Divergent morphological and microbiome strategies of two neighbor sponges to cope with low pH in Mediterranean CO2 vents

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Ocean Acidification (OA) profoundly impacts marine biochemistry, resulting in a net loss of biodiversity. Porifera are often forecasted as winner taxa, yet the strategies to cope with OA can vary and may generate diverse fitness status. In this study, microbial shifts based on the V3–V4 16S rRNA gene marker were compared across neighboring Chondrosia reniformis sponges with high microbial abundance (HMA), and Spirastrella cunctatrix with low microbial abundance (LMA) microbiomes. Sponge holobionts co-occurred in a CO2 vent system with low pH (pHT ~ 7.65), and a control site with Ambient pH (pHT ~ 8.05) off Ischia Island, representing natural analogues to study future OA, and species' responses in the face of global environmental change. Microbial diversity and composition varied in both species across sites, yet at different levels. Increased numbers of core taxa were detected in S. cunctatrix, and a more diverse and flexible core microbiome was reported in C. reniformis under OA. Vent S. cunctatrix showed morphological impairment, along with signs of putative stress-induced dysbiosis, manifested by: 1) increases in alpha diversity, 2) shifts from sponge related microbes towards seawater microbes, and 3) high dysbiosis scores. Chondrosia reniformis in lieu, showed no morphological variation, low dysbiosis scores, and experienced a reduction in alpha diversity and less number of core taxa in vent specimens. Therefore, C. reniformis is hypothesized to maintain an state of normobiosis and acclimatize to OA, thanks to a more diverse, and likely metabolically versatile microbiome. A consortium of differentially abundant microbes was identified associated to either vent or control sponges, and chiefly related to carbon, nitrogen and sulfur-metabolisms for nutrient cycling and vitamin production, as well as probiotic symbionts in C. reniformis. Diversified symbiont associates supporting functional convergence could be the key behind resilience towards OA, yet specific acclimatization traits should be further investigated.