Intracellular signaling in proto-eukaryotes evolves to alleviate regulatory conflicts of endosymbiosis

PLoS Comput Biol. 2024 Feb 9;20(2):e1011860. doi: 10.1371/journal.pcbi.1011860. eCollection 2024 Feb.

Abstract

The complex eukaryotic cell resulted from a merger between simpler prokaryotic cells, yet the role of the mitochondrial endosymbiosis with respect to other eukaryotic innovations has remained under dispute. To investigate how the regulatory challenges associated with the endosymbiotic state impacted genome and network evolution during eukaryogenesis, we study a constructive computational model where two simple cells are forced into an obligate endosymbiosis. Across multiple in silico evolutionary replicates, we observe the emergence of different mechanisms for the coordination of host and symbiont cell cycles, stabilizing the endosymbiotic relationship. In most cases, coordination is implicit, without signaling between host and symbiont. Signaling only evolves when there is leakage of regulatory products between host and symbiont. In the fittest evolutionary replicate, the host has taken full control of the symbiont cell cycle through signaling, mimicking the regulatory dominance of the nucleus over the mitochondrion that evolved during eukaryogenesis.

MeSH terms

  • Biological Evolution*
  • Eukaryota / genetics
  • Eukaryotic Cells / metabolism
  • Phylogeny
  • Prokaryotic Cells / metabolism
  • Symbiosis* / genetics

Grants and funding

This work was supported by The Netherlands Organisation for Scientific Research (NWO-Vici 016.160.638 to B.S.): https://www.nwo.nl/. The funder did not play any role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.