Stimulable and Spontaneous Bioluminescence in the Marine Dinoflagellates, <i>Pyrodinium bahamense, Gonyaulax polyedra</i>, and <i>Pyrocystis lunula </i>

Biggley, W. H.; Swift, Elijah; Buchanan, Rasmus; Seliger, H. H.

doi:10.1085/jgp.54.1.96

Cited by 124 publications

(85 citation statements)

References 9 publications

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“…Cell abundance was determined by counting samples under a dissecting microscope. Two hours prior to the end of the day phase, when cells are mechanically unexcitable (Biggley et al 1969), aliquots from cultures exhibiting exponential growth were added to 0.45-m filtered seawater in the head tank so that the calculated cell concentration was 15 cells ml Ϫ1 or as otherwise stated. For most experiments, the contents of the head tank were slowly stirred at 0.5 rpm with a 20-cm-wide paddle to create a homogenous distribution of cells; stirring was terminated prior to the beginning of testing.…”

Section: Methodsmentioning

confidence: 99%

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Luminescent response of the red tide dinoflagellate Lingulodinium polyedrum to laminar and turbulent flow

Latz

Rohr

1999

Limnology & Oceanography

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While it is universally accepted that plankton continually experience a dynamic fluid environment, their sensitivity to the features of the surrounding flow field at the relevant length and time scales of the organism is poorly characterized. The present study uses bioluminescence as a tool to understand how the red tide dinoflagellate Lingulodinium polyedrum (ϭ Gonyaulax polyedra) responds to well-characterized hydrodynamic forces present in fully developed laminar and turbulent pipe flow. The response of L. polyedrum to hydrodynamic stimulation was best characterized by wall shear stress; at similar values of wall shear stress, the response was similar for laminar and turbulent flows.The response threshold occurred in laminar flow at a wall shear stress of approximately 0.3 N m Ϫ2. At these low flow rates, video analysis of the velocity of flash trajectories revealed that responding cells were positioned only near the pipe wall, where local shear stress levels were equal to or greater than threshold. For cell concentrations ranging over four orders of magnitude, threshold values of wall shear stress were restricted to a narrow range, consistent with an antipredation function for dinoflagellate bioluminescence. For laminar flows with above-threshold wall shear stress values Յ 1 N m Ϫ2 , mean bioluminescence increased with wall shear stress according to a power (log-log) relationship, with the slope of the power function dependent on cell concentration. The increase in bioluminescence within this range was due primarily to an increasing population response rate and, to a lesser extent, an increase in maximum flash intensity per cell and the increased flux of organisms with higher flow rates. For wall shear stress levels Ͼ 1 N m Ϫ2 , the maximum intensity per cell remained approximately constant with increasing wall shear stress, even as the flow transitioned from laminar to turbulent, and the smallest turbulent length scales became less than the average cell size.All plankton experience a dynamic fluid environment due to the effects of wind, waves, tides, and currents. For phytoplankton, turbulence regulates the vertical transport of cells (Lewis et al. 1984;Cowles and Desiderio 1993), which affects primary production through changes in the average level of incident illumination (reviewed by Kiørboe 1993), the sedimentation rate of cells from the mixed layer (Ruiz et al. 1996), the coagulation of cells caused by shear-induced collisions between suspended phytoplankton (Jackson 1990), and the encounter rate of phytoplankton to grazers and microbes (Bowen et al. 1993). It also relaxes diffusion limitation of nutrient uptake, which can lead to enhanced growth (Pasciak and Gavis 1975; reviewed by Kiørboe 1993 andKarp-Boss et al. 1996). Turbulence can negatively affect phytoplankton growth and cell division (Thomas andGibson 1990a, 1995;Berdalet 1992; reviewed by Estrada and Berdalet 1997) and alter cell motility (Thomas and Gibson 1990a).The present study applies bioluminescence as a tool to characterize how...

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Section: Methodsmentioning

confidence: 99%

“…At the beginning of the dark phase, the apparatus was covered with opaque sheeting. Testing commenced 2.5 h into the dark phase, when the bioluminescence of L. polyedrum is maximal (Biggley et al 1969).…”

Section: Methodsmentioning

confidence: 99%

Luminescent response of the red tide dinoflagellate Lingulodinium polyedrum to laminar and turbulent flow

Latz

Rohr

1999

Limnology & Oceanography

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“…Zooplankton used for the swimmingspeed measurements were collected in the northern Sargasso Sea during BIOWATT II The bioluminescence potentials of the organisms found in our Sargasso Sea samples were measured with the techniques of Biggley et al (1969). Measurements used to es-timate bioluminescence potential for each species or taxonomic category were collected on numerous cruises in the Sargasso Sea, Caribbean Sea, and Gulf of Mexico.…”

Section: Methodsmentioning

confidence: 99%

An encounter model to predict natural planktonic bioluminescence

Buskey¹,

Swift

1990

Limnology & Oceanography

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Natural bioluminescence results from the emissions of bioluminescent organisms in the absence of man-made disturbance. Most epipelagic and mesopelagic bioluminescence is caused by planktonic organisms. Limited attempts to measure natural bioluminescence in situ with surface deployed and moored instruments have recorded much higher levels of natural bioluminescence than have been observed from submersibles. We present a model predicting the frequency of interactions among planktonic organisms leading to natural bioluminescent emissions. The results suggest that natural bioluminescent flashes caused by interactions between zooplankters may be rare events in the Sargasso Sea, with our model predicting a maximum of nearly 600 flashes h-l m-3 at night in surface waters of the northern Sargasso Sea where there was an unusually high concentration of euphausiids and small bioluminescent dinoflagellates, but < 1 flash h-' m-3 in the southern Sargasso Sea. In both locations most of the natural bioluminescence was predicted to be caused by euphausiids and copepods of the genus Pleuromamma and natural bioluminescence generally decreased with depth. The more intense displays of natural bioluminescence are probably the result of the bioluminescence of numerous smaller dinoflagellates common in coastal waters and may also be the result of disturbances caused by interactions of larger organisms with bioluminescent plankters.

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“…Cell concentrations were determined from cell counts of defined volumes (usually 10 μl) in a multi-well slide under the microscope. Toward the end of the light phase, when dinoflagellate bioluminescence is not mechanically stimulable (Biggley et al, 1969), a sample from the desired culture at a concentration of 2000-15,000 cells ml -1 was loaded into a 60 ml plastic syringe that was covered with opaque material at the beginning of the dark phase.…”

Section: Test Organismsmentioning

confidence: 99%

Bioluminescent response of individual dinoflagellate cells to hydrodynamic stress measured with millisecond resolution in a microfluidic device

Latz

Bovard

VanDelinder

et al. 2008

Journal of Experimental Biology

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SUMMARYDinoflagellate bioluminescence serves as a model system for examining mechanosensing by suspended motile unicellular organisms. The response latency, i.e. the delay time between the mechanical stimulus and luminescent response, provides information about the mechanotransduction and signaling process, and must be accurately known for dinoflagellate bioluminescence to be used as a flow visualization tool. This study used a novel microfluidic device to measure the response latency of a large number of individual dinoflagellates with a resolution of a few milliseconds. Suspended cells of several dinoflagellate species approximately 35 μm in diameter were directed through a 200 μm deep channel to a barrier with a 15 μm clearance impassable to the cells. Bioluminescence was stimulated when cells encountered the barrier and experienced an abrupt increase in hydrodynamic drag, and was imaged using high numerical aperture optics and a high-speed low-light video system. The average response latency for Lingulodinium polyedrum strain HJ was 15 ms (N>300 cells) at the three highest flow rates tested, with a minimum latency of 12 ms. Cells produced multiple flashes with an interval as short as 5 ms between individual flashes, suggesting that repeat stimulation involved a subset of the entire intracellular signaling pathway. The mean response latency for the dinoflagellates Pyrodinium bahamense, Alexandrium monilatum and older and newer isolates of L. polyedrum ranged from 15 to 22 ms, similar to the latencies previously determined for larger dinoflagellates with different morphologies, possibly reflecting optimization of dinoflagellate bioluminescence as a rapid anti-predation behavior. Supplementary material available online at

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Stimulable and Spontaneous Bioluminescence in the Marine Dinoflagellates, Pyrodinium bahamense, Gonyaulax polyedra, and Pyrocystis lunula

Cited by 124 publications

References 9 publications

Luminescent response of the red tide dinoflagellate Lingulodinium polyedrum to laminar and turbulent flow

Luminescent response of the red tide dinoflagellate Lingulodinium polyedrum to laminar and turbulent flow

An encounter model to predict natural planktonic bioluminescence

Bioluminescent response of individual dinoflagellate cells to hydrodynamic stress measured with millisecond resolution in a microfluidic device

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