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MBE Advance Access published online on September 21, 2006
Molecular Biology and Evolution, doi:10.1093/molbev/msl129
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© The Author 2006. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org
Accepted September 18, 2006

Research Article

The Complete Chloroplast Genome of the Chlorarachniophyte Bigelowiella natans: Evidence for Independent Origins of Chlorarachniophyte and Euglenid Secondary Endosymbionts

Matthew B. Rogers 1, Paul R. Gilson 2, Vanessa Su 3, Geoffrey I. McFadden 3, and Patrick J. Keeling 1 *

1 Botany Department, University of British Columbia, British Columbia, Canada
2 The Walter and Eliza Hall Institute of Medical Research, Parkville 3050, Australia
3 School of Botany, University of Melbourne, VIC 3010, Australia

* To whom correspondence should be addressed.
Patrick J. Keeling, E-mail: pkeeling{at}interchange.ubc.ca


  Abstract

Chlorarachniophytes are amoeboflagellate cercozoans that acquired a plastid by secondary endosymbiosis. Chlorarachniophytes are the last major group of algae for which there is no completely sequenced plastid genome. Here we describe the 69.2 kbp chloroplast genome of the model chlorarachniophyte Bigelowiella natans. The genome is highly reduced in size compared with plastids of other photosynthetic algae, and is closer in size to genomes of several non-photosynthetic plastids. Unlike non-photosynthetic plastids, however, the B. natans chloroplast genome has not sustained a massive loss of genes, and it retains nearly all of the functional photosynthesis-related genes represented in the genomes of other green algae. Instead, the genome is highly compacted and gene-dense. The genes are organized with a strong strand bias and several unusual rearrangements and inversions also characterize the genome; notably an inversion in the SSU rRNA gene, a translocation of three genes in the major ribosomal protein operon, and the fragmentation of the cluster encoding the large photosystem proteins PsaA and PsaB. The chloroplast endosymbiont is known to be a green alga, but its evolutionary origin and relationship to other primary and secondary green plastids has been much debated. A recent hypothesis proposes that the endosymbionts of chlorarachniophytes and euglenids share a common origin (the Cabozoa hypothesis). We inferred phylogenies using individual and concatenated gene sequences for all genes in the genome. Concatenated gene phylogenies show a relationship between the B. natans plastid and the ulvophyte-trebouziophyte-chlorophte clade of green algae to the exclusion of Euglena. The B. natans plastid is thus not closely related to that of Euglena, which suggests plastids originated independently in these two groups and the Cabozoa hypothesis is false.

Keywords: plastid; genome; chlorarachniophyte; phylogeny; endosymbiosis.
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