Metabolic connectivity as a driver of host and endosymbiont integration

Abstract

The origin of oxygenic photosynthesis in the Archaeplastida common ancestor was foundational for the evolution of multicellular life. It is very likely that the primary endosymbiosis that explains plastid origin relied initially on the establishment of a metabolic connection between the host cell and captured cyanobacterium. We posit that these connections were derived primarily from existing host-derived components. To test this idea, we used phylogenomic and network analysis to infer the phylogenetic origin and evolutionary history of 37 validated plastid innermost membrane (permeome) metabolite transporters from the model plant Arabidopsis thaliana. Our results show that 57% of these transporter genes are of eukaryotic origin and that the captured cyanobacterium made a relatively minor (albeit important) contribution to the process. We also tested the hypothesis that the bacterium-derived hexose-phosphate transporter UhpC might have been the primordial sugar transporter in the Archaeplastida ancestor. Bioinformatic and protein localization studies demonstrate that this protein in the extremophilic red algae Galdieria sulphuraria and Cyanidioschyzon merolae are plastid targeted. Given this protein is also localized in plastids in the glaucophyte alga Cyanophora paradoxa, we suggest it played a crucial role in early plastid endosymbiosis by connecting the endosymbiont and host carbon storage networks. In summary, our work significantly advances understanding of plastid integration and favors a hostcentric view of endosymbiosis. Under this view, nuclear genes of either eukaryotic or bacterial (noncyanobacterial) origin provided key elements of the toolkit needed for establishing metabolic connections in the primordial Archaeplastida lineage.Arabidopsis thaliana | endosymbiosis | evolution | network analysis | symbiont integration

Horizontal and endosymbiotic gene transfer in early plastid evolution

“…Gene transfers from bacteria other than cyanobionts and their retargeting to the early plastid seem to have been very frequent in both primary photosynthetic lineages, many possibly replacing genes that have been lost from the cyanobiont genome. Nonetheless, the eukaryotic host seems to have been the largest contributor of plastid‐targeted proteins, with most of these involved in plastid maintenance and transport of metabolites, this situation supports the idea that the host drove the early steps of plastid endosymbiosis (Karkar et al ., ).…”

“…For instance, metabolite transporters that originated from the retargeting of host membrane proteins are particularly overrepresented in the plastid envelope (58% of plastid transporters appear to derive from host membrane proteins in Arabidopsis thaliana; Tyra et al, 2007). These findings suggest that the host drove the integration of the cyanobiont by providing the proteins necessary to connect the cyanobiont metabolism with the energy demands of the host ('hostcentric' endosymbiosis model; Karkar et al, 2015).…”

An antimicrobial origin of transit peptides accounts for early endosymbiotic events

“…The physiological conditions that prevailed at the time when the host cell and the endosymbiont started their metabolic integration have been—and still are—a matter of debate . The assumption of a mutual benefit, even if serendipitously experienced, involves specific conditions that led to the persistent internalization of the prokaryote by the host cell. In that respect, it is now widely accepted that, among all α‐proteobacteria branches, the mitochondrial ancestor roots close to Rickettsiaceae that are obligate intracellular pathogens .…”

Biotic interactions as drivers of algal origin and evolution

“…The rarity of primary endosymbiosis has fascinated scientists for many years and is usually attributed to the extensive innovations required for organelle establishment. These include: (1) events that lead to the protection of the nascent endosymbiont from host digestion; (2) tailoring of processes critical for the exchange of metabolites between the endosymbiont and host cell (Facchinelli & Weber, ); (3) the origin of an import system to move cytosolic proteins into the nascent organelle (Schleiff & Becker, ); (4) foreign gene acquisition through HGT and the integration of the HGT‐derived protein products into both host and newly developing organelle pathways (Cavalier‐Smith, ; Karkar et al ., ); and (5) movement of genes from the organelle to the host nucleus to escape Muller's ratchet, that is, the accumulation of mutations in nonrecombining genomes (Felsenstein, ). Processes that would exacerbate the impact of Muller's ratchet and make the relocation of genes from the organelle to the nuclear genome more imperative are the mutagenic effect of damaging reactive oxygen species (ROS) produced as a consequence of photosynthesis in the organelle (van Creveld et al ., ), and as yet unexplained processes associated with greater damage of DNA in organelles than in their aerobic bacterial ancestors (Raven, ).…”