Why is primary endosymbiosis so rare?

Abstract

Endosymbiosis is a relationship between two organisms wherein one cell resides inside the other. This affiliation, when stable and beneficial for the 'host' cell, can result in massive genetic innovation with the foremost examples being the evolution of eukaryotic organelles, the mitochondria and plastids. Despite its critical evolutionary role, there is limited knowledge about how endosymbiosis is initially established and how host-endosymbiont biology is integrated. Here, we explore this issue, using as our model the rhizarian amoeba Paulinella, which represents an independent case of primary plastid origin that occurred c. 120 million yr ago. We propose the 'chassis and engine' model that provides a theoretical framework for understanding primary plastid endosymbiosis, potentially explaining why it is so rare.

Keywords: Rhizaria; endosymbiotic gene transfer; genome reduction; organellogenesis; photosynthetic eukaryotes; primary endosymbiosis.

Fig. 1

The history of plastid endosymbiosis in eukaryotes. This is a highly reduced tree that only shows the groups of interest (see also Ponce-Toledo et al., 2019). Primary plastid origin occurred in the ancestors of Archaeplastida and photosynthetic Paulinella (within Rhizaria). Green algal secondary endosymbiosis occurred independently in the chlorarachniophyte (Rhizaria) and Euglenozoa lineages. Red algal secondary endosymbiosis has occurred in the alveolates (e.g. dinoflagellates), stramenopiles, cryptophytes and haptophytes. These taxa are informally referred to as CRASH (i.e. cryptophytes, rhizarians, alveolates, stramenopiles and haptophytes) with phylogenetic evidence existing for the monophyly of SAR (stramenopiles, alveolates and rhizarians) taxa (Bhattacharya & Price, 2020; Fan et al., 2020). Broken lines indicate unclear phylogenetic affiliations that may impact the number of red algal endosymbiosis if some (or all, highly unlikely) of these lineages share a single event. There is a variety of plastid-lacking heterotrophic lineages, not shown here, such as ciliates, telonemids and katablepharids, that are sister to photosynthetic taxa in the CRASH. Multiple tertiary endosymbioses involving green algae, haptophytes and diatoms have occurred in the dinoflagellates that are not shown here (Gross et al., 2012).

Fig. 2

Putative timeline of plastid evolution in Paulinella encompassing both a historical and future perspective based on the chassis and engine model. (a) Heterotrophic Paulinella ingesting cyanobacterial cells likely using filose, feeding pseudopodia as a result of the presence of silica scales on the cell surface (Johnson et al., 1988). DNA from ingested bacterial cells can enter the nucleus and become integrated into the host genome via horizontal gene transfer (HGT). These foreign genes, as well as other novel ‘dark’ genes that evolved in this lineage, enabled the host to maintain the cyanobacteria in food vacuoles for increasingly longer periods of time until the association became permanent. (b) The status of extant photosynthetic Paulinella showing the two chromatophores and current evolutionary processes. (c) Putative future status of photosynthetic Paulinella. The chromatophore will encode only essential genes that cannot be transferred to the host genome because the encoded proteins either are problematic to transport into the chromatophore or require redox regulationwithin the organelle(e.g. co-locationfor redox regulation (CoRR hypothesis); Allen, 2017).The chromatophore may also lose its peptidoglycan layer, as observed in other lineages containing primary plastids (except Glaucophyta). Adaptations will probably increase the Paulinella growth rate and the ability to deal with high light, expanding its environmental niche. (d) The chassis and engine model of plastid endosymbiosis. The approximate size of the chromatophore genome and the number of genes it encodes across Paulinella species are shown inside the engine. Parts of the model where questions remain about the endosymbiosis in Paulinella are shown in red text (for more detail see Box 1). crTP, chromatophore targeting peptide; EGT, endosymbiotic gene transfer; mt, mitochondrion; ROS, reactive oxygen species.