Hidden in plain sight: a novel symbiotic haplosclerid sponge species revealed by its mitochondrial genome

Sponges (phylum Porifera) are known to form symbiotic relationships with a variety of organisms, including other sponges. Recently, such symbiosis has been described between two homoscleromorph species (Plakortis symbiotica and P. deweerdtaephila) and two representatives of the demosponge order Haplosclerida (Xestospongia deweerdtae and Haliclona plakophila). While studying genomic data from the H. plakophila-P. symbiotica association, we discovered an unusual third mitochondrial genome (mitogenome). Additional sampling conducted for this study revealed that this genome belongs to a new species of Haplosclerida, which we name Metilla boricua  gen. nov. sp. nov. Here we describe this new species along with its mitogenome. While M. boricua is superficially similar to H. plakophila, it can be distinguished both by skeletal organization and spicule composition. Its mitogenome is also highly unusual, featuring an elevated GC content and missing the cox2 gene. Phylogenetic analyses based on nuclear 18S and 28S gene sequences place M. boricua into a poorly sampled clade F within the order Haplosclerida. We also report the mitogenome of symbiotic haplosclerid X. deweerdtae, which we sequenced before the new species was identified. Our results support three independent origins of Haplosclerida-Plakortis symbiosis, a finding that redefines the context for future investigation of these relationships.