Cell density-dependent swimming patterns of Alexandrium fundyense early stationary phase cells

Abstract

Different life-history stages of Alexandrium fundyense have different swimming behaviors and show different responses to water movement. Early stationary phase cells assemble in bioconvection patterns along the water surface and as stripes in the water, while cells in exponential growth do not. We studied the swimming behavior of early stationary phase A. fundyense cells, both on the individual level and on the population level. Cells assembled in spots in shallow Petri dishes, and were studied using an inverted microscope. We analyzed 53 videos of cells at different distances from the center of accumulated spots of cells with the program CellTrak for swimming behavior of individual cells. The closer the cells were to the center of spots, the faster they swam (> 600 µm s −1 in the center of spots compared to ca. 300 µm s −1 outside) and the more often they changed direction (>1400 degrees s −1 in the center compared to < 400 degrees s −1 outside). On a population level, the behavior of spots of assembled cells was studied using time-lapse photo graphy. The spots entrained more and more cells as they grew and fused with each other; the closer the spots came to each other, the faster they moved until they fused. We suggest that chemical attraction between gametes causes the observed behavior. KEY WORDS: Alexandrium fundyense · Swimming pattern · Stationary phase · Gamete · Cell density Resale or republication not permitted without written consent of the publisherAquat Microb Ecol 68: [251][252][253][254][255][256][257][258] 2013 amounts that they cause an unstable density stratification that triggers instability in the form of descending plumes of cells (Kessler 1985, 1986, Pedley & Kessler 1992, Bees & Hill 1997, Hopkins & Fauci 2002, Nguyen-Quang et al. 2009). In such a plume, the fluid velocity is higher than the swimming velocity of individual cells -the collective behavior of cells has changed the density distribution in such a way that patterns are formed at a scale greater than individual cells. The underlying cause of the assemblage of cells is a tactic behavior of individual cells, being attracted to light, nutrients, oxygen, etc., or swimming upwards to avoid sinking (gravit axis). When geometry of cells, density distribution within cells, placement of flagella, etc. affects the swimming direction, the term used is gyrotaxis. Gyrotaxis is directional swimming due to a combination of upward swimming and rotational drag due to shear (e.g. Kessler 1985, Durham et al. 2009). Bioconvection patterns concentrate microorganisms into dense regions separated by regions with few organisms, which can facilitate mating (Wager 1911, Kessler 1986, Pedley & Kessler 1992.In many dinoflagellate species, including all that produce resting cysts, gametes are formed at the end of the growth season. Attraction between gametes is necessary, otherwise sexual fusion and production of resting cysts for survival during the winter would be impossible. The 'season cue' for gamete formation may be composed of many diff...

Differences in pigmentation between life cycle stages in Scrippsiella lachrymosa (dinophyceae)

“…Microscopy confirmed straight (i.e., nonerratic) swimming patterns and equally sized, drop‐shaped cells with a short but pronounced apical horn (as described in Lewis , for swimming pattern interpretation, see Smith and Persson , Persson et al. and Persson and Smith ). Cells were thus harvested in mid‐exponential growth phase.…”

“…When dinoflagellate gametes are formed, they are attracted to each other, and their swimming behavior causes bio‐convection patterns (Persson and Smith ). Gamete swimming patterns and the resulting dense cell accumulations are concentrated further and transported by water circulation patterns (e.g., fronts, currents; Persson and Smith and references therein, Wyatt and Zingone ) which might bring gametes and zygotes closer to the surface than they would be found as vegetative cells. These differences in movements and transportation might elicit a need for more photoprotection in zygotes, especially for a species that thrives at lower light depths as vegetative cells.…”

“…Gametes and vegetative cells are very similar in size but have different swimming behavior (as described in Smith and Persson , Persson et al. and Persson and Smith ) and small morphological differences (gametes are rounder and paler). The biovolume of cells was not determined in this experiment since focus was on cellular pigment content.…”

“…, Smith and Persson ) in 2.8‐L Fernbach flasks (six replicates – three for gametes, three for pellicle cysts of gametes). These cultures were monitored by light microscopy for morphology and swimming behavior of cells (Persson and Smith , Persson et al. ).…”

Growth and diel vertical migration patterns of the toxic dinoflagellate Protoceratium reticulatum in a water column with salinity stratification: the role of bioconvection and light

“…During withdrawal, the cells moved horizontally inwards and became more and more concentrated into 1 main aggregate/patch. For A. fundyense (Dinophyceae), assembly of cells into horizontal bioconvection spots/stripes was restricted to the early stationary phase of the life cycle, and has been explained by life-history-related swimming patterns and/or responses related to water movements (Persson & Smith 2013). Such patchy and dense aggregations of harmful dinoflagellate cells represent high accumulations of biomass which can facilitate transfer of algal toxins to higher trophic levels (Manfrin et al 2012).…”