Mortality in cultures of the dinoflagellate Amphidinium carterae during culture senescence and darkness

Abstract

The study of cell death in higher plants and animals has revealed the existence of an active ('programmed') process in most types of cell, and similarities in cell death between plants, animals, yeast and bacteria suggest an evolutionarily ancient origin of programmed cell death (PCD). Despite their global importance in primary production, information on algal cell death is limited. Algal cell death could have similarities with metazoan cell death. One morphotype of metazoan PCD, apoptosis, can be induced by light deprivation in the unicellular chlorophyte Dunaliella tertiolecta. The situation in other algal taxa is less clear. We used a model dinoflagellate (Amphidinium carterae) to test whether mortality during darkness and culture senescence showed apoptotic characteristics. Using transmission electron microscopy, fluorescent biomarkers, chlorophyll fluorescence and particulate carbon analysis we analysed the process of cell mortality and found that light deprivation caused mass mortality. By contrast, fewer dead cells (5-20% of the population) were found in late-phase cultures, while a similar degenerate cell morphology (shrunken, chlorotic) was observed. On morphological grounds, our observations suggest that the apoptotic cell death described in D. tertiolecta does not occur in A. carterae. Greater similarity was found with paraptosis, a recently proposed alternative morphotype of PCD. A paraptotic conclusion is supported by inconclusive DNA fragmentation results. We emphasize the care that must be taken in transferring fundamental paradigms between phylogenetically diverse cell types and we argue for a greater consistency in the burden of proof needed to assign causality to cell death processes.

What is the role and nature of programmed cell death in phytoplankton ecology?

“…is also thought to undergo PCD (displaying an apoptotic morphology) due to heat stress (Dunn et al, 2002). However, in the dinoflagellate Amphidinium carterae, cell death in darkness, and during culture senescence, results in similar morphological changes without definitive apoptotic characteristics (Franklin & Berges, 2004). Mortality in A. carterae shows greatest morphological similarity with paraptosis (see Table 1) -an alternative outcome of PCD (Sperandio et al, 2000), which was originally observed in mammalian nerve tissue.…”

“…One possible functional role of such a pathway in unicellular algae (and yeast) is to recycle the organic remains of cells for use by conspecifics (Gomez et al, 1974;Frohlich & Madeo, 2000). This idea is controversial and requires a convincing demonstration of conspecific nutritional (or other) benefit resulting from the cell death of some proportion of the cells (Franklin & Berges, 2004). That cell death could provide nutritional benefit for remaining conspecifics is an idea that is easier to accept for yeast, because yeast cell division can be clearly asymmetric (e.g.…”

Temporal variation of caspase 3-like protein activity in cultures of the harmful dinoflagellates Karenia brevis and Karenia mikimotoi

“…However, several other species of microalgae have been proposed to undergo programmed cell death (PCD), necrosis (Dunn et al, 2002) as well as a range of intermediate cell death modes (Franklin and Berges, 2004;Franklin et al, 2006;Jiménez et al, 2009). Because it results in the complete loss of the organism, the occurrence of PCD in unicellular cells seems counterintuitive.…”

Effect of dead phytoplankton cells on the apparent efficiency of photosystem II

“…Heat-killed cells have a shrunken appearance, with cytoplasmic bunching and reduced chlorophyll fluorescence. These characteristics are similar to the 'senescent' appearance of microalgae in nutrientexhausted batch cultures, which are also called 'chlorotic' cells (La Roche et al 1993, Franklin & Berges 2004). Therefore, heat-killed cells may offer a reasonable physical simulation of natural dead cells, if one accepts that natural cell death in nature is caused primarily by nutrient starvation and results in the chlorotic state.…”