Expressed protein profile of a Tectomicrobium and other microbial symbionts in the marine sponge Aplysina aerophoba as evidenced by metaproteomics

Maryam Chaib De Mares,Paul Wilmes,Jan Dirk Van Elsas,Giorgia Palladino,Detmer Sipkema,Emilie E L Muller,Diego Javier Jiménez,Laura A Lebrun,Johanna Gutleben

doi:10.1038/s41598-018-30134-0

Abstract

Aplysina aerophoba is an emerging model marine sponge, with a well-characterized microbial community in terms of diversity and structure. However, little is known about the expressed functional capabilities of its associated microbes. Here, we present the first metaproteomics-based study of the microbiome of A. aerophoba. We found that transport and degradation of halogenated and chloroaromatic compounds are common active processes in the sponge microbiomes. Our data further reveal that the highest number of proteins were affiliated to a sponge-associated Tectomicrobium, presumably from the family Entotheonellaceae, as well as to the well-known symbiont “Candidatus Synechococcus spongiarium”, suggesting a high metabolic activity of these two microorganisms in situ. Evidence for nitric oxide (NO) conversion to nitrous oxide was consistently observed for Tectomicrobia across replicates, by production of the NorQ protein. Moreover, we found a potential energy-yielding pathway through CO oxidation by putative Chloroflexi bacteria. Finally, we observed expression of enzymes that may be involved in the transformation of chitin, glycoproteins, glycolipids and glucans into smaller molecules, consistent with glycosyl hydrolases predicted from analyses of the genomes of Poribacteria sponge symbionts. Thus, this study provides crucial links between expressed proteins and specific members of the A. aerophoba microbiome.

Highlights

IntroductionSponges (phylum Porifera) have been documented as complex environments hosting microbial representatives from all three domains of life
Sponges have been documented as complex environments hosting microbial representatives from all three domains of life1,2
The resulting peptides were matched against predicted proteins from two metagenomic assemblies, one per habitat

Summary

Introduction

Sponges (phylum Porifera) have been documented as complex environments hosting microbial representatives from all three domains of life. In particular in HMA sponges, many of the associated microbes are understood as an essential part of the sponge This typically includes bacterial and archaeal clades found only in marine sponges. Even though the prokaryotic diversity and composition within A. aerophoba is known at a rather broad level, we understand much less regarding the active functional profile of the sponge-associated microbiome. The reasons are twofold: most sponge-associated microbes have not been brought into culture, and culture-independent ‘omics’ methods have only recently started to be applied to sponges The latter methods can provide us with either an overview of functions present (i.e. through metagenomics or single cell genomics); or of realized (active) functions (using for instance metatranscriptomics and/or metaproteomics). A draft genome of the sponge-associated “Candidatus Synechococcus spongiarum” from A. aerophoba is available

Methods

Results

Conclusion