Too hot for my bugs: mediterranean heatwave disrupts associated microbiomes in the sponge Petrosia ficiformis.

backgroundGlobal climate change exacerbates the incidence of marine heatwaves (MHWs), which have increased in intensity and frequency over the past years, causing severe impacts on marine coastal ecosystems. MHWs have already triggered mass mortalities of habitat-forming species, including corals, sponges and gorgonians, in temperate, tropical and polar seas. In the Mediterranean, these high peaks of temperature have been shown to affect several sponge species, and likely, their symbiotic microbial communities. During the summer of 2022, populations of the sponge Petrosia ficiformis (Poiret, 1789) were conspicuously observed with signs of thermal stress linked to a MHW around the Gulf of Naples (Tyrrhenian Sea, Italy). These included depigmentation spots and tissue texture alterations, which often evolved in necrotic processes and eventual death. At the peak of the MHW, however, apparently thermoresistant sponges co-occurred with sensitive unhealthy specimens. In order to explore potential microbial drivers correlated with these divergent thermal-stress tolerances, Healthy and Unhealthy individuals were sampled along the coast of Ischia Island in early September 2022.

resultsProkaryotic community characterization based on the 16 S rRNA gene revealed dissimilar compositions in Unhealthy versus apparently Healthy sponges. Increased alpha diversity richness and low evenness in thermosensitive sponges were due to an extensive presence of rare taxa, and to the introduction of potentially pathogenic groups (e.g., Vibrio spp.). Major microbial families regularly associated with P. ficiformis - SAR202, Caldilineaceae, Poribacteria or TK17, were replaced in thermosensitive specimens by professed opportunistic groups within Lentimicrobiaceae, Rhodobacteraceae or Flavobacteriaceae. In turn, conservancy of hub microbes and thermotolerant symbionts (e.g., Rhodothermaceae, Thermoanaerobaculaceae) in Healthy sponges were observed during this disrupting event. Unhealthy microbiomes reflected lower network stability with respect to Healthy holobionts, due to the inconsistency of functional keystone taxa and prevalence of transient microbes.

conclusionsDysbiotic shifts due to colonization of scavenger groups and opportunistic microbes, and interconnectivity loss characterized thermally stressed sponges. In contrast, resistant specimens retained keystone symbionts that could have ensured functional cooperation, and maintenance of prokaryotic community cohesion under thermal stress. The existence of stress-resistant phenotypes in sponge holobionts offers a glimmer of hope for species persistence, and their study may identify potential source populations for ecosystem recovery.