Marine karst ecosystems exist at the land-sea interface and are characterised by underwater formations sculpted over time by the action of seawater. Submerged caves and crevices of these ecosystems host a rich array of marine life of which sponges are among the most abundant and diverse components. In the present study, we describe elements of the sponge fauna sampled from a unique karst ecosystem at a remote island, Orchid Island, off the southeastern coast of Taiwan. The present study includes several understudied sponge taxa, including sclerosponges (Acanthochaetetes wellsi, and Astrosclera willeyana) and several lithistid species from dark, shallow-water caves. Prokaryotic communities were obtained from a total of 22 demosponge species, of which 11 are potentially new to science. The tetracladinid, lithistids harboured prokaryotic communities, which clustered separately from all other sponge species, contrasting with the non-tetracladinid, lithistid Vetulina incrustans. The tetracladinid, lithistids, furthermore, formed two distinct clusters with species of the Spirophorina suborder clustering apart from those of the Astrophorina suborder. The sclerosponge A. wellsi also harboured a distinct prokaryotic community in terms of composition including five unique, abundant OTUs with relatively low sequence similarities to organisms in GenBank. All cave sponges were enriched with SAR202 members, a group of bacteria known for their role in the degradation of recalcitrant compounds. The highest relative abundance of SAR202 was found in A. wellsi. We propose that the cave sponges of Orchid Island may play an as-yet uncharted role in nutrient dynamics at the land-sea interface.