Metagenomic insights into co-proliferation of Vibrio spp. and dinoflagellates Prorocentrum during a spring algal bloom in the coastal East China Sea

Coastal harmful algal blooms (HABs), commonly termed 'red tides', have severe undesirable consequences to the marine ecosystems and local fishery and tourism industries. Increase in nitrogen and/or phosphorus loading is often regarded as the major culprits of increasing frequency and intensity of the coastal HAB; however, fundamental understanding is lacking as to the causes and mechanism of bloom formation despite decades of intensive investigation. In this study, we interrogated the prokaryotic microbiomes of surface water samples collected at two neighboring segments of East China Sea that contrast greatly in terms of the intensity and frequency of Prorocentrum-dominated HAB. Mantel tests identified significant correlations between the structural and functional composition of the microbiomes and the physicochemical state and the algal biomass density of the surface seawater, implying the possibility that prokaryotic microbiota may play key roles in the coastal HAB. A conspicuous feature of the microbiomes at the sites characterized with high trophic state index and eukaryotic algal cell counts was disproportionate proliferation of Vibrio spp., and their complete domination of the functional genes attributable to the dissimilatory nitrate reduction to ammonia (DNRA) pathway substantially enriched at these sites. The genes attributed to phosphorus uptake function were significantly enriched at these sites, presumably due to the Pi-deficiency induced by algal growth; however, the profiles of the phosphorus mineralization genes lacked consistency, barring any conclusive evidence with regard to contribution of prokaryotic microbiota to phosphorus bioavailability. The results of the co-occurrence network analysis performed with the core prokaryotic microbiome supported that the observed proliferation of Vibrio and HAB may be causally associated. The findings of this study suggest a previously unidentified association between Vibrio proliferation and the Prorocentrum-dominated HAB in the subtropical East China Sea, and opens a discussion regarding a theoretically unlikely, but still possible, involvement of Vibrio-mediated DNRA in Vibrio-Prorocentrum symbiosis. Further experimental substantiation of this supposed symbiotic mechanism may prove crucial in understanding the dynamics of explosive local algal growth in the region during spring algal blooms.

Automated summary

The study reveals a potential key role of prokaryotic microbiota in coastal harmful algal blooms based on significant correlations between the microbiomes and physicochemical properties of seawater. The findings suggest a previously unidentified association between Vibrio proliferation and the Prorocentrum-dominated HAB, indicating a possible involvement of Vibrio-mediated DNRA in symbiosis with Prorocentrum.