Ecological roles of dinoflagellates as symbionts, mixotrophic predators and prey for zooplankton in Korean coastal ecosystems and an effective cultivation of microalgae for heterotrophic dinoflagellates.

Abstract

Marine dinoflagellates are ubiquitous and observed at diverse habitats such as water column, macroalgae, and marine organisms. They are one of the major components of marine ecosystem and play diverse roles in even Korean. Despite the huge economic losses due to dinoflagellates red tides, multiple approach for the diveres rolse of dinoflagellates are rare. To understand ecological roles of dinoflagellates in Korean coastal ecosystems and their potential impact on marine environments and humans, multiple approach studies based on extensive investigations are needed. Thus, I investigated the three kinds of ecological roles of the dinoflagellates in Korean coastal waters such as symbiotic partners of corals, mixotrophic predators of red tides species, and prey for zooplankton predators. In addition, as an application, I developed the newly designed effective photobioreactor to cultivate algal preys in high concentration for the massive production of heterotrophic dinoflagellates. To investigate ecological roles of the symbiotic dinoflagellates Symbiodinium spp. in Korean waters, I took samples from the coral Alveopora japonica in the coastal waters of Jeju Isalnd on monthly basis from 2012 to 2013 and analyzed the composition of Symbiodinium ribotypes using Quantitative PCR. Symbiodinium clade F took over > 99% of total Symbiodinium abundance inside the A. japonica all the sample intervals, while Symbiodinium clade B, C, and E were detected. The temporal variation in the abundance and prevalence of the background Symbiodinium were not affected by temperature, salinity, major nutrients, and chlorophyll-a concentration. Therefore, only main symbiotic dinoflagellate species that occur in high concentration are important for the coral-dinoflagellate mutualisms. To investigate whether the phototrophic dinoflagellate Polykrikos hartmannii is able to feed on any other algal prey or not, its feeding occurrence, identification of prey species, and feeding mechanism were explored. Furthermore, the growth and ingestion rates of P. hartmannii on the mixotrophic red tide dinoflagellate Cochlodinium polykrikoides that is the major cause species of red tides and economic losses in Korea were also measured. For the first time, P. hartmannii is reported to be a mixotrophic dinoflagellate in this study. When diverse algal species were provided as potential prey, P. hartmannii fed only on chain-forming toxic mixotrophic dinoflagellates C. polykrikoides and Gymnodinium catenatum. P. hartmannii ingested prey cells by engulfment after anchoring a prey cell using a nematocyst–taeniocyst complex. With increasing mean prey concentration, the ingestion rate of P. hartmannii on C. polykrikoides increased, to reach saturation at a prey concentration over 945 ng C ml-1 (1350 cells ml-1). The maximum ingestion rate of P. hartmannii on C. polykrikoides was 1.9 ng C predator-1 d-1 (2.7 cells predator-1 d-1). The calculated grazing coefficients for P. hartmannii on co-occurring C. polykrikoides were up to 0.324 d-1 (equivalent to 28% of the population of C. polykrikoides was removed by P. hartmannii populations in a day). The results of the present study showed that P. hartmannii might exert considerable and negative influence on the red tide population of C. polykrikoides. To explore the grazing impacts of metazooplankton on red tide dinoflagellates in Korean waters, the spatial and temporal variations in the abundance of metazooplankton were investigated before, during, and after red tides dominated by phototrophic dinoflagellates in South Sea of Korea from May to November 2014. Grazing impacts by dominant metazooplankton taxa on populations of dominant red tide dinoflagellates were also estimated. Simultaneously, some of the important environmental parameters such as water temperature, salinity, chlorophyll-a were analyzed. The calanoid copepods did not exhibit grazing impact high enough to directly control the populations of the red tide dinoflagellates Prorocentrum donghaiense and Cochlodinium polykrikoides (up to 0.029 d-1 and 0.018 d 1, resprectively) in South Sea of Korea. However, their predation impacts on the population of the heterotrophic dinoflagellate Gyrodinium spp. (up to 0.047 d 1), the important predator of P. donghaiense, were greater than the grazing impact of calanoids on P. donghaiense during the blooming stage of P. donghaiense red tides. In addition, the grazing impact of calanoids on diatom species like Skeletonema costatum and Chaetoceros spp., the inhibitors of C. polykrikoides, were much greater (up to 0.05 d 1 and 0.032d 1, respectively) than their predation impacts on C. polykrikoides at the very early stage of C. polykrikoides red tides. Therefore, the calanoid copepods may support the rapid population growth of the red tide dinoflagellate species by suppressing the population growths of the heterotrophic dinoflagellate predator and the diatom inhibitors. Microalgae such as dinoflagellates and green algae have been envisioned to be valuable raw materials for biofuel. Their potential oil productivity is estimated to be at least four times greater than that by the land plants. Furthermore, some heterotrophic dinoflagellate species are known to produce large amount of unsaturated fatty acids (PUFA). I developed an effective photo bioreactor (PBR) for cultivating algal prey species for the economically reasonable production heterotrophic dinoflagellates. The newly designed PBRs include airlift bubble columns made of polycarbonate (PC) material. A set of PBR consisting of five parts can be assemble together that can be increased the total cultivation volume by assemble more parts. Furthermore, the disassembled PBR units are autoclavable at 121°C. The maximum cell concentrations and growth in the same PBRs may mainly depends on CO2 concentration and pH. The maximum cell concentration and maximum growth rate of D. tertiolecta were 7.2 x 107 cells ml-1 and 1.7 d-1 in the PBR when 5% CO2 was continuously supplied. This maximum cell concentration is far greater than that obtained by any other devise for cultivating D. tertiolecta under indoor operation conditions. Therefore, the newly developed PBR should be very useful for the massive production of D. tertiolecta biomass, that can be fed into another cultivation system to obtain high biomass of biotechnologically useful heterotrophic dinoflagellate. The results of this study may lead us to better understand ecological roles of dinoflagellates as symbiotic partners of corals, mixotrophic predators, prey for metazooplankton in marine ecosystems and the associated food web interactions.