Gene transfers from diverse bacteria compensate for reductive genome evolution in the chromatophore of Paulinella chromatophora

Abstract

Plastids, the photosynthetic organelles, originated >1 billion y ago via the endosymbiosis of a cyanobacterium. The resulting proliferation of primary producers fundamentally changed global ecology. Endosymbiotic gene transfer (EGT) from the intracellular cyanobacterium to the nucleus is widely recognized as a critical factor in the evolution of photosynthetic eukaryotes. The contribution of horizontal gene transfers (HGTs) from other bacteria to plastid establishment remains more controversial. A novel perspective on this issue is provided by the amoeba Paulinella chromatophora, which contains photosynthetic organelles (chromatophores) that are only 60-200 million years old. Chromatophore genome reduction entailed the loss of many biosynthetic pathways including those for numerous amino acids and cofactors. How the host cell compensates for these losses remains unknown, because the presence of bacteria in all available P. chromatophora cultures excluded elucidation of the full metabolic capacity and occurrence of HGT in this species. Here we generated a high-quality transcriptome and draft genome assembly from the first bacteria-free P. chromatophora culture to deduce rules that govern organelle integration into cellular metabolism. Our analyses revealed that nuclear and chromatophore gene inventories provide highly complementary functions. At least 229 nuclear genes were acquired via HGT from various bacteria, of which only 25% putatively arose through EGT from the chromatophore genome. Many HGT-derived bacterial genes encode proteins that fill gaps in critical chromatophore pathways/processes. Our results demonstrate a dominant role for HGT in compensating for organelle genome reduction and suggest that phagotrophy may be a major driver of HGT.endosymbiosis | genome evolution | organellogenesis | horizontal gene transfer | coevolution

Metabolic quirks and the colourful history of the Euglena gracilis secondary plastid

“…Being noted previously (Maruyama et al, 2011;Markunas and Triemer, 2016;Lakey and Triemer, 2017;Ponce-Toledo et al, 2018), it was suggested that these genes were acquired from 'chromophyte' prey or a symbiont by the common ancestor of eukaryovorous and/or phototrophic euglenids. These genes could have originated: from the eukaryovorous ancestor of euglenids, sensu the 'you are what you eat' hypothesis (Doolittle, 1998); from initial stages of endosymbiont integration when the euglenid host was presumably obligatorily mixotrophic (much like Rapaza viridis; Yamaguchi et al, 2012), and such transfers could have compensated for the reductive evolution of the endosymbiont genome, as proposed for the chromatophore of Paulinella (Marin et al, 2005;Nowack et al, 2016); from gene transfers from a cryptic endosymbiont, kleptoplastid or even true plastid putatively present in the euglenophyte ancestor and replaced by the extant organelle, in the 'shopping bag' (Larkum Fig. Cohorts related to chlorarachniophytes, ochrophytes and haptophytes account for over 60 E. gracilis plastid proteins (19% of the algal LGT candidates).…”

Horizontal and endosymbiotic gene transfer in early plastid evolution

“…The chromatophore genome is highly reduced, encoding 867 proteins that represent about one‐third of proteins of its free‐living counterparts (Nowack et al ., ). Similar to the EGTs found in Archaeplastida, P. chromatophora has relocated > 70 chromatophore genes into the nuclear genome (mostly involved in photosynthesis‐related functions) (Nowack et al ., ; Zhang et al ., ). By contrast, these genes represent < 1% of the Paulinella nuclear genome, while in A. thaliana some reports have suggested that the genes of cyanobacterial origin can account for up to 18% of the nuclear genes (Martin et al ., ).…”

Did some red alga‐derived plastids evolve via kleptoplastidy? A hypothesis

“…Burki et al., ). It is possible that the ‘green genes’ were acquired via horizontal gene transfer (HGT) before red algal endosymbiosis, but alternatively they could have reached the host nuclear genome during the establishment of the red plastid (Ku et al., ; see also Nowack et al., ), although at present it is unclear how long the process was and exactly how it proceeded [note that Ku et al . () and Nowack et al .…”