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Abstract

Sponges host a remarkable diversity of microbial symbionts, however, the
benefit their microbes provide is rarely understood. Here, we describe
two new sponge species from deep-sea asphalt seeps and show that they
live in a nutritional symbiosis with methane-oxidizing (MOX) bacteria.
Metagenomics and imaging analyses revealed unusually high amounts of MOX
symbionts in hosts from a group previously assumed to have low microbial
abundances. These symbionts belonged to the Marine Methylotrophic Group
2 Glade. They are host-specific and likely vertically transmitted, based
on their presence in sponge embryos and streamlined genomes, which
lacked genes typical of related free-living MOX. Moreover, genes known
to play a role in host-symbiont interactions, such as those that encode
eukaryote-like proteins, were abundant and expressed. Methane
assimilation by the symbionts was one of the most highly expressed
metabolic pathways in the sponges. Molecular and stable carbon isotope
patterns of lipids confirmed that methane-derived carbon was
incorporated into the hosts. Our results revealed that two species of
sponges, although distantly related, independently established highly
specific, nutritional symbioses with two closely related methanotrophs.
This convergence in symbiont acquisition underscores the strong
selective advantage for these sponges in harboring MOX bacteria in the
food-limited deep sea.