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)