Phycosphere microbiome remodeling and Brevundimonas partnership establishment enhance microalgal nonylphenol tolerance.

INTRODUCTION

Microalgae are vital primary producers in aquatic ecosystems yet increasingly threatened by nonylphenol (NP), a common endocrine disruptor. Current ecotoxicological assessments, however, largely rely on single-species models, overlooking the role of the phycosphere microbiome in host stress adaptation.

METHODS

Here, using the NP-tolerant microalgae Dictyosphaerium sp. as a model holobiont, we integrated multi-omics, axenic algae-bacteria co-culture, physiological, and metabolic analyses to unravel how associated microbes contribute to microalgal NP fitness.

RESULTS

Under environmentally relevant NP concentrations (10-900 µg/L), the holobiont sustained 20.3-91.3% higher biomass than axenic cultures. NP exposure reshaped the phycosphere community, enriching beneficial taxa. Among 16 bacterial isolates, Brevundimonas sp. D-1 exerted the strongest protective effect, boosting algal biomass by 39.9%. Mechanistically, D-1 significantly accelerated NP removal (P < 0.05), achieving a 28.8% increase within 4 days. Oxidative stress in NP-exposed algae was also markedly achieved, as reflected by 29.3% and 46.8% reductions in reactive oxygen species and malondialdehyde levels, respectively, alongside ultrastructural preservation and > 1.3-fold increases in photosynthetic pigment contents. Moreover, D-1 modulated extracellular polymeric substances, restraining their overproduction while enriching tyrosine- and tryptophan-like components to reinforce the interfacial barrier. Transcriptomic profiling further revealed downregulation of stress-defense genes (e.g., DNA repair and photoprotection) and restoration of growth-related pathways, including photosynthesis and energy metabolism.

CONCLUSION

Our findings establish a community-to-strain paradigm for phycosphere microbiome-mediated tolerance of microalgae to NP, deepen our understanding of inter-species cooperation, and provide a basis for designing tailored algae-bacteria consortia for bioremediation.