Amoeba Genome Reveals Dominant Host Contribution to Plastid Endosymbiosis

Abstract

Eukaryotic photosynthetic organelles, plastids, are the powerhouses of many aquatic and terrestrial ecosystems. The canonical plastid in algae and plants originated >1 billion years ago and therefore offers limited insights into the initial stages of organelle evolution. To address this issue, we focus here on the photosynthetic amoeba Paulinella micropora strain KR01 (hereafter, KR01) that underwent a more recent (ca. 124 Mya) primary endosymbiosis, resulting in a photosynthetic organelle termed the chromatophore. Analysis of genomic and transcriptomic data resulted in a high-quality draft assembly of size 707 Mbp and 32,361 predicted gene models. A total of 291 chromatophore targeted proteins were predicted in silico, 206 of which comprise the ancestral organelle proteome in photosynthetic Paulinella species with functions, among others, in nucleotide metabolism and oxidative stress response. Gene co-expression analysis identified networks containing known high light stress response genes as well as a variety of genes of unknown function (“dark” genes). We characterized diurnally rhythmic genes in this species and found that over 51% are dark. It was recently hypothesized that large double-stranded DNA viruses may have driven gene transfer to the nucleus in Paulinella and facilitated endosymbiosis. Our analyses do not support this idea, but rather suggest that these viruses in the KR01 and closely related P. micropora MYN1 genomes resulted from a more recent invasion.

Why is primary endosymbiosis so rare?

“…c . 98 derived through HGT; Lhee et al ., 2021a), there is strong selection for host‐centered solutions to chromatophore maintenance and integration. The origin of novel genes and genetic elements plays a key role in endosymbiont maintenance, with > 51% of the predicted diurnally (day/night) rhythmic genes in KR01 lacking an annotation.…”

“…Despite an approximately two‐thirds reduction in chromatophore genome size, only c . 50 endosymbiotic gene transfer (EGT) candidates have been found in the nuclear genome of Paulinella species (Nowack et al ., 2016, Lhee et al ., 2021a). By contrast, c .…”

“…Research on artificial endosymbiosis highlights the importance of several key aspects of biotic associations: compartmentalization, synchronized growth and cell division, processing of genetic and other types of information and, importantly, energy transduction and adaptability (Yewdall et al ., 2018). In the case of Paulinella , these aspects have been accommodated with clear evidence of synchronized cell division of the chromatophore compartment and host cell (Hoogenraad, 1927; Melkonian & Mollenhauer, 2005), the finding that the ancestral pool of chromatophore‐targeted long proteins are involved in genetic information processing (Lhee et al ., 2021a), and the generation of energy in the chromatophore and its transfer to the amoeba (Sato et al ., 2020), which is no longer capable of phagotrophic growth (Bhattacharya et al ., 2012).…”

“…The second plastid primary endosymbiosis occurred more recently (c. 120 million yr ago) in the rhizarian amoeba Paulinella. This event involved a heterotrophic ancestor of Paulinella and an acyanobacterial prey, with the latter evolving into a photosynthetic organelle termed the 'chromatophore' (Lauterborn et al, 1895;Melkonian & Mollenhauer, 2005;Lhee et al, 2021a). Given the incomplete and fragmented genomic evidence regarding early events in plastid evolution that is available from the Archaeplastida (Gabr et al, 2020), there is a need for new models from nature or the application of synthetic biology approaches to understand this process (e.g.…”

A bipartite chromatophore targeting peptide and N-terminal processing of proteins in the Paulinella chromatophore

“…CC-BY-NC-ND 4.0 International license perpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for this this version posted September 21, 2021. ; https://doi.org/10.1101/2021.09.19.461000 doi: bioRxiv preprint 4 high degree of sequence conservation between chromatophore-targeted proteins including those in the photosynthetic sister species P. micropora (Singer et al, 2017;Lhee et al, 2021).…”