Morphostasis in a novel eukaryote illuminates the evolutionary transition from phagotrophy to phototrophy: description of Rapaza viridis n. gen. et sp. (Euglenozoa, Euglenida)

Abstract

BackgroundMorphostasis of traits in different species is necessary for reconstructing the evolutionary history of complex characters. Studies that place these species into a molecular phylogenetic context test hypotheses about the transitional stages that link divergent character states. For instance, the transition from a phagotrophic mode of nutrition to a phototrophic lifestyle has occurred several times independently across the tree of eukaryotes; one of these events took place within the Euglenida, a large group of flagellates with diverse modes of nutrition. Phototrophic euglenids form a clade that is nested within lineages of phagotrophic euglenids and that originated through a secondary endosymbiosis with green algae. Although it is clear that phototrophic euglenids evolved from phagotrophic ancestors, the morphological disparity between species representing these different nutritional modes remains substantial.ResultsWe cultivated a novel marine euglenid, Rapaza viridis n. gen. et sp. ("green grasper"), and a green alga, Tetraselmis sp., from the same environment. Cells of R. viridis were comprehensively characterized with light microscopy, SEM, TEM, and molecular phylogenetic analysis of small subunit rDNA sequences. Ultrastructural and behavioral observations demonstrated that this isolate habitually consumes a specific strain of Tetraselmis prey cells and possesses a functional chloroplast that is homologous with other phototrophic euglenids. A novel feeding apparatus consisting of a reduced rod of microtubules facilitated this first and only example of mixotrophy among euglenids. R. viridis also possessed a robust photoreception apparatus, two flagella of unequal length, euglenoid movement, and a pellicle consisting of 16 strips and one (square-shaped) whorl of posterior strip reduction. The molecular phylogenetic data demonstrated that R. viridis branches as the nearest sister lineage to phototrophic euglenids.ConclusionsThe unusual combination of features in R. viridis combined with its molecular phylogenetic position completely conforms to the expected transitional stage that occurred during the early evolution of phototrophic euglenids from phagotrophic ancestors. The marine mixotrophic mode of nutrition, the preference for green algal prey cells, the structure of the feeding apparatus, and the organization of the pellicle are outstanding examples of morphostasis that clarify pivotal stages in the evolutionary history of this diverse group of microbial eukaryotes.

Evolutionary Origin of Euglena

“…Whereas the monophyly of the Euglenozoa is indisputable, the internal relationships among kinetoplastids, diplonemids, symbiontids and euglenids are less clear. The most controversial is the phylogenetic position of symbiontids, which group together with bacteriovorus euglenids -in effect the Euglenida seems to be paraphyletic (Yamaguchi et al 2012;Breglia et al 2013). Symbiontids are a small group of microaerophilic or anaerobic euglenozoans enveloped by episymbiotic bacteria.…”

“…This species contains functional chloroplasts but its photosynthetic capacity is probably not sufficient to support growth. The crucial component of the R. viridis diet is a green alga prey Tetraselmis sp., which is engulfed by phago-or myzocytosis (Yamaguchi et al 2012). Other green euglenids are split into two groups: Eutreptiales, which comprises species living in marine and brackish environment and Euglenales (=Euglenea) containing species living mostly in small, astatic freshwater reservoirs.…”

Diversity and Evolutionary History of the Symbiontida (Euglenozoa)

“…The group is distinguished from other euglenozoans by a system of proteinaceous pellicle strips that subtend the plasma membrane (Leander et al, 2007). Most phagotrophic euglenids inhabit marine environments, and most photosynthetic lineages inhabit freshwater environments; however, the three earliest branching lineages of photosynthetic euglenids, Rapaza, Eutreptia, and Eutreptiella, also inhabit marine environments (Yamaguchi et al, 2012). The largest (>20 microns) phagotrophic euglenids tend to be eukaryovorous and possesses a flexible pellicle and a robust feeding apparatus.…”

“…The largest (>20 microns) phagotrophic euglenids tend to be eukaryovorous and possesses a flexible pellicle and a robust feeding apparatus. Eukaryovorous modes of feeding facilitated the secondary endosymbiotic origin of euglenid chroloplasts from a close relative of Pyramimonas, a marine lineage of green algae (Leander, 2004;Yamaguchi et al, 2012;Jackson et al, 2018). Eukaryovore euglenids are the closest relatives to the clade of photosynthetic euglenids, and the earliest branching lineage within photosynthetic euglenids, namely Rapaza viridis, is a mixotroph capable of eukaryovory (Yamaguchi et al, 2012).…”

A contemplation on the secondary origin of green algal and plant plastids

“…Phagocytosis appears to be better retained in photosynthetic eukaryotes harboring secondary or tertiary plastids. These include phago-mixotrophic members of the chlorarachniophytes, cryptophytes, dinoflagellates, euglenophytes, haptophytes, and stramenopiles [57,58]. Better retention of phagotrophy might be partially explained by a relatively shorter time that has elapsed since secondary-or tertiary-plastid bearing lineages became phototrophic; in other words, with less time, there is more chance that phagocytosis has been retained.…”