Comparative Genomics of a Bacterivorous Green Alga Reveals Evolutionary Causalities and Consequences of Phago-Mixotrophic Mode of Nutrition

Genome Biology and Evolution, Nov 2015

Cymbomonas tetramitiformis—a marine prasinophyte—is one of only a few green algae that still retain an ancestral particulate-feeding mechanism while harvesting energy through photosynthesis. The genome of the alga is estimated to be 850 Mb–1.2 Gb in size—the bulk of which is filled with repetitive sequences—and is annotated with 37,366 protein-coding gene models. A number of unusual metabolic pathways (for the Chloroplastida) are predicted for C. tetramitiformis, including pathways for Lipid-A and peptidoglycan metabolism. Comparative analyses of the predicted peptides of C. tetramitiformis to sets of other eukaryotes revealed that nonphagocytes are depleted in a number of genes, a proportion of which have known function in feeding. In addition, our analysis suggests that obligatory phagotrophy is associated with the loss of genes that function in biosynthesis of small molecules (e.g., amino acids). Further, C. tetramitiformis and at least one other phago-mixotrophic alga are thus unique, compared with obligatory heterotrophs and nonphagocytes, in that both feeding and small molecule synthesis-related genes are retained in their genomes. These results suggest that early, ancestral host eukaryotes that gave rise to phototrophs had the capacity to assimilate building block molecules from inorganic substances (i.e., prototrophy). The loss of biosynthesis genes, thus, may at least partially explain the apparent lack of instances of permanent incorporation of photosynthetic endosymbionts in later-divergent, auxotrophic eukaryotic lineages, such as metazoans and ciliates.

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Comparative Genomics of a Bacterivorous Green Alga Reveals Evolutionary Causalities and Consequences of Phago-Mixotrophic Mode of Nutrition

Advance Access publication July Comparative Genomics of a Bacterivorous Green Alga Reveals Evolutionary Causalities and Consequences of Phago-Mixotrophic Mode of Nutrition John A. Burns 0 Amber Paasch 0 Apurva Narechania 0 Eunsoo Kim 0 0 Sackler Institute for Comparative Genomics and Division of Invertebrate Zoology, American Museum of Natural History , New York, NY Cymbomonas tetramitiformis-a marine prasinophyte-is one of only a few green algae that still retain an ancestral particulatefeeding mechanism while harvesting energy through photosynthesis. The genome of the alga is estimated to be 850 Mb-1.2 Gb in size-the bulk of which is filled with repetitive sequences-and is annotated with 37,366 protein-coding gene models. A number of unusual metabolic pathways (for the Chloroplastida) are predicted for C. tetramitiformis, including pathways for Lipid-A and peptidoglycan metabolism. Comparative analyses of the predicted peptides of C. tetramitiformis to sets of other eukaryotes revealed that nonphagocytes are depleted in a number of genes, a proportion of which have known function in feeding. In addition, our analysis suggests that obligatory phagotrophy is associated with the loss of genes that function in biosynthesis of small molecules (e.g., amino acids). Further, C. tetramitiformis and at least one other phago-mixotrophic alga are thus unique, compared with obligatory heterotrophs and nonphagocytes, in that both feeding and small molecule synthesis-related genes are retained in their genomes. These results suggest that early, ancestral host eukaryotes that gave rise to phototrophs had the capacity to assimilate building block molecules from inorganic substances (i.e., prototrophy). The loss of biosynthesis genes, thus, may at least partially explain the apparent lack of instances of permanent incorporation of photosynthetic endosymbionts in later-divergent, auxotrophic eukaryotic lineages, such as metazoans and ciliates. Chloroplastida; Cymbomonas; green algae; mixotrophy; phagocytosis Introduction Chloroplastida (or Viridiplantae) is one of the major eukaryotic lineages, comprising green algae and land plants (Adl et al. 2012) . The group is rich in diversity, including about 370,000 described species (Melkonian 1990; Plant List 2013) , and is responsible for about half of the total global primary production (Kirchman 2012) . Together, Chloroplastida, Rhodophyta, and Glaucophyta constitute Archaeplastida, the group characterized by having a plastid that is bound by two membranes, which is the basis for classifying them as primary plastids (i.e., direct descendants of endosymbiotic cyanobacteria) (Archibald 2009) . The three archaeplastid lineages are assumed by many to have originated from a shared endosymbiotic event and to form a monophyletic group. However, data, especially those bearing on nucleocytoplasmic traits, thus far have not been able to unambiguously support the “Archaeplastida” hypothesis (Mackiewicz and Gagat 2014; Stiller 2014) . Of the primary-plastid-containing eukaryotes, only a few are known to be phagocytotic, despite the presumption that phagocytotic engulfment of a photo-symbiont was necessary for the evolution of a photosynthetic organelle (Maruyama and Kim 2013) . Most primary-plastid-bearing eukaryotes appear therefore to have lost the capacity to feed on bacteria or other large particulate matter, presumably as phototrophy took over the primary nutritive role after plastids were acquired (Raven et al. 2009; Cavalier-Smith 2013) . No red algae or glaucophytes are known to be phagocytotic; however, some “early-diverging” green algae have been suggested to be phago-mixotrophic based on their internal cell morphology (Moestrup et al. 2003; Maruyama and Kim 2013) . Of these, the marine tetraflagellate Cymbomonas tetramitiformis was definitively confirmed to engulf bacteria by transmission electron microscopy (Maruyama and Kim 2013) . This green alga (fig. 1) appears to utilize a tubular channel to transport particles from the exterior environment into a permanent acidic vacuole, where digestion takes place (Maruyama and Kim 2013) . Note that internalization of bacteria into root cells has been reported from some flowering plants (e.g., Leborgne-Castel et al. 2010; Paungfoo-Lonhienne et al. 2010) ; however, it is structurally different from green algal phagocytosis (e.g., absence/presence of a feeding channel) and thus likely represents a derived trait (also see CavalierSmith 2013), possibly stemming from inherent properties of the eukaryotic cell membrane. From a broad evolutionary perspective, phagocytosis is restricted to the eukaryotes and is absent in prokaryotes (Cavalier-Smith 2002) . The distribution of phagocytosis across a wide range of eukaryotic groups suggests that phagocytosis was present in the last eukaryotic common ancestor (LECA), although it has since been lost in several lineages after they diverged from LECA (Cavalier-Smith 20 (...truncated)


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John A. Burns, Amber Paasch, Apurva Narechania, Eunsoo Kim. Comparative Genomics of a Bacterivorous Green Alga Reveals Evolutionary Causalities and Consequences of Phago-Mixotrophic Mode of Nutrition, Genome Biology and Evolution, 2015, pp. 3047-3061, 7/11, DOI: 10.1093/gbe/evv144