New Organelles by Gene Duplication in a Biophysical Model of Eukaryote Endomembrane Evolution

Abstract

Extant eukaryotic cells have a dynamic traffic network that consists of diverse membrane-bound organelles exchanging matter via vesicles. This endomembrane system arose and diversified during a period characterized by massive expansions of gene families involved in trafficking after the acquisition of a mitochondrial endosymbiont by a prokaryotic host cell >1.8 billion years ago. Here we investigate the mechanistic link between gene duplication and the emergence of new nonendosymbiotic organelles, using a minimal biophysical model of traffic. Our model incorporates membrane-bound compartments, coat proteins and adaptors that drive vesicles to bud and segregate cargo from source compartments, and SNARE proteins and associated factors that cause vesicles to fuse into specific destination compartments. In simulations, arbitrary numbers of compartments with heterogeneous initial compositions segregate into a few compositionally distinct subsets that we term organelles. The global structure of the traffic system (i.e., the number, composition, and connectivity of organelles) is determined completely by local molecular interactions. On evolutionary timescales, duplication of the budding and fusion machinery followed by loss of cross-interactions leads to the emergence of new organelles, with increased molecular specificity being necessary to maintain larger organellar repertoires. These results clarify potential modes of early eukaryotic evolution as well as more recent eukaryotic diversification.

Missing Pieces of an Ancient Puzzle: Evolution of the Eukaryotic Membrane-Trafficking System

“…The strongest evidence in favor of this mechanism was the observation that, whereas many of the organelle-specific subfamilies of SNAREs, Rabs, and Adaptins had duplicated pre-LECA, a few of the paralogs associated with endocytic organelles had emerged in lineage-specific fashion independently, but with parallel functions implying a general process for organelle evolution acting on the system . Recent computer simulations have confirmed that such a mechanism could indeed produce an organelle-generating mechanism based on purely theoretical calculations of protein -protein interactions and the evolution of specificity within paralogs (Ramadas and Thattai 2013).…”

Ancient dynamin segments capture early stages of host–mitochondrial integration

“…eukaryote evolution | mitochondria | vesicles | dynamin | FtsZ E ukaryotes arose through the acquisition of mitochondria by an archaeal host cell about 2 billion y ago (1,2), a watershed moment in the evolution of the modern compartmentalized cell plan (3). A second transformative endosymbiotic event, the acquisition of a cyanobacterium by a eukaryotic host to form chloroplasts, gave rise to the photosynthetic eukaryotic lineages (4).…”

Wine glasses and hourglasses: Non-adaptive complexity of vesicle traffic in microbial eukaryotes

“…Models that focus on size distributions allow for a continuum of structures from transport vesicles to large compartments, and account for fission and fusion of all such structures [26]. Many models focus on compartments and the complex rules of molecular specificity, but do not treat transport vesicles explicitly and do not account for inter-vesicle fusion [25], [28], [29]. In such models, compartment compositions are specified by the concentrations of various molecules, and vesicle traffic is represented by a series of ordinary differential equations.…”

“…In this context, mathematical modeling has proved useful in connecting basic molecular events, such as budding and fusion, to dynamic processes, such as cargo transport, and finally to the compartmental compositions of the endomembrane system [25], [26], [27], [28], [29], [30]. These models require the specification of a large number of parameters.…”