De novo organelle biogenesis in the cyanobacterium TDX16 released from the green algaHaematococcus pluvialis

Abstract

AbstractIt is believed that eukaryotes arise from prokaryotes, which means that organelles can form in the latter. Such events, however, had not been observed previously. Here, we report the biogenesis of organelles in the endosymbiotic cyanobacterium TDX16 that escaped from its senescent/necrotic host cell of green algaHaematococcus pluvialis. In brief, organelle biogenesis in TDX16 initiated with cytoplasm compartmentalization, followed by de-compartmentalization, DNA allocation, and re-compartmentalization, as such two composite organelles-the primitive chloroplast and primitive nucleus sequestering minor and major fractions of cellular DNA respectively were formed. Thereafter, the eukaryotic cytoplasmic matrix was built up from the matrix extruded from the primitive nucleus; mitochondria were assembled in and segregated from the primitive chloroplast, whereby the primitive nucleus and primitive chloroplast matured into nucleus and chloroplast respectively; while most mitochondria turned into double-membraned vacuoles after matrix degradation. Results of pigment analyses, 16S rRNA and genome sequencing revealed that TDX16 is a phycocyanin-containing cyanobacterium resemblingChroococcidiopsis thermalis, which had acquired 9,017,401bp DNAs with 10301 genes form its host. Therefore, organelle biogenesis in TDX16 was achieved by hybridizing the acquired eukaryotic DNAs with its own ones and expressing the hybrid genome.Organelle biogenesis in TDX16 results in its transition into a new eukaryotic alga TDX16-DE, which provides a reference to re-understand the development, structure, function and association of organelles in eukaryotes and the reasons behind them, and has implications on other sections of biology, particularly cancer biology and evolutionary biology: (1) the formation and maturation of the small organelle-less nascent cancer cells share striking similarities with TDX16 development and transition, so, it is most likely that cancer cells arise from bacteria; (2) organelle biogenesis in TDX16 uncovers a way of new organelle and new single-celled eukaryote formation, and in light of which, the ancestral organelles were likely formed in rather than transformed form the endosymbiotic prokaryotes that had acquired their hosts’ DNAs.