Abstract
BackgroundThe photosynthetic organelle (plastid) originated via primary endosymbiosis in which a phagotrophic protist captured and harnessed a cyanobacterium. The plastid was inherited by the common ancestor of the red, green (including land plants), and glaucophyte algae (together, the Plantae). Despite the critical importance of primary plastid endosymbiosis, its ancient derivation has left behind very few “footprints” of early key events in organelle genesis.Methodology/Principal FindingsTo gain insights into this process, we conducted an in-depth phylogenomic analysis of genomic data (nuclear proteins) from 17 Plantae species to identify genes of a surprising provenance in these taxa, Chlamydiae bacteria. Previous studies show that Chlamydiae contributed many genes (at least 21 in one study) to Plantae that primarily have plastid functions and were postulated to have played a fundamental role in organelle evolution. Using our comprehensive approach, we identify at least 55 Chlamydiae-derived genes in algae and plants, of which 67% (37/55) are putatively plastid targeted and at least 3 have mitochondrial functions. The remainder of the proteins does not contain a bioinformatically predicted organelle import signal although one has an N-terminal extension in comparison to the Chlamydiae homolog. Our data suggest that environmental Chlamydiae were significant contributors to early Plantae genomes that extend beyond plastid metabolism. The chlamydial gene distribution and protein tree topologies provide evidence for both endosymbiotic gene transfer and a horizontal gene transfer ratchet driven by recurrent endoparasitism as explanations for gene origin.Conclusions/SignificanceOur findings paint a more complex picture of gene origin than can easily be explained by endosymbiotic gene transfer from an organelle-like point source. These data significantly extend the genomic impact of Chlamydiae on Plantae and show that about one-half (30/55) of the transferred genes are most closely related to sequences emanating from the genome of the only environmental isolate that is currently available. This strain, Candidatus Protochlamydia amoebophila UWE25 is an endosymbiont of Acanthamoeba and likely represents the type of endoparasite that contributed the genes to Plantae.
Highlights
The origin of the photosynthetic organelle in eukaryotes occurred via the capture and enslavement of a cyanobacterium [1,2]
Later analyses showed that many of these proteins are plastid-targeted in plants [15]. These findings led to a number of different hypotheses to explain chlamydial gene origin in photosynthetic eukaryotes including an ancient, unappreciated relationship between Chlamydiae and the cyanobacterial donor of the plastid [15], the possibility that infected insects may have been the vectors for introducing Chlamydiae genes into plants [20], and ancient horizontal gene transfer from Chlamydiae to the Plantae ancestor that may have played a role in plastid establishment (e.g., [17,21])
Our ability to identify a larger set of Chlamydiae genes than Huang and Gogarten [22] likely reflected the fact that we used the combined protein set from 17 Plantae genomes, thereby including as large a diversity of query sequences as possible
Summary
The origin of the photosynthetic organelle (plastid) in eukaryotes occurred via the capture and enslavement of a cyanobacterium (primary endosymbiosis) [1,2] This ‘‘primary’’ plastid is shared by the red, green (including land plants), and glaucophyte algae (together the Plantae) [3,4]. We use phylogenomics to search for genes contributed to Plantae by a surprising source, Chlamydiae bacteria These prokaryotes are well known as obligate intracellular vertebrate pathogens and encode a unique gene, the ADP/ATP translocase to parasitize energy from the host. Despite the critical importance of primary plastid endosymbiosis, its ancient derivation has left behind very few ‘‘footprints’’ of early key events in organelle genesis
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