Dataset Information

Behavioral and mechanistic characteristics of the predator-prey interaction between the dinoflagellate Dinophysis acuminata and the ciliate Mesodinium rubrum.

ABSTRACT: Predator-prey interactions of planktonic protists are fundamental to plankton dynamics and include prey selection, detection, and capture as well as predator detection and avoidance. Propulsive, morphology-specific behaviors modulate these interactions and therefore bloom dynamics. Here, interactions between the mixotrophic, harmful algal bloom (HAB) dinoflagellate Dinophysis acuminata and its ciliate prey Mesodinium rubrum were investigated through quantitative microvideography using a high-speed microscale imaging system (HSMIS). The dinoflagellate D. acuminata is shown to detect its M. rubrum prey via chemoreception while M. rubrum is alerted to D. acuminata via mechanoreception at much shorter distances (89?±?39??m versus 41?±?32 ?m). On detection, D. acuminata approaches M. rubrum with reduced speed. The ciliate M. rubrum responds through escape jumps that are long enough to detach its chemical trail from its surface, thereby disorienting the predator. To prevail, D. acuminata uses capture filaments and/or releases mucus to slow and eventually immobilize M. rubrum cells for easier capture. Mechanistically, results support the notion that the desmokont flagellar arrangement of D. acuminata lends itself to phagotrophy. In particular, the longitudinal flagellum plays a dominant role in generating thrust for the cell to swim forward, while at other times, it beats to supply a tethering or anchoring force to aid the generation of a posteriorly-directed, cone-shaped scanning current by the transverse flagellum. The latter is strategically positioned to generate flow for enhanced chemoreception and hydrodynamic camouflage, such that D. acuminata can detect and stealthily approach resting M. rubrum cells in the water column.

SUBMITTER: Jiang H

PROVIDER: S-EPMC6089243 | biostudies-literature | 2018 Jul

REPOSITORIES: biostudies-literature

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Behavioral and mechanistic characteristics of the predator-prey interaction between the dinoflagellate Dinophysis acuminata and the ciliate Mesodinium rubrum.

Jiang Houshuo H Kulis David M DM Brosnahan Michael L ML Anderson Donald M DM

Harmful algae 20180618

Predator-prey interactions of planktonic protists are fundamental to plankton dynamics and include prey selection, detection, and capture as well as predator detection and avoidance. Propulsive, morphology-specific behaviors modulate these interactions and therefore bloom dynamics. Here, interactions between the mixotrophic, harmful algal bloom (HAB) dinoflagellate Dinophysis acuminata and its ciliate prey Mesodinium rubrum were investigated through quantitative microvideography using a high-spe ...[more]

PMID: 30005801

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Project description:The development of Dinophysis populations, producers of diarrhetic shellfish toxins, has been attributed to both abiotic (e.g., water column stratification) and biotic (prey availability) factors. An important process to consider is mixotrophy of the Dinophysis species, which is an intensive feeding of the Mesodinium species for nutrients and a benefit from kleptochloroplasts. During the feeding process, the nutritional status in the environment changes due to the preference of Mesodinium and/or Dinophysis for different nutrients, prey cell debris generated by sloppy feeding, and their degradation by micro-organisms changes. However, there is little knowledge about the role of the bacterial community during the co-occurrence of Mesodinium and Dinophysis and how they directly or indirectly interact with the mixotrophs. In this study, laboratory experiments were performed to characterize the environmental changes including those of the prey present, the bacterial communities, and the ambient dissolved nutrients during the co-occurrence of Mesodinium rubrum and Dinophysis acuminata. The results showed that, during the incubation of the ciliate prey Mesodinium with its predator Dinophysis, available dissolved nitrogen significantly shifted from nitrate to ammonium especially when the population of M. rubrum decayed. Growth phases of Dinophysis and Mesodinium greatly affected the structure and composition of the bacterial community. These changes could be mainly explained by both the changes of the nutrient status and the activity of Dinophysis cells. Dinophysis feeding activity also accelerated the decline of M. rubrum and contamination of cultures with okadaic acid, dinophysistoxin-1, and pectenotoxin-2, but their influence on the prokaryotic communities was limited to the rare taxa (<0.1%) fraction. This suggests that the interaction between D. acuminata and bacteria is species-specific and takes place intracellularly or in the phycosphere. Moreover, a majority of the dominant bacterial taxa in our cultures may also exhibit a metabolic flexibility and, thus, be unaffected taxonomically by changes within the Mesodinium-Dinophysis culture system.

Project description:During a series of blooms of Noctiluca scintillans and Mesodinium rubrum, we applied high-throughput sequencing of the 16S rRNA gene to investigate the population dynamics of free-living (FL) and particle-attached (PA) bacteria in an attempt to evaluate the influence of protozoan bloom-induced disturbances on the structuring of these two communities. Our findings revealed that the FL and PA bacterial community compositions (BCCs) displayed distinct profiles during sequential blooms, and the PA flora responded more dynamically to these pulse perturbations. The dominant bacterial groups (e.g., Flavobacteriaceae, Rhodobacteraceae, Vibrionaceae, and SAR11 subclade I) in these two communities displayed different levels of connectivity with the bloom-causative species and environmental factors. In addition, more FL bacterial groups were associated with M. rubrum, while more PA bacterial groups were related to N. scintillans. Potential endocytic bacteria of N. scintillans, particularly Vibrionaceae and Rickettsiaceae, opportunistically thrived at the peak of the bloom, suggesting that they could be important players influencing the dynamics and biogeochemical cycling of the blooms. Overall, disparities in the substrate preferences and thermal niches of various bacterial taxa as well as the short duration of the blooms (1 to 3 days) contributed to the diverse responses of the FL and PA bacterial communities to these protozoan blooms. Our research provides insight into the responses of FL and PA bacterial communities to blooms caused by protozoa like N. scintillans and M. rubrum and highlights the ecological significance of certain keystone bacterial groups during this kind of cosmopolitan protozoan bloom. IMPORTANCE Shifts in the bacterioplankton community composition during phytoplankton blooms have been studied extensively; however, investigations on protozoan blooms are rare. This study first evaluated the impact of perturbations caused by sequential protozoan blooms of the heterotrophic dinoflagellate Noctiluca scintillans and the mixotrophic ciliate Mesodinium rubrum on the structuring of these two bacterial communities. Our findings shed light on the responses of these two bacterial communities to such cosmopolitan protozoan blooms and highlight the possible ecological significance of certain keystone bacterial groups during these blooms. This research prepares the way for more focused studies that will help in understanding the roles that bacteria play during protozoan blooms and their impact on environmental health.

Dataset Information

Behavioral and mechanistic characteristics of the predator-prey interaction between the dinoflagellate Dinophysis acuminata and the ciliate Mesodinium rubrum.

Publications

Behavioral and mechanistic characteristics of the predator-prey interaction between the dinoflagellate Dinophysis acuminata and the ciliate Mesodinium rubrum.

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