Comparative metatranscriptomic profiling and microRNA sequencing to reveal active metabolic pathways associated with a dinoflagellate bloom

Harmful algal blooms (HABs) have increased as a result of global climate and environmental changes, exerting increasing impacts on the aquatic ecosystem, coastal economy, and human health. Despite great research efforts, our understanding on the drivers of HABs is still limited in part because HAB species' physiology is difficult to probe in situ. Here, we used molecular ecological analyses to characterize a dinoflagellate bloom at Xiamen Harbor, China. Prorocentrum donghaiense was identified as the culprit, which nutrient bioassays showed were not nutrient-limited. Metatranscriptome profiling revealed that P. donghaiense highly expressed genes related to N- and P-nutrient uptake, phagotrophy, energy metabolism (photosynthesis, oxidative phophorylation, and rhodopsin) and carbohydrate metabolism (glycolysis/gluconeogenesis, TCA cycle and pentose phosphate) during the bloom. Many genes in P. donghaiense were up-regulated at night, including phagotrophy and environmental communication genes, and showed active expression in mitosis. Eight microbial defense genes were up-regulated in the bloom compared with previously analyzed laboratory cultures. Furthermore, 76 P. donghaiense microRNA were identified from the bloom, and their target genes exhibited marked differences in amino acid metabolism between the bloom and cultures and the potential of up-regulated antibiotic and cell communication capabilities. These findings, consistent with and complementary to recent reports, reveal major metabolic processes in P. donghaiense potentially important for bloom formation and provide a gene repertoire for developing bloom markers in future research.