Shear-Stress Dependence of Dinoflagellate Bioluminescence

Maldonado, Elisa M.; Latz, Michael I.

doi:10.2307/25066606

Cited by 58 publications

(50 citation statements)

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“…The bioluminescence of dinoflagellates is stimulated by the velocity gradient rather than absolute flow velocity Maldonado and Latz, 2007) and can thus serve as a reporter of local velocity gradients and hydrodynamic stresses, making it a unique tool for both field Rohr et al, 2002) and laboratory (Chen et al, 2003;Stokes et al, 2004) flow visualization. Based on laboratory studies using well-characterized flow fields (Latz et al, 1994;Latz and Rohr, 1999;Latz et al, 2004a;Latz et al, 2004b) a statistical model has recently been developed that predicts bioluminescence intensity as a function of shear stress level and cell concentration (Deane and Stokes, 2005).…”

Section: Introductionmentioning

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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Section: Introductionmentioning

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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“…At smaller scales, spermatozoa exhibit rheotaxis, likely resulting from a passive hydrodynamic effect, whereby the combination of a gravitational torque and a shear-induced torque orients the swimming direction preferentially upstream (14)(15)(16). Responses to shear are also observed in copepods and dinoflagellates, which rely on shear detection to attack prey or escape predators (5,(17)(18)(19), orient in flow (20), and retain a preferential depth (21). Evidence of shear-driven motility in prokaryotes is limited to the upstream motion of mycoplasma (22), E. coli (23), and Xylella fastidiosa (24), all of which require the presence of a solid surface.…”

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confidence: 99%

Bacterial rheotaxis

Marcos

Powers

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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The motility of organisms is often directed in response to environmental stimuli. Rheotaxis is the directed movement resulting from fluid velocity gradients, long studied in fish, aquatic invertebrates, and spermatozoa. Using carefully controlled microfluidic flows, we show that rheotaxis also occurs in bacteria. Excellent quantitative agreement between experiments with Bacillus subtilis and a mathematical model reveals that bacterial rheotaxis is a purely physical phenomenon, in contrast to fish rheotaxis but in the same way as sperm rheotaxis. This previously unrecognized bacterial taxis results from a subtle interplay between velocity gradients and the helical shape of flagella, which together generate a torque that alters a bacterium's swimming direction. Because this torque is independent of the presence of a nearby surface, bacterial rheotaxis is not limited to the immediate neighborhood of liquid-solid interfaces, but also takes place in the bulk fluid. We predict that rheotaxis occurs in a wide range of bacterial habitats, from the natural environment to the human body, and can interfere with chemotaxis, suggesting that the fitness benefit conferred by bacterial motility may be sharply reduced in some hydrodynamic conditions. low Reynolds number | directional motion | chirality T he effectiveness and benefit of motility are largely determined by the dependence of movement behavior on environmental stimuli. For example, chemical stimuli may affect the spreading of tumor cells (1) and allow bacteria to increase uptake by swimming toward larger nutrient concentrations (2, 3), whereas hydrodynamic stimuli can stifle phytoplankton migration (4), allow protists to evade predators (5), and change sperm-egg encounter rates for external fertilizers (6). Microorganisms exhibit a broad range of directed movement responses, called "taxes". Whereas some of these responses, such as chemotaxis (7) and thermotaxis (8), are active and require the ability to sense and respond to the stimulus, others, such as magnetotaxis (9) and gyrotaxis (4), are passive and do not imply sensing, instead resulting purely from external forces.Chemotaxis is the best studied among these directional motions: Bacteria measure chemical concentrations and migrate along gradients (Fig. 1A). For instance, chemotaxis guides Escherichia coli to epithelial cells in the human gastrointestinal tract, favoring infection (10); Rhizobium bacteria to legume root hairs in soil, favoring nitrogen fixation (2); and marine bacteria to organic matter, favoring remineralization (3). Equally as pervasive as chemical gradients in microbial habitats are gradients in ambient fluid velocity or "shear" (Fig. 1B). Although nearly every fluid environment experiences velocity gradientsfrom laminar shear in bodily conduits and soil to turbulent shear in streams and oceans-the effect of velocity gradients on bacterial motility has received negligible attention compared with chemical gradients, partly due to the difficulty of studying motility under controlled flow conditi...

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“…Similar to ciliates, mechanoreceptors that enable predator detection have also been described for dinoflagellates (Maldonado & Latz, 2007). Jakobsen et al (2006) reported highly effective escape behaviour for two different dinoflagellates when being attacked by a predator.…”

Section: Transfer Techniquementioning

confidence: 91%

Conserving original in situ diversity in microzooplankton grazing set-ups

Löder¹,

Aberle²,

Klaas

et al. 2010

Mar. Biodivers. Rec.

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Grazing experiments targeting the determination of in situ grazing rates are standard. In two separate experiments the effect of the frequently used siphon filling technique on the abundance of microzooplankton during the set-up of grazing experiments was investigated and compared to results from an alternative filling method. Hereby, water containing natural communities from Helgoland Roads, Germany (54811.3 ′ N 7854.0 ′ E), was transferred into incubation bottles using a funnel system (funnel-transfer technique (FTT)). The impact of pre-screening with a 200 mm net for excluding larger mesozooplankton grazers from the incubations was evaluated. Results show that the ciliate community was strongly affected by siphoning and pre-screening, leading to significant differences in abundance and Margalef diversity. The most affected ciliates were Lohmanniella oviformis and Myrionecta rubra, both important species in the North Sea. Dinoflagellates did not show any significant response to either siphoning or pre-screening with the exception of one athecate species. Such artificial bias in ciliate assemblages is very problematic for biodiversity consideration and grazing investigations. Simply changing the method of filling during the experimental set-up can ensure the measurement of accurate grazing rates of field abundances of microzooplankton. We thus recommend using conservative filling approaches like the FTT in experiments, especially when sensitive species are present, in order to avoid shifts in the overall microzooplankton community. Furthermore, we recommend introducing a control to evaluate the degree of changes in the target community due to the experimental set-up.

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Shear-Stress Dependence of Dinoflagellate Bioluminescence

Cited by 58 publications

References 53 publications

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

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

Bacterial rheotaxis

Conserving original in situ diversity in microzooplankton grazing set-ups

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