Single-bacterial genomics validates rich and varied specialized metabolism of uncultivated Entotheonella sponge symbionts

Author:

Mori Tetsushi,Cahn Jackson K. B.,Wilson Micheal C.,Meoded Roy A.,Wiebach Vincent,Martinez Ana Flávia Canovas,Helfrich Eric J. N.,Albersmeier Andreas,Wibberg Daniel,Dätwyler Steven,Keren Ray,Lavy Adi,Rückert Christian,Ilan Micha,Kalinowski Jörn,Matsunaga Shigeki,Takeyama Haruko,Piel Jörn

Abstract

Marine sponges are prolific sources of unique bioactive natural products. The sponge Theonella swinhoei is represented by several distinct variants with largely nonoverlapping chemistry. For the Japanese chemotype Y harboring diverse complex polyketides and peptides, we previously provided genomic and functional evidence that a single symbiont, the filamentous, multicellular organism “Candidatus Entotheonella factor,” produces almost all of these compounds. To obtain further insights into the chemistry of “Entotheonella,” we investigated another phylotype, “Candidatus Entotheonella serta,” present in the T. swinhoei WA sponge chemotype, a source of theonellamide- and misakinolide-type compounds. Unexpectedly, considering the lower chemical diversity, sequencing of individual bacterial filaments revealed an even larger number of biosynthetic gene regions than for Ca. E. factor, with virtually no overlap. These included genes for misakinolide and theonellamide biosynthesis, the latter assigned by comparative genomic and metabolic analysis of a T. swinhoei chemotype from Israel, and by biochemical studies. The data suggest that both compound families, which were among the earliest model substances to study bacterial producers in sponges, originate from the same bacterium in T. swinhoei WA. They also add evidence that metabolic richness and variability could be a more general feature of Entotheonella symbionts.

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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