Eukaryogenesis, a syntrophy affair

Abstract

Eukaryotes evolved from a symbiosis involving alphaproteobacteria and archaea phylogenetically nested within the Asgard clade. Two recent studies explore the metabolic capabilities of Asgard lineages, supporting refined symbiotic metabolic interactions that might have operated at the dawn of eukaryogenesis.

Figure 1. Metabolic symbiosis at the origin of eukaryotes.

Current phylogenomic evidence supports symbiotic models for the origin of the eukaryotic cell. Eukaryotic genomes are mosaics containing a substantial number of genes (~1,000) of archaeal and bacterial ancestry that can now be traced to specific lineages^,,. This information supports the idea that eukaryotes evolved from a symbiosis between a member of the recently described Asgard archaea more closely related (so far) to the Heimdallarchaeota and, at least, the facultatively aerobic alphaproteobacterium that gave rise to the mitochondrion. Comparative analyses of the Asgard archaeal metabolic potential allow Spang et al. and Bulzu et al. to conclude that Asgard archaea were primarily organoheterotrophic organisms that can produce and consume hydrogen. Some Heimdallarchaeota also gained the capability to use oxygen and nitrate as final electron acceptors by horizontal gene transfer in a later stage. Based on Asgard archaeal metabolic reconstruction and ecological considerations, Spang et al. propose the ‘reverse flow model’. This refined symbiogenetic model for the origin of eukaryotes invokes a metabolic symbiosis, or syntrophy, mediated by hydrogen or electron transfer between archaea and bacteria. However, unlike the original hydrogen and syntrophy hypotheses, which proposed interspecies hydrogen transfer from the bacterial to the archaeal symbiont, the ‘reverse flow model’ involves electron or hydrogen flow from the archaeal to the bacterial symbiont. This eukaryogenetic syntrophy likely established in anoxic or microoxic environments^,. Although the model specifically involves one archaeon and one bacterium, Spang et al. leave open the possibility that symbiotic interactions with other prokaryotes might have intervened, in consonance with recent proposals for serial symbioses.