Did trypanosomatid parasites have photosynthetic ancestors?

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Abstract

Some molecular phylogenies of plastid-like genes suggest that chloroplasts (the structures responsible for photosynthesis in plants and algae) might have been secondarily lost in trypanosomatid parasites. Chloroplasts are present in some euglenids, which are closely related to trypanosomatids, and it has been argued that chloroplasts arose early in the diversification of the lineage Euglenozoa, to which trypanosomatids and euglenids belong (plastids-early hypothesis). This article reviews how euglenid ultrastructural systems are functionally integrated and phylogenetically correlated. I argue that chloroplast acquisition profoundly altered the structure of certain euglenids, and that the complete absence of these modifications in other euglenozoans is most consistent with their never having had a chloroplast. Ultrastructural evidence suggests that chloroplasts arose relatively recently within a specific subgroup of euglenids and that trypanosomatids are not secondarily non-photosynthetic (plastids-recent hypothesis).

Section snippets

Hypothetical origins of euglenozoan chloroplasts

The established sisterhood between kinetoplastids and euglenids has resulted in a rather counter-intuitive phylogenetic framework that closely links lethal human parasites (e.g. Trypanosoma) with innocuous free-living algae (e.g. Euglena) 4, 5, 6, 7 (Box 1; Figure 1). However, the chloroplasts in phototrophic euglenids were ultimately derived from a secondary endosymbiosis (see Glossary) with a green algal prey cell, an inference that is supported by biochemical, morphological and gene sequence

The diversification of bacterivores in euglenozoan evolution

The earliest stages of euglenozoan evolution were probably dominated by independent radiations of small bacterivores. Surveys of euglenozoan diversity indicate that (i) the majority of free-living kinetoplastids (all of which are bodonids) are very small bacterivores (∼5 μm long) and (ii) the majority of phagotrophic euglenids are also small bacterivores. Although current molecular phylogenetic data are tenuous, bodonids, in the broad sense, occupy the earliest diverging positions in

The first euglenids

The origin of the Euglenida is demarcated by the emergence of pellicle strips (Figure 1, Figure 2, step 1), which are cytoskeletal structures that are S-shaped in transverse section and composed mostly of a novel family of proteins called articulins 25, 26, 27. Pellicle strips run beneath the plasma membrane from anterior to posterior and articulate along their lateral margins (Figure 2). Although only a few species have been studied using electron microscopy, the earliest diverging euglenids

Origin of euglenid eukaryovory

Somatic plasticity is a basic requirement for any relatively small predator attempting to ingest large incompressible food items. Some euglenid predators are able to accommodate consumed prey cells that are close to their own size. Some species of Dinema, for instance, are relatively small euglenids with a rod-and-vane-based feeding apparatus that extends the length of the cell, as is the case in many bacterivores (Figure 2), but is capable of completely devouring very large and unyielding prey

The evolutionary radiation of phototrophic euglenids

Molecular phylogenies consistently place phototrophic euglenids in a monophyletic group that is nested within the Euglenozoa (Figure 1) 21, 35, 36, 37, 38, 39, 40. Moreover, it appears more than coincidental that the eukaryovore P. trichophorum is almost always a close sister lineage to phototrophic euglenids in molecular phylogenies 36, 37, 38, 40. This sisterhood is entirely congruent with comparative morphological data 22, 24. For instance, the earliest diverging phototrophic euglenids,

Concluding remarks and morphology-based implications

Although the plastids-early and plastids-recent hypotheses are both valid frameworks for future research, in my opinion, the overall pattern of morphological change in euglenids undermines the parsimony argument that is associated with the plastids-early hypothesis and favors a plastids-recent hypothesis in euglenozoan evolution (Figure 1). In addition, phagotrophic lineages are never intermixed with phototrophic lineages in molecular phylogenetic analyses, which would be an expectation of the

Acknowledgements

I gratefully acknowledge N.M. Fast, C.A. Leander, R. F. Waller, J.T. Harper and three anonymous reviewers for providing comments. This work was supported by the Canadian Institute for Advanced Research, Program in Evolutionary Biology. Several of the electron micrographs used for illustrative purposes were acquired during my doctoral research, which was supported by an NSF-PEET grant to R. E. Triemer and M. A. Farmer.

Glossary

Glossary

Bodonids:
refers to mostly free-living kinetoplastids with an anteriorly directed dorsal flagellum, a posteriorly directed ventral flagellum and a simple feeding apparatus.
Euglenoid Movement:
a peculiar wriggling movement facilitated by the sliding of adjacent pellicle strips. Movements can range from subtle deformations in cell shape to highly coordinated cycles of peristalsis-like deformations. Euglenoid movement is a basic property of eukaryovorous euglenids, some phototrophic euglenids, and

References (51)

  • M.A. Farmer et al.

    Flagellar systems in the euglenoid flagellates

    Biosystems

    (1988)
  • D. Patterson

    The diversity of eukaryotes

    Am. Nat.

    (1999)
  • A.J. Roger

    Reconstructing early events in eukaryotic evolution

    Am. Nat.

    (1999)
  • R.E. Triemer et al.

    An ultrastructural comparison of the mitotic apparatus, feeding apparatus, flagellar apparatus and cytoskeleton in euglenoids and kinetoplastids

    Protoplasma

    (1991)
  • A.G.B. Simpson et al.

    Protein phylogenies robustly resolve deep-level relationships within Euglenozoa

    Mol. Phylog. Evol.

    (2003)
  • P.A. Kivic et al.

    An evaluation of the possible phylogenetic relationship between Euglenophyta and Kinetoplastida

    Orig. Life

    (1984)
  • R.B. Hallick

    Complete sequence of Euglena gracilis chloroplast DNA

    Nucleic Acids Res.

    (1993)
  • S.P. Gibbs

    The chloroplasts of Euglena might have evolved from symbiotic green algae

    Can. J. Bot.

    (1978)
  • V. Hannaert

    Plant-like traits associated with metabolism of Trypanosoma parasites

    Proc. Natl. Acad. Sci. U. S. A.

    (2003)
  • W. Martin et al.

    Secondary loss of chloroplasts in trypanosomatids

    Proc. Natl. Acad. Sci. U. S. A.

    (2003)
  • J.O. Anderson et al.

    A cyanobacterial gene in nonphotosynthetic protists - An early chloroplast acquisition in eukaryotes?

    Curr. Biol.

    (2002)
  • T. Cavalier-Smith et al.

    Phylogeny of the choanozoa, apusozoa, and other protozoa and early eukayote megaevolution

    J. Mol. Evol.

    (2003)
  • T. Cavalier-Smith

    Principles of protein and lipid targeting in secondary symbiogenesis: Euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree

    J. Eukaryot. Microbiol.

    (1999)
  • H. Nozaki

    The phylogenetic position of red algae revealed by multiple nuclear genes from mitochondria-containing eukaryotes and an alternative hypothesis on the origin of plastids

    J. Mol. Evol.

    (2003)
  • Rogers, M.B., Keeling and P.J. Lateral transfer and re-compartmentalisation in Calvin cycle enzymes in plants and...

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