Too hot for my bugs: Mediterranean heatwaves disrupt associated microbiomes in the sponge Petrosia ficiformis

Background: Global 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 massive coral bleaching and mass mortalities of habitat-forming species, including 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 summers of 2022 and 2023, populations of the sponge Petrosia ficiformis (Poiret, 1789) were conspicuously observed with signs of thermal stress linked to MHWs 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 both MHWs, 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. Results: Prokaryotic community characterization based on the 16S 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 seeming opportunistic groups within Lentimicrobiaceae , Rhodobacteriaceae or Flavobacteriaceae . In lieu, preeminent association between healthy sponges and thermotolerant microbes (e.g., Rhodothermaceae ) could afford stress-tolerance during these disrupting events. Unhealthy microbiomes reflected lower interactome stability with respect to healthy holobionts, due to the inconsistency of functional keystone taxa and prevalence of transient microbes. Conclusions: Dysbiotic shifts due to colonization of scavenger groups and opportunistic microbes, and interconnectivity loss characterized thermally stressed sponges. In contrast, resistant phenotypes retained keystone symbionts that ensured interactome functionality, and displayed consistent partnership with thermoresistant taxa. The existence of stress-resistant phenotypes offers a shade of hope for species persistence, and their study may help identify potential source populations for ecosystem recovery.