Evolutionary dynamics of the chromatophore genome in three photosynthetic Paulinella species

• Published in: Scientific reports Vol. 9; no. 1; p. 2560
• Main Authors: Lhee, Duckhyun, Ha, Ji-San, Kim, Sunju, Park, Myung Gil, Bhattacharya, Debashish, Yoon, Hwan Su
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 22.02.2019; Nature Publishing Group
• Subjects: 45; 45/23; 631/181/757; 631/449; Chromatophores; Deoxyribonucleic acid; DNA; Gene deletion; Gene families; Genes; Genomes; Humanities and Social Sciences; Insertion; multidisciplinary; Nucleotide sequence; Paulinella; Plastids; Science; Science (multidisciplinary)
• ISSN: 2045-2322; 2045-2322
• DOI: 10.1038/s41598-019-38621-8

The thecate amoeba Paulinella is a valuable model for understanding plastid organellogenesis because this lineage has independently gained plastids (termed chromatophores) of alpha-cyanobacterial provenance. Plastid primary endosymbiosis in Paulinella occurred relatively recently (90–140 million years ago, Mya), whereas the origin of the canonical Archaeplastida plastid occurred >1,500 Mya. Therefore, these two events provide independent perspectives on plastid formation on vastly different timescales. Here we generated the complete chromatophore genome sequence from P . longichromatophora (979,356 bp, GC-content = 38.8%, 915 predicted genes) and P . micropora NZ27 (977,190 bp, GC-content = 39.9%, 911 predicted genes) and compared these data to that from existing chromatophore genomes. Our analysis suggests that when a basal split occurred among photosynthetic Paulinella species ca. 60 Mya, only 35% of the ancestral orthologous gene families from the cyanobacterial endosymbiont remained in chromatophore DNA. Following major gene losses during the early stages of endosymbiosis, this process slowed down significantly, resulting in a conserved gene content across extant taxa. Chromatophore genes faced relaxed selection when compared to homologs in free-living alpha-cyanobacteria, likely reflecting the homogeneous intracellular environment of the Paulinella host. Comparison of nucleotide substitution and insertion/deletion events among different P . micropora strains demonstrates that increases in AT-content and genome reduction are ongoing and dynamic processes in chromatophore evolution.