Warming and nutrient enrichment can trigger seaweed loss by dysregulation of the microbiome structure and predicted function

• Published in: The Science of the total environment 2023-06, Vol.879, p.162919-162919, Article 162919
• Main Authors: Mancuso, Francesco Paolo, Morrissey, Kathryn Lee, De Clerck, Olivier, Airoldi, Laura
• Format: Article
• Language: English
• Subjects: air; algicides; Bacteria; bacteria-host interaction; bacterial communities; Canopy-forming seaweeds; Cystoseira; Ecosystem; environment; Foundation species; Holobiont; Humans; littoral zone; macroalgae; Mediterranean Sea; microbiome; Microbiota; Multiple stressors; Nutrients; Phaeophyceae; photosynthesis; Seaweed - physiology; variance
• ISSN: 0048-9697; 1879-1026
• DOI: 10.1016/j.scitotenv.2023.162919

Warming and nutrient enrichment are key pervasive drivers of ecological shifts in both aquatic and terrestrial ecosystems, impairing the physiology and survival of a wide range of foundation species. But the underlying mechanisms often remain unclear, and experiments have overlooked the potential effects mediated by changes in the microbial communities. We experimentally tested in the field orthogonal stress combinations from simulated air warming and nutrient enrichment on the intertidal foundation seaweed Cystoseira compressa, and its associated bacterial communities. A total of 523 Amplicon Sequence Variance (ASVs) formed the bacterial community on C. compressa, with 222 ASVs assigned to 69 taxa at the genus level. Most bacteria taxa experienced changes in abundance as a result of additive (65 %) and antagonistic (30 %) interactions between the two stressors, with synergies (5 %) occurring less frequently. The analysis of the predicted bacterial functional profile identified 160 metabolic pathways, and showed that these were mostly affected by additive interactions (74 %) between air warming and nutrient enrichment, while antagonisms (20 %) and synergisms (6 %) were less frequent. Overall, the two stressors combined increased functions associated with seaweed disease or degradation of major cell-wall polymers and other algicidal processes, and decreased functions associated with Quorum Quenching and photosynthetic response. We conclude that warming and nutrient enrichment can dysregulate the microbiome of seaweeds, providing a plausible mechanism for their ongoing loss, and encourage more research into the effects of human impacts on crucial but yet largely unstudied host-microbiome relationships in different aquatic and terrestrial species. [Display omitted] •Air warming and nutrient enrichment were simulated on the intertidal Cystoseira holobiont.•Additive and antagonistic interactions between the two stressors were mainly observed.•Stressors increased bacterial processes linked to illness or algicidal processes.•Quorum Quenching and the seaweed's metabolism related functions were also educed.•Warming and nutrient enrichment can dysregulate the seaweed microbiome and photosynthetic efficiency.