Expression of eukaryotic‐like protein in the microbiome of sponges

Abstract

Eukaryotic-like proteins (ELPs) are classes of proteins that are found in prokaryotes, but have a likely evolutionary origin in eukaryotes. ELPs have been postulated to mediate host-microbiome interactions. Recent work has discovered that prokaryotic symbionts of sponges contain abundant and diverse genes for ELPs, which could modulate interactions with their filter-feeding and phagocytic host. However, the extent to which these ELP genes are actually used and expressed by the symbionts is poorly understood. Here, we use metatranscriptomics to investigate ELP expression in the microbiomes of three different sponges (Cymbastella concentrica, Scopalina sp. and Tedania anhelens). We developed a workflow with optimized rRNA removal and in silico subtraction of host sequences to obtain a reliable symbiont metatranscriptome. This showed that between 1.3% and 2.3% of all symbiont transcripts contain genes for ELPs. Two classes of ELPs (cadherin and tetratricopeptide repeats) were abundantly expressed in the C. concentrica and Scopalina sp. microbiomes, while ankyrin repeat ELPs were predominant in the T. anhelens metatranscriptome. Comparison with transcripts that do not encode ELPs indicated a constitutive expression of ELPs across a range of bacterial and archaeal symbionts. Expressed ELPs also contained domains involved in protein secretion and/or were co-expressed with proteins involved in extracellular transport. This suggests these ELPs are likely exported, which could allow for direct interaction with the sponge. Our study shows that ELP genes in sponge symbionts represent actively expressed functions that could mediate molecular interaction between symbiosis partners.

Characterization of a thaumarchaeal symbiont that drives incomplete nitrification in the tropical spongeIanthella basta

“…N. ianthellae encodes a number of genes containing domains postulated to have an evolutionary origin within the eukaryotes and which are thought to be important for modulating interactions between bacteria and eukaryotic hosts (Callebaut et al ., ; Lurie‐Weinberger et al ., ; Patterson et al ., ). Recent metagenomic analyses revealed an abundance of genes encoding such eukaryotic‐like proteins (ELPs) in the bacterial symbionts of sponges (Fan et al ., ; Reynolds and Thomas, ; Díez‐Vives et al ., ), with many of these being expressed (Díez‐Vives et al ., ). Four types of ELPs are found in Ca .…”

Marine sponges as Chloroflexi hot-spots: Genomic insights and high resolution visualization of an abundant and diverse symbiotic clade

“…Eukaryotic-like proteins (ELPs) seem to be a general genomic feature of sponge symbionts (20, 50, 60, 61, 68–70). Particularly ankyrin (ANK), tetratricopeptide (TPR), and leucine-rich (LRR) repeat proteins are postulated to be involved in mediating host-microbe interactions (71, 72). Ankyrin and ankyrin repeat containing proteins were detected in all six genomes (Figure S5, Table S5A).…”

Understanding Animal Evolution: The Added Value of Sponge Transcriptomics and Genomics

“…More complete and updated taxonomy can be found on the Word Porifera Database . The names of species are written as follows: 1) in red, when transcriptomic and genomic analyses are already published (whether the corresponding databases are publicly available or not); 2) in violet, when transcriptome analyses are already published (whether the corresponding databases are publicly available or not) and there is a known* on‐going genome project; 3) in blue, when transcriptome analyses are already published (whether the corresponding databases are publicly available or not) and there is NO known* on‐going genome project; 4) in gray, when there are known* on‐going transcriptome and/or genome projects but not yet published sequence analyses (except on symbiotic content). *According to what was presented at the last World Sponge Conference (Galway, June 2017).…”