Validation of key sponge symbiont pathways using genome-centric metatranscriptomics

Area of Science:

• Marine biology
• Microbial ecology
• Symbiotic interactions

Background:

• Sponge microbiomes are crucial for nutrient cycling in nutrient-limited marine environments.
• Genomic data suggest key microbial roles in carbohydrate degradation, carbon fixation, nitrogen and sulfur metabolism, and B-vitamin synthesis.
• Limited experimental validation exists for predicted microbial functions within sponge holobionts.

Purpose of the Study:

• To validate metagenomic predictions of sponge microbiome functions using metatranscriptomics.
• To investigate the active metabolic roles of symbionts in three coral reef sponge species.
• To compare gene expression profiles with genomic potential for nutrient cycling pathways.

Main Methods:

• Sequencing of metagenomes and metatranscriptomes from three sponge species: Ircinia ramosa, Ircinia microconulosa, and Phyllospongia foliascens.
• Analysis of gene expression for carbohydrate active enzymes, carbon fixation, nitrogen metabolism (nitrification, denitrification), sulfur compound transformations, and B-vitamin synthesis and transport.
• Comparison of metatranscriptomic data with existing metagenomic data to infer microbial activity.

Main Results:

• Expression of carbohydrate-degrading enzymes by Poribacteria, Bacteroidota, and Cyanobacteria symbionts, indicating dissolved organic matter assimilation.
• Widespread expression of carbon fixation and sulfur metabolism pathways across all studied sponges.
• Predominance of anaerobic nitrogen metabolism (denitrification, nitrate reduction) over aerobic nitrification, with nitrification observed only in I. ramosa.
• Common expression of B-vitamin biosynthetic pathways, but limited expression of associated transporter genes.

Conclusions:

• Metatranscriptomics provides crucial validation and reveals disparities compared to metagenomic predictions of sponge microbiome functions.
• Microbial symbionts actively contribute to nutrient cycling, including carbon, nitrogen, sulfur, and B-vitamins, supporting sponge host health.
• New microbial taxa involved in nutrient exchange and sponge symbiosis were identified.