Cross-domain microbiome legacy of a natural Phaeocystis globosa bloom in eutrophic coastal waters: a framework for monitoring bloom onset, collapse, and post-bloom recovery

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Abstract
When a harmful algal bloom collapses, does the coastal water quality recover? We addressed this question using the natural bloom of the haptophyte Phaeocystis globosa in coastal waters around Xiamen Island, China. Bacterial and microeukaryotic communities in the water samples ( n = 105) monthly collected from five sites from September 2023 to March 2024 were analyzed using 16S and 18S rRNA amplicon sequencing, genotype-specific qPCR, iCAMP-based assembly inference, partial least squares path modeling, bloom stage-specific co-occurrence networks, and amplicon-based functional prediction. Bloom development drove coordinated physicochemical change. Both bacterial and microeukaryotic communities were displaced from their pre-bloom state but did not return to the original state within the 7-month series. However, their patterns of succession were different. Bacterial communities underwent coherent system-wide succession. They diverged spatially during the bloom. Their assembly shifted toward stochasticity, with the deterministic contribution falling from 46.3% pre-bloom to 27.8% during the bloom and recovering only to 30.3% post-bloom. Their co-occurrence network was most complex during the bloom period. In contrast, microeukaryotic communities retained stronger site-specific structure throughout succession, and their network connectivity peaked after the bloom collapsed. Water quality variables explained 45.9% of bacterial but only 13.1% of microeukaryotic community variation. Predicted functional profiles also showed stage-associated changes. The same bloom thus pushed bacterial and microeukaryotic communities toward different post-disturbance configurations on different timescales. We therefore propose a cross-domain monitoring framework that integrates stage-specific taxa, a community state index, and network complexity. This framework can diagnose bloom onset, collapse, and genuine post-bloom recovery in eutrophic coastal waters. IMPORTANCE: Harmful algal blooms disturb coastal waters well beyond the period when the causative alga is abundant. This study shows that the effects of a Phaeocystis globosa bloom on the coastal microbiome lasted after the bloom itself ended and that bacteria and microeukaryotes recovered along different paths and on different timescales. Algal counts or nutrient concentrations alone therefore cannot adequately capture the recovery of coastal water quality. We suggest an alternative monitoring framework that combines stage-specific indicator taxa, a community state index, and network topology, so that coastal water quality can be assessed more reliably.
Funding Information
  • National Natural Science Foundation of China (42577480)

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