What makes a chloroplast? Reconstructing the establishment of photosynthetic symbioses

Abstract

SummaryEarth is populated by an extraordinary diversity of photosynthetic eukaryotes. Many eukaryotic lineages contain chloroplasts, obtained through the endosymbiosis of a wide range of photosynthetic prokaryotes or eukaryotes, and a wide variety of otherwise nonphotosynthetic species form transient associations with photosynthetic symbionts. Chloroplast lineages are likely to be derived from preexisting transient symbioses, but it is as yet poorly understood what steps are required for the establishment of permanent chloroplasts from photosynthetic symbionts. In the past decade, several species that contain relatively recently acquired chloroplasts, such as the rhizarian Paulinella chromatophora, and non-photosynthetic taxa that maintain photosynthetic symbionts, such as the sacoglossan sea slug Elysia, the ciliate Myrionecta rubra and the dinoflagellate Dinophysis, have emerged as potential model organisms in the study of chloroplast establishment. In this Commentary, we compare recent molecular insights into the maintenance of chloroplasts and photosynthetic symbionts from these lineages, and others that might represent the early stages of chloroplast establishment. We emphasise the importance in the establishment of chloroplasts of gene transfer events that minimise oxidative stress acting on the symbiont. We conclude by assessing whether chloroplast establishment is facilitated in some lineages by a mosaic of genes, derived from multiple symbiotic associations, encoded in the host nucleus.

Functional remodeling of RNA processing in replacement chloroplasts by pathways retained from their predecessors

“…In such a highly divergent chloroplast system, a concerted transcriptediting and polyuridylylation pathway might correct otherwise potentially deleterious mutations in genome sequence, for example, by converting premature termination codons to coding sequence, as in the case of the K. mikimotoi psaA transcript (Dataset S2). If the fast sequence evolution observed in dinoflagellate chloroplasts is a feature of the host, the superimposition of ancestral chloroplast transcript-processing pathways on replacement chloroplasts could be an important step in the replacement, allowing the new lineage to tolerate a host environment that might otherwise prove disadvantageous (2,19).…”

“…organelle | fucoxanthin | haptophyte | poly(U) | alveolate C hloroplasts originate through endosymbiosis, in which a freeliving photosynthetic symbiont is taken up by a eukaryotic host, with processes becoming established within the host to support the biogenesis and maintenance of the symbiont (1,2). It has long been understood that many such endosymbiotic events have occurred across the eukaryotes, giving rise to a diverse array of extant chloroplast lineages (2)(3)(4).…”

“…It has long been understood that many such endosymbiotic events have occurred across the eukaryotes, giving rise to a diverse array of extant chloroplast lineages (2)(3)(4). Genomic and phylogenetic evidence has suggested that several major chloroplast-containing lineages have replaced their original chloroplasts with others derived from a different evolutionary lineage in a process termed "serial endosymbiosis of chloroplasts" (2,5). The best-supported examples of chloroplast replacement are found within the dinoflagellate algae, within which at least three distinct chloroplast replacement events are known to have occurred (2,6,7).…”

“…Genomic and phylogenetic evidence has suggested that several major chloroplast-containing lineages have replaced their original chloroplasts with others derived from a different evolutionary lineage in a process termed "serial endosymbiosis of chloroplasts" (2,5). The best-supported examples of chloroplast replacement are found within the dinoflagellate algae, within which at least three distinct chloroplast replacement events are known to have occurred (2,6,7). Two even more dramatic hypotheses of chloroplast replacement have recently been put forward.…”

“…It is well understood that processes originating in the host play important roles in chloroplast biogenesis and maintenance (2,20,21). This raises the question whether processes established during an earlier chloroplast symbiosis could be retained through serial endosymbiosis and contribute to the function of the replacement chloroplast.…”