Evolutionary dynamics of the chromatophore genome in three photosynthetic Paulinella species

Abstract

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.

Phytoplankton pangenome reveals extensive prokaryotic horizontal gene transfer of diverse functions

“…In addition to the example shown in Fig. 2A (18)(19)(20). It should be noted that the lack of a large number of HGTs from single donor sources contrasts with the obvious single-donor gene transfers often associated with endosymbiosis and EGT (8,21).…”

Genomic Insights into Plastid Evolution

“…The sequencing of additional chromatophore genomes has provided further insight into the endosymbiont-to-organelle transition in this understudied lineage. Lhee et al. (2019) showed conservation of gene content and genome structure between the chromatophore genomes of a variety of Paulinella species and strains, suggesting that most of the genome reduction (∼65% of the protein coding genes) occurred in the common ancestor of studied Paulinella species before they diverged from one another.…”

Amoeba Genome Reveals Dominant Host Contribution to Plastid Endosymbiosis

“…1 G ). Barring independent crTP evolution, these represent the ancestral set of chromatophore-targeted proteins in photosynthetic Paulinella species that split ∼60 Ma ( Lhee et al. 2019 ).…”

“…However, the chromatophore is resolved in phylogenetic trees as a sister to the entire Synechococcus / Prochlorococcus clade or in a basal position within Synechococcus ( Yoon et al 2006 ; Marin et al 2005 ). Calculation of the number of orthologous gene families (OGFs) in the chromatophore ancestor suggests this number is 2,502 ( Lhee et al. 2019 ).…”