Tightly Constrained Genome Reduction and Relaxation of Purifying Selection during Secondary Plastid Endosymbiosis

Abstract

Endosymbiosis, the establishment of a former free-living prokaryotic or eukaryotic cell as an organelle inside a host cell, can dramatically alter the genomic architecture of the endosymbiont. Plastids or chloroplasts, the light-harvesting organelle of photosynthetic eukaryotes, are excellent models to study this phenomenon because plastid origin has occurred multiple times in evolution. Here, we investigate the genomic signature of molecular processes acting through secondary plastid endosymbiosis—the origination of a new plastid from a free-living eukaryotic alga. We used phylogenetic comparative methods to study gene loss and changes in selective regimes on plastid genomes, focusing on green algae that have given rise to three independent lineages with secondary plastids (euglenophytes, chlorarachniophytes, and Lepidodinium). Our results show an overall increase in gene loss associated with secondary endosymbiosis, but this loss is tightly constrained by retention of genes essential for plastid function. The data show that secondary plastids have experienced temporary relaxation of purifying selection during secondary endosymbiosis. However, this process is tightly constrained, with selection relaxed only relative to the background in primary plastids. Purifying selection remains strong in absolute terms even during the endosymbiosis events. Selection intensity rebounds to pre-endosymbiosis levels following endosymbiosis events, demonstrating the changes in selection efficiency during different origin phases of secondary plastids. Independent endosymbiosis events in the euglenophytes, chlorarachniophytes, and Lepidodinium differ in their degree of relaxation of selection, highlighting the different evolutionary contexts of these events. This study reveals the selection-drift interplay during secondary endosymbiosis, and evolutionary parallels during organellogenesis.

Human Follicular Mites: Ectoparasites Becoming Symbionts

“…Purifying selection contributes to genome reductions in prokaryotic species ( Williams and Wernegreen 2012 ; Albalat and Cañestro 2016 ; Valadez-Cano et al 2017 ); it is observed in endosymbionts that confer an advantage to their host and in organellogenesis ( Uthanumallian et al 2022 ). No endosymbiotic eukaryotic animals have been identified to date.…”

In the spotlight, losing IR region: insights from euglenophytes challenge the importance of inverted repeats in the genomes of secondary plastids

“…However, these analyses took only the data from primary plastids into account, leaving the diverse secondary plastid-bearing taxa understudied in this regard. Thus, given that there is a growing body of evidence for dissimilarity of evolutionary dynamics and selection intensity between primary and complex plastids (Uthanumallian et al, 2021), the missing piece of the puzzle may be tremendously important. To fill this information void, we have undertaken an analysis of the sequence evolution rate in ribosomal subunit genes, which form the bulk of the length of the plastid inverted repeats, as well as in protein-coding genes encoded outside of the IRs in the IR-bearing and IR-less plastomes of Euglenophyta.…”

Nuclear genome of a pedinophyte pinpoints genomic innovation and streamlining in the green algae

“…The pedinophyte nuclear genome represents a missing link to examine the evolution of the Chlorophyta. The coding regions show strong codon and GC biases, which are also observed in their compact, intron‐lacking chloroplast genomes (Marin, 2012; Jackson et al ., 2018; Uthanumallian et al ., 2021), indicating that they are under comparatively strong selection. The pedinophyte lineage also appears to have experienced considerable loss of homologous gene groups.…”