Rhodoliths holobionts in a changing ocean: Host-microbes interactions mediate coralline algae resilience under ocean acidification

Background: Life in the ocean will increasingly have to contend with a complex matrix of concurrent shifts in environmental properties that impact their physiology and control their life histories. Rhodoliths are coralline red algae (Corallinales, Rhodophyta) that are photosynthesizers, calcifiers, and ecosystem engineers and therefore represent important targets for ocean acidification (OA) research. Here, we exposed live rhodoliths to near-future OA conditions to investigate responses in their photosynthetic capacity, calcium carbonate production, and associated microbiome using carbon uptake, decalcification assays, and whole genome shotgun sequencing metagenomic analysis, respectively. The results from our live rhodolith assays were compared to similar manipulations on dead rhodolith (calcareous skeleton) biofilms and water column microbial communities, thereby enabling the assessment of host-microbiome interaction under climate-driven environmental perturbations. Results: Under high pCO₂ conditions, live rhodoliths exhibited positive physiological responses, i.e. increased photosynthetic activity, and no calcium carbonate biomass loss over time. Further, whereas the microbiome associated with live rhodoliths remained stable and resembled a healthy holobiont, the microbial community associated with the water column changed after exposure to elevated pCO₂. Conclusions: Our results suggest that a tightly regulated microbial-host interaction, as evidenced by the stability of the rhodolith microbiome recorded here under OA-like conditions, is important for host resilience to environmental stress. This study extends the scarce comprehension of microbes associated with rhodolith beds and their reaction to increased pCO₂, providing a more comprehensive approach to OA studies by assessing the host holobiont.