Comparative Genomics Reveals Ecological and Evolutionary Insights into Sponge-Associated Thaumarchaeota

Area of Science:

• Marine microbiology
• Symbiotic evolution
• Genomics

Background:

• Marine sponges (phylum Porifera) frequently associate with Thaumarchaeota.
• Limited understanding of adaptations distinguishing sponge-associated Thaumarchaeota from free-living counterparts.
• Sponges serve as crucial models for studying metazoan-microbial symbiotic interactions.

Purpose of the Study:

• To reconstruct and analyze thaumarchaeal metagenome-assembled genomes (MAGs) from marine sponges.
• To identify genomic features and ecological roles of sponge-associated Thaumarchaeota.
• To gain evolutionary and ecological insights into sponge-thaumarchaeal symbiosis.

Main Methods:

• Reconstruction of thaumarchaeal MAGs from metagenomic data of three marine sponge species.
• Phylogenetic and taxonomic analyses to identify novel species and genera.
• Comparative genomic analysis of sponge-associated MAGs against free-living Thaumarchaeota and Sponge Earth Microbiome Project data.

Main Results:

• Three novel thaumarchaeal MAGs were identified, representing two new *Nitrosopumilus* species and one new genus: "*Ca*^U*Nitrosopumilus hexadellus*," "*Ca*^U*Nitrosopumilus detritiferus*," and "*Ca*^U*Cenporiarchaeum stylissum*."
• "*Ca*^U*Cenporiarchaeum stylissum*" is a sponge specialist, while "*Ca*^U*Nitrosopumilus detritiferus*" and "*Ca*^U*Nitrosopumilus hexadellus*" exhibit generalist lifestyles.
• Sponge-associated Thaumarchaeota possess distinct functional traits related to nutrient transport, metabolism, defense, and host interactions, indicating varying evolutionary adaptations and ecological niches.

Conclusions:

• Thaumarchaeota exhibit diverse strategies for associating with marine sponges, ranging from specialized to generalist lifestyles.
• Genomic analysis reveals specific adaptations in sponge-associated Thaumarchaeota for nutrient metabolism and host interaction.
• The study provides significant evolutionary and ecological insights into the complex symbiosis between sponges and Thaumarchaeota.