Photoparasitism as an Intermediate State in the Evolution of Apicomplexan Parasites
Despite the benefits of phototrophy, many algae have lost photosynthesis and have converted back to heterotrophy. Parasitism is a heterotrophic strategy, with apicomplexans being among the most devastating parasites for humans. The presence of a nonphotosynthetic plastid in apicomplexan parasites suggests their phototrophic ancestry. The discovery of related phototrophic chromerids has unlocked the possibility to study the transition between phototrophy and parasitism in the Apicomplexa. The chromerid Chromera velia can live as an intracellular parasite in coral larvae as well as a free-living phototroph, combining phototrophy and parasitism in what I call photoparasitism. Since early-branching apicomplexans live extracellularly, their evolution from an intracellular symbiont is unlikely. In this opinion article I discuss possible evolutionary trajectories from an extracellular photoparasite to an obligatory apicomplexan parasite.
phototrophy, mixotrophy, parasitism, photoparasitism, evolution, Apicomplexa
- Apicomplexan parasites evolved from a phototrophic ancestor.
- Parasitism evolved multiple times in the Apicomplexa and in Apicomplexa-like protists.
- Chromerid algae are the closest known phototrophic relatives of parasitic Apicomplexa.
- The chromerid Chromera velia is a free-living alga that can infect coral larvae and live like a parasite.
Apicomplexans Are Parasitic Algae
Apicomplexan parasites are obligate parasites of animals, including humans. They are responsible for hundreds of thousands of deaths annually (malaria) and high economic losses. These alveolate parasitic protists are characterized by the presence of the apical complex, a set of tubular and vesicular organelles at the anterior apex of the cell used for penetration of the host cell . Apicomplexan parasites contain highly reduced organelles; the mitochondrion and the apicoplast (see Glossary), a relic nonphotosynthetic plastid [1,2]. The plastid has lost photosynthetic function, is surrounded by four membranes, suggesting its origin in a complex endosymbiosis, and contains a circular genome about 35 kb in size which lacks any traces of genes encoding photosynthetic functions [3–7]. Despite the absence of photosynthetic ability, the plastid is essential for the host cell because it is responsible for the synthesis of indispensable compounds such as heme, isoprenoids, and fatty acids. However, not all apicomplexans contain the plastid. Although complete loss of the plastid is quite rare in nature it has happened at least three times in the evolution of the Apicomplexa [3,4,8] (Figure 1): in protists of the genus Cryptosporidium, intestinal parasites of mammals and birds, and twice in neogregarines , a group of gregarines that usually infect the gut of insects and worms . Both groups of protists are related and constitute early branches in the apicomplexan phylogenetic tree (Figure 1); in some taxonomic systems the genus Cryptosporidium is even classified within the frame of gregarines . Apicomplexans are members of myzozoans , a group of protists capable of myzocytosis, a modified version of phagocytosis. The group also contains coral-associated complex algae named chromerids [10,11]; their relatives, colpodellids, predatory nonphotosynthetic marine flagellates (Figure 2); and dinoflagellates – marine and freshwater algae with complex plastids . Colpodellids contain a plastid that lacks both a genome and photosynthetic ability , but which hosts the same essential pathways as the apicoplast. The presence of the plastid in the Apicomplexa has led to the suggestion that these deadly parasites have evolved from a photosynthetic algal ancestor  and that they are just modified algae. However, the evolutionary pathway leading from a photoautotrophic alga to an obligate parasite had been, for a long time, difficult to trace because of the absence of close phototrophic relatives to parasitic apicomplexans. This obstacle was overcome by the discovery of chromerids [10,11].
Chromerids Are the Old Phototrophic Sisters of Parasitic Apicomplexans
Although the phototrophic ancestry of apicomplexans is beyond reasonable doubt, it was rather difficult to find their close photosynthetic relatives. The apicomplexan sister group, dinoflagellates, could not be efficiently used for meaningful comparison because they are too divergent. Frankly speaking, dinoflagellates are so unusual that they are difficult to compare to any other alveolates. They contain extremely large genomes, organized on chromosomes condensed during the entire life cycle, but are known to lack regular eukaryotic histones, which have been replaced by the virus-originated histone-like proteins . Their original peridinin-pigmented plastid of supposedly secondary origin contains a highly reduced and diverse genome, containing only photosynthesis-related genes and ribosomal RNA genes, all located on minicircles . Any attempts at comparison of the dinoflagellate plastid genome with that of the apicoplast failed, either because of no overlap in the protein-coding genes , or due to the high divergence of the rRNA genes [17,18]. Only the discovery of coral-associated chromerid algae [10,11] yielded a model useful for the comparison of relatively closely related phototrophic and obligate parasitic protists. So far, only two chromerid species, Chromera velia  and Vitrella brassicaformis , have been formally described and are available in culture. They are fully phototrophic, with plastid characterized by the absence of chlorophyll c, a pigment typical for algae with a rhodophyte-derived plastid [10,11]. Although the two species are the closest phototrophic relatives within apicomonads , they differ substantially in their morphology [10,11,19–23]; life cycles [10,11,21,23]; nuclear , plastid , and mitochondrial genomes ; and likely also their lifestyles. While an apical complex reduced to the form of the pre-conoid was found in C. velia [21,22], any such structure is absent from V. brassicaformis . This may suggest a more intimate association between C. velia and its coral host than the second chromerid has.
Oborník M. 2020: Photoparasitism as an intermediate state in the evolution of apicomplexan parasites. Trends in Parasitology (in press). [IF=6.918]