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

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.

Cultivation of Sponge-Associated Bacteria from Agelas sventres and Xestospongia muta Collected from Different Depths

“…The latter is a recurring issue in attempts to isolate dominant representatives of sponge-associated bacteria that reside in the inner part of the sponge tissues (mesohyl) [14,38,40,41,42] and has often been explained by the recovery of isolates that were present in low numbers in the canal systems and choanocyte chambers of sponges before processing [14,16,40]. The failure to recover the bacteria abundant in the sponge in the laboratory stresses that new cultivation approaches where metabolic capacities of sponge-associated bacteria—partly unveiled by recent metagenomics studies—are integrated need to be implemented [43,44,45,46,47].…”

Diversity of tryptophan halogenases in sponges of the genus Aplysina

“…Nonetheless, Nitrospinae are closely related to the candidate phylum Tectomicrobia, which occurs in Aplysina species (Chaib De Mares et al . 2018) and of which some members are renowned for their large secondary metabolism gene repertoire (Wilson et al . 2014; Smith et al .…”

“…Sequences were clustered at 95% amino acid sequence identity based on the average protein sequence identity in genomes of the same bacterial species (Rodriguez-R and Konstantinidis 2014; Chaib De Mares et al . 2018) using the uclust algorithm (Edgar 2010). The most abundant sequence per cluster was retained as representative sequence.…”

Cultivation of Bacteria From Aplysina aerophoba: Effects of Oxygen and Nutrient Gradients

“…Marine sponges represent the oldest, living lineage of the animal kingdom, with a longstanding association to microorganisms (Hooper and Van Soest, 2012;McFall-Ngai et al, 2013). To date, 41 prokaryotic phyla have been found in association with sponges and accordingly, this vast genetic potential is hypothesized to be accountable for numerous interactions between sponge symbionts and their hosts (Webster and Moitinho-Silva et al, 2017;Chaib De Mares et al, 2018). In recent years, omics-based methods (Horn et al, 2016;Slaby et al, 2017) as well as physiological in situ studies have shed some light on microbial processes in sponges Becerro et al, 2012).…”