How an Organism Dies Affects the Fitness of Its Neighbors

Abstract

Programmed cell death (PCD), a genetically regulated cell suicide program, is ubiquitous in the living world. In contrast to multicellular organisms, in which cells cooperate for the good of the organism, in unicells the cell is the organism and PCD presents a fundamental evolutionary problem. Why should an organism actively kill itself as opposed to dying in a nonprogrammed way? Proposed arguments vary from PCD in unicells being maladaptive to the assumption that it is an extreme form of altruism. To test whether PCD could be beneficial to nearby cells, we induced programmed and nonprogrammed death in the unicellular green alga Chlamydomonas reinhardtii. Cellular contents liberated during non-PCD are detrimental to others, while the contents released during PCD are beneficial. The number of cells in growing cultures was used to measure fitness. Thermostability studies revealed that the beneficial effect of the PCD supernatant most likely involves simple heat-stable biomolecules. Non-PCD supernatant contains heat-sensitive molecules like cellular proteases and chlorophyll. These data indicate that the mode of death affects the origin and maintenance of PCD. The way in which an organism dies can have beneficial or deleterious effects on the fitness of its neighbors.

Programmed death in a unicellular organism has species-specific fitness effects

“…Growth dynamics were atypical due to the relatively nutrient-depleted media (PCD supernatant obtained after 1-2 days). The effect of PCD on growth of the same species was positive ( figure 2a,b), consistent with previous reports [5,11]. Unexpectedly, PCD supernatant from C. reinhardtii CC125 inhibited the growth of two other species, C. moewusii ( figure 2c,d) and C. debaryana (figure 2e,f ).…”

“…The mechanism is unknown; however, in another chlorophyte, Dunaliella salina, PCD releases organic materials that are either used directly by D. salina cells not undergoing PCD or re-mineralized by a co-habiting archaeon [11]. A similar mechanism may be at work in Chlamydomonas and is supported by our previous findings that the active ingredients are simple heat-stable molecules [5].…”

Candida albicans Czf1 and Efg1 Coordinate the Response to Farnesol during Quorum Sensing, White-Opaque Thermal Dimorphism, and Cell Death

“…Alternatively, white-to-opaque switching during stationary phase-a period typically characterized by nutrient limitation and increasing concentrations of farnesol-could result in a unique altruistic cooperation within the culture where the subpopulation that switches to opaque is killed by farnesol (8), resulting in the release of nutrients into the surrounding medium. Unicellular algal species, such as Chlamydomonas reinhardtii, release beneficial nutrients into the surrounding medium during programmed cell death (37), but this type of altruistic behavior has yet to be seen in a Candida species. A mechanism for triggering cell death within a subset of the Candida community, for example, within the matrix of a biofilm, could improve survival within a host.…”

The first suicides: a legacy inherited by parasitic protozoans from prokaryote ancestors

“…Although protozoan apoptosis has been argued to be an altruistic trait [9,108], evidence of benefit to surviving con-specifics is, so far, scarce. Durand and colleagues [109] have shown that the contents of the unicellular green algae, Chlamydomonas reinhardtii , were beneficial to colony members if PCD occurred, but harmful if it was non-PCD. However Segovia et al [110] claim that members of a colony of the chlorophyte Dunaliella tertiolecta that were kept in the dark did not gain from death associated with DNA fragmentation, caspase-like activity and morphological features of apoptosis of some members.…”