Impact of light intensity and quality on chromatophore and nuclear gene expression in Paulinella chromatophora, an amoeba with nascent photosynthetic organelles.
Plastid evolution has been attributed to a single primary endosymbiotic event that occurred about 1.6 billion years ago (BYA) in which a cyanobacterium was engulfed and retained by a eukaryotic cell, although early steps in plastid integration are poorly understood. The photosynthetic amoeba Paulinella chromatophora represents a unique model for the study of plastid evolution because it contains cyanobacterium-derived photosynthetic organelles termed 'chromatophores' that originated relatively recently (0.09-0.14 BYA). The chromatophore genome is about a third the size of the genome of closely related cyanobacteria, but 10-fold larger than most plastid genomes. Several genes have been transferred from the chromatophore genome to the host nuclear genome through endosymbiotic gene transfer (EGT). Some EGT-derived proteins could be imported into chromatophores for function. Two photosynthesis-related genes (psaI and csos4A) are encoded by both the nuclear and chromatophore genomes, suggesting that EGT in Paulinella chromatophora is ongoing. Many EGT-derived genes encode proteins that function in photosynthesis and photoprotection, including an expanded family of high-light-inducible (ncHLI) proteins. Cyanobacterial hli genes are high-light induced and required for cell viability under excess light. We examined the impact of light on Paulinella chromatophora and found that this organism is light sensitive and lacks light-induced transcriptional regulation of chromatophore genes and most EGT-derived nuclear genes. However, several ncHLI genes have reestablished light-dependent regulation, which appears analogous to what is observed in cyanobacteria. We postulate that expansion of the ncHLI gene family and its regulation may reflect the light/oxidative stress experienced by Paulinella chromatophora as a consequence of the as yet incomplete integration of host and chromatophore metabolisms.
Department of Plant Biology, Carnegie Institution for Science, Stanford, CA, 94305, USA.
Ru
http://orcid.org/0000-0002-4860-7800
R
Zhang
Department of Plant Biology, Carnegie Institution for Science, Stanford, CA, 94305, USA.|Department of Biology, Heinrich Heine University, Düsseldorf, 40225, Germany.
Eva C M
EC
Nowack
Department of Plant Biology and Pathology, Rutgers University, New Brunswick, NJ, 08901, USA.
Dana C
DC
Price
Department of Ecology, Evolution and Natural Resources, Rutgers University, New Brunswick, NJ, 08901, USA.
Debashish
D
Bhattacharya
Department of Plant Biology, Carnegie Institution for Science, Stanford, CA, 94305, USA.
Arthur R
AR
Grossman
D000656:Amoeba / Q000166:cytology* / Q000378:metabolism*; D002856:Chromatophores / Q000378:metabolism*; D008027:Light; D018384:Oxidative Stress / Q000528:radiation effects; D010788:Photosynthesis / Q000235:genetics / Q000502:physiology; D018087:Plastids / Q000378:metabolism; D013559:Symbiosis / Q000528:radiation effects

Paulinella chromatophora
; endosymbiotic gene transfer; excess light; high-light-inducible proteins; oxidative stress; plastid evolution; primary endosymbiosis