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SECONDARY SYMBIOTIC ORIGIN OF ALGAL PLASTIDS
AND THE PHYLOGENY OF THE
BANGIOPHYCIDAE (RHODOPHYTA)
(NSF DEB-01-07754)

     
  PI: Debashish Bhattacharya
  Co-PIs: Kirsten Müller
    Robert Sheath

PROJECT SUMMARY:
The ability to engulf and incorporate a previously free-living bacterial (primary symbiosis) or eukaryotic (secondary symbiosis) cell and transform it into an organelle is one of the defining characteristics of eukaryotes. Understanding the process of organelle genesis provides, therefore, fundamental insights into eukaryotic evolution. All plastids likely trace their origin to a single cyanobacterial primary symbiosis in the common ancestor of the red, green, and glaucophyte algae (Fig. A). In contrast, secondary symbiosis has led to the origin of photosynthesis in evolutionarily distantly related protists multiple independent times. The number of secondary symbioses and the specific source(s) of the different secondary plastids is, however, unknown in most cases. The red algae, composed of the subclasses Bangiophycidae and Florideophycidae, offer a model for understanding secondary symbiosis because Bangiophycidae are the sources of secondary plastids in four major algal groups (Cryptophyta, Haptophyta, Heterokonta, Dinophyceae). This proposal addresses the phylogenetic relationship between plastids in Bangiophycidae and their descendants (through secondary symbiosis) in Cryptophyta, Haptophyta, and Heterokonta (Fig. B), and the systematics of the Bangiophycidae. We will determine the phylogeny of plastids in the Bangiophycidae, Cryptophyta, Haptophyta, and Heterokonta by comparing concatenated plastid small subunit (SSU) rDNA and RuBisCo large subunit (rbcL) coding regions. The phylogeny of the Bangiophycidae nuclear lineage will be inferred by analyzing concatenated nuclear and plastid SSU rDNA, rbcL, and mitochondrial coxI coding regions.

  
Results of preliminary phylogenetic analyses of nuclear and plastid DNA coding regions show that one of the major orders of the Bangiophycidae, the Porphyridiales, is split into at least three different lineages and that the Florideophycidae is monophyletic with weak support for an origin from the Bangiales (Fig. A). We have determined that the plastids of the Heterokonta are likely derived from members of the Cyanidiales and are not directly related to the plastids in the Cryptophyta and the Haptophyta.  
These results lead us to make five major hypotheses about secondary symbiosis and the
evolutionary history of the Bangiophycidae that will be tested in the proposed research:
  • Secondary plastids in the Cryptophyta, Haptophyta, and Heterokonta have polyphyletic
    origins (scenario 1 in Fig. B). An alternative scenario (scenario 2 in Fig. B) is that a single
    secondary symbiosis, followed by divergence of the host cells, explains plastid origin in
    these algae.
  • The Cyanidiales is the source of plastids in the Heterokonta.
  • Porphyridiales is paraphyletic, and requires a major taxonomic revision (Fig. A).
  • The Bangiales is the sister group of the Florideophycidae, with support from morphological
    data such as the association of the Golgi apparatus with the mitochondrion in these groups.
  • Vegetative morphology (e.g., uni- or multicellular) is convergent in different lineages of the
    Bangiophycidae.
Our multi-gene approach will resolve the ancestry of the secondary plastids in the Cryptophyta,
Haptophyta, and Heterokonta and will result in a natural classification of the Rhodophyta. These
results will be of fundamental importance to understanding the process of organelle genesis and
the radiation of one of the most ancient photosynthetic groups on our planet.


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