Laboratory Culture-Based Characterization of the Resting Stage Cells of the Brown-Tide-Causing Pelagophyte, Aureococcus anophagefferens

Abstract

Life history (life cycle) plays a vital role in the ecology of some microalgae; however, the well-known brown-tide-causing pelagophyte Aureococcus anophagefferens has been barely investigated in this regard. Recently, based mainly on detections in marine sediments from China, we proved that this organism has a resting stage. We, therefore, conducted a follow-up study to characterize the resting stage cells (RSCs) of A. anophagefferens using the culture CCMP1984. The RSCs were spherical, larger than the vegetative cells, and smooth in cell surface and contained more aggregated plastid but more vacuolar space than vegetative cells. RSCs contained a conspicuous lipid-enriched red droplet. We found a 9.9-fold decrease in adenosine triphosphate (ATP) content from vegetative cells to RSCs, indicative of a "resting" or dormant physiological state. The RSCs stored for 3 months (at 4 °C in darkness) readily reverted back to vegetative growth within 20 days after being transferred to the conditions for routine culture maintenance. Our results indicate that the RSCs of A. anophagefferens are a dormant state that differs from vegetative cells morphologically and physiologically, and that RSCs likely enable the species to survive unfavorable conditions, seed annual blooms, and facilitate its cosmopolitan distribution that we recently documented.

The diel disconnect between cell growth and division inAureococcusis interrupted by giant virus infection

“…This would create a separation between uninfected cells and new viruses released into the water column (an innate defense against community infection). Moreover, given the inability of K. quantuckense to lyse A. anophagefferens in the dark, the expediated sinking could foster an opportunity for survival against infection, given cellular mechanisms a chance to purge the virus or enter a cyst-like state and prevent viral propagation (Ma et al, 2020). It is yet unclear if entering this resting stage has such an effect or if the lytic cycle continues once the cell is metabolically active again.…”

Kratosvirus quantuckense: the history and novelty of an algal bloom disrupting virus and a model for giant virus research

“…Due to the later appearance of bloom events in Saldanha Bay and the Bohai Sea it was thought that A. anophagefferens may have traveled by ballast water contained in ships ( Doblin et al, 2004 ). This was made more plausible by the discovery of a dormant (resting) cell stage ( Ma et al, 2020 ). However, this hypothesis has been complicated by sediment core analyses that provide evidence of a historical presence of A. anophagefferens in China’s Bohai Sea of over 1,500 years, and subsequently a confirmation of global distribution similar to other pelagophytes ( Tang et al, 2019 ; Choi et al, 2020 ).…”

“…Described as a picoplankton with spherical cells of 1.5–2 μm in size with a “golden” color ( Sieburth et al, 1988 ), subsequent observations place these cells at 2–3 μm in a vegetative state ( Bricelj and Lonsdale, 1997 ; Ma et al, 2020 ). A. anophagefferens cells possess a single nucleus, chloroplast, and mitochondria, as well as an exopolysaccharide layer (glycocalyx), of which little of the molecular content is understood ( Sieburth et al, 1988 ).…”

Taxonomy and Ecology of Marine Algae

“…Ma et al [10] proved that the well-known brown-tide-causing pelagophyte Aureococcus anophagefferens has a resting stage. They conducted a follow-up study to characterize the resting stage cells (RSCs) of A. anophagefferens using the culture CCMP1984.…”