Taming chlorophylls by early eukaryotes underpinned algal interactions and the diversification of the eukaryotes on the oxygenated Earth

Abstract

Extant eukaryote ecology is primarily sustained by oxygenic photosynthesis, in which chlorophylls play essential roles. The exceptional photosensitivity of chlorophylls allows them to harvest solar energy for photosynthesis, but on the other hand, they also generate cytotoxic reactive oxygen species. A risk of such phototoxicity of the chlorophyll must become particularly prominent upon dynamic cellular interactions that potentially disrupt the mechanisms that are designed to quench photoexcited chlorophylls in the phototrophic cells. Extensive examination of a wide variety of phagotrophic, parasitic, and phototrophic microeukaryotes demonstrates that a catabolic process that converts chlorophylls into nonphotosensitive 132,173-cyclopheophorbide enols (CPEs) is phylogenetically ubiquitous among extant eukaryotes. The accumulation of CPEs is identified in phagotrophic algivores belonging to virtually all major eukaryotic assemblages with the exception of Archaeplastida, in which no algivorous species have been reported. In addition, accumulation of CPEs is revealed to be common among phototrophic microeukaryotes (i.e., microalgae) along with dismantling of their secondary chloroplasts. Thus, we infer that CPE-accumulating chlorophyll catabolism (CACC) primarily evolved among algivorous microeukaryotes to detoxify chlorophylls in an early stage of their evolution. Subsequently, it also underpinned photosynthetic endosymbiosis by securing close interactions with photosynthetic machinery containing abundant chlorophylls, which led to the acquisition of secondary chloroplasts. Our results strongly suggest that CACC, which allowed the consumption of oxygenic primary producers, ultimately permitted the successful radiation of the eukaryotes throughout and after the late Proterozoic global oxygenation.

The Cell Division Cycle of Euglena gracilis Indicates That the Level of Circadian Plasticity to the External Light Regime Changes in Prolonged-Stationary Cultures

“…Previous studies have reported that dark orange or reddish-brown to dark brown globules are commonly observed within Euglenida cells in aged cultures [ 25 , 26 ]. Consistent with this, we observed several brown globules within cells from 1- or 2-month-old cultures ( Figure 1 B; Supplementary Figure S2 ).…”

“…Consistent with this, we observed several brown globules within cells from 1- or 2-month-old cultures ( Figure 1 B; Supplementary Figure S2 ). Kashiyama et al [ 26 ] isolated the brown globules from E. gracilis cells, and determined that they contained chlorophyll- a -derived 13 2 ,17 3 -cyclopheophorbides a enol (cPPB- a E) and related compounds. Since cPPB- a E and its derivatives gradually accumulate in E. gracilis cells after the stationary phase, Kashiyama et al [ 26 ] concluded that globule formation was associated with 13 2 ,17 3 -cyclopheophorbide enol (CPE)-accumulating chlorophyll catabolism (CACC) during chloroplast dismantling.…”

“…Kashiyama et al [ 26 ] isolated the brown globules from E. gracilis cells, and determined that they contained chlorophyll- a -derived 13 2 ,17 3 -cyclopheophorbides a enol (cPPB- a E) and related compounds. Since cPPB- a E and its derivatives gradually accumulate in E. gracilis cells after the stationary phase, Kashiyama et al [ 26 ] concluded that globule formation was associated with 13 2 ,17 3 -cyclopheophorbide enol (CPE)-accumulating chlorophyll catabolism (CACC) during chloroplast dismantling. Our previous studies [ 27 , 28 , 29 ] showed that although the cellular chlorophyll ( a + b ) content of E. gracilis , grown under high-intensity light or in cold and intense light conditions, decreased by up to 75% and 87%, respectively, pigmented brown globules were not observed within stressed cells.…”

Effect of pH on metabolite excretion and cell morphology of Euglena gracilis under dark, anaerobic conditions

“…3). In E. gracilis cultivated under dark conditions, chloroplasts are degraded, but brown granules remain in the cells [34]. These granules are reported to be massive membrane structures generated from degraded thylakoids [34].…”

Synthesis of Cationic Pyridinium‐(Bacterio)Chlorophyll Conjugates Bearing a Bacteriochlorin, Chlorin, or Porphyrin π‐Skeleton and their Photophysical and Electrochemical Properties

“…Naturally occurring chlorophylls (Chls) primarily function as photosynthetic pigments, and are observed in metabolites of phototrophs as well as in aqueous environments and sediments They have various molecular structures with three types of cyclic tetrapyrroles . Bacteriochlorophyll(BChl)‐ a is found in anoxygenic photosynthetic bacteria.…”