritifera, Hexadella cf. detritifera, and Stylissa flabelliformis. Phylogenetic and taxonomic analyses revealed that the three thaumarchaeal MAGs represent two new species within the genus Nitrosopumilus and one novel genus, for which we propose the names “Candidatus UNitrosopumilus hexadellus,” “Candidatus UNitrosopumilus detritiferus,” and “Candidatus UCenporiarchaeum stylissum” (the U superscript indicates that the taxon is uncultured). Comparison of these genomes to data from the Sponge Earth Microbiome Project revealed that “Ca. UCenporiarchaeum stylissum” has been exclusively detected in sponges and can hence be classified as a specialist, while “Ca. UNitrosopumilus detritiferus” and “Ca. UNitrosopumilus hexadellus” are also detected outside the sponge holobiont and likely lead a generalist lifestyle. Comparison of the sponge-associated MAGs to genomes of free-living Thaumarchaeota revealed signatures that indicate functional features of a sponge-associated lifestyle, and these features were related to nutrient transport and metabolism, restriction-modification, defense mechanisms, and host interactions. Each species exhibited distinct functional traits, suggesting that they have reached different stages of evolutionary adaptation and/or occupy distinct ecological niches within their sponge hosts. Our study therefore offers new evolutionary and ecological insights into the symbiosis between sponges and their thaumarchaeal symbionts. IMPORTANCE Sponges represent ecologically important models to understand the evolution of symbiotic interactions of metazoans with microbial symbionts. Thaumarchaeota are commonly found in sponges, but their potential adaptations to a host-associated lifestyle are largely unknown. Here, we present three novel sponge-associated thaumarchaeal species and compare their genomic and predicted functional features with those of closely related free-living counterparts. We found different degrees of specialization of these thaumarchaeal species to the sponge environment that is reflected in their host distribution and their predicted molecular and metabolic properties. Our results indicate that Thaumarchaeota may have reached different stages of evolutionary adaptation in their symbiosis with sponges.
format	article
author	Shan Zhang Weizhi Song Bernd Wemheuer Julie Reveillaud Nicole Webster Torsten Thomas
author_facet	Shan Zhang Weizhi Song Bernd Wemheuer Julie Reveillaud Nicole Webster Torsten Thomas
author_sort	Shan Zhang
title	Comparative Genomics Reveals Ecological and Evolutionary Insights into Sponge-Associated <italic toggle="yes">Thaumarchaeota</italic>
title_short	Comparative Genomics Reveals Ecological and Evolutionary Insights into Sponge-Associated <italic toggle="yes">Thaumarchaeota</italic>
title_full	Comparative Genomics Reveals Ecological and Evolutionary Insights into Sponge-Associated <italic toggle="yes">Thaumarchaeota</italic>
title_fullStr	Comparative Genomics Reveals Ecological and Evolutionary Insights into Sponge-Associated <italic toggle="yes">Thaumarchaeota</italic>
title_full_unstemmed	Comparative Genomics Reveals Ecological and Evolutionary Insights into Sponge-Associated <italic toggle="yes">Thaumarchaeota</italic>
title_sort	comparative genomics reveals ecological and evolutionary insights into sponge-associated <italic toggle="yes">thaumarchaeota</italic>
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/79c42aec14294963970e0073f2e6fbae
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Comparative Genomics Reveals Ecological and Evolutionary Insights into Sponge-Associated <italic toggle="yes">Thaumarchaeota</italic>

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