Chlamydia, cyanobiont, or host: who was on top in the ménage à trois?

•Endosymbiotic origin of plastids: interaction of host cell, cyanobacterium, and Chlamydia-like bacterium.•Cyanobacterial ancestor and Chlamydia-like bacterium simultaneously entered the host cell.•Cohabitation of cyanobiont and Chlamydia-like parasite enabled evolution of the endosymbiotic plastid.•Secreted chlamydial effectors enabled the metabolic integration of the plastid and the host cell.

The endosymbiont hypothesis proposes that photosynthate from the cyanobiont was exported to the cytosol of the eukaryote host and polymerized from ADP-glucose into glycogen. Chlamydia-like pathogens are the second major source of foreign genes in Archaeplastida, suggesting that these obligate intracellular pathogens had a significant role during the establishment of endosymbiosis, likely through facilitating the metabolic integration between the endosymbiont and the eukaryotic host. In this opinion article, we propose that a hexose phosphate transporter of chlamydial origin was the first transporter responsible for exporting photosynthate out of the cyanobiont. This connection pre-dates the recruitment of the host-derived carbon translocators on the plastid inner membranes of green and red algae, land plants, and photosynthetic organisms of higher order endosymbiotic origin.