The origin of phagocytosis in Earth history

Abstract

Phagocytosis, or 'cell eating', is a eukaryote-specific process where particulate matter is engulfed via invaginations of the plasma membrane. The origin of phagocytosis has been central to discussions on eukaryogenesis for decades-, where it is argued as being either a prerequisite for, or consequence of, the acquisition of the ancestral mitochondrion. Recently, genomic and cytological evidence has increasingly supported the view that the pre-mitochondrial host cell-a bona fide archaeon branching within the 'Asgard' archaea-was incapable of phagocytosis and used alternative mechanisms to incorporate the alphaproteobacterial ancestor of mitochondria. Indeed, the diversity and variability of proteins associated with phagosomes across the eukaryotic tree suggest that phagocytosis, as seen in a variety of extant eukaryotes, may have evolved independently several times within the eukaryotic crown-group. Since phagocytosis is critical to the functioning of modern marine food webs (without it, there would be no microbial loop or animal life), multiple late origins of phagocytosis could help explain why many of the ecological and evolutionary innovations of the Neoproterozoic Era (e.g. the advent of eukaryotic biomineralization, the 'Rise of Algae' and the origin of animals) happened when they did.

Keywords: Asgard archaea; Neoproterozoic; Rise of Algae; eukaryogenesis; eukaryovory; phagocytosis.

Figure 1.

Timeline of palaeontological, organic geochemical and molecular clock evidence regarding the age of crown-group eukaryotes and the earliest evidence for eukaryotic predation. The Sturtian (717–660 Ma) and the Marinoan (640–635 Ma) glaciations are each shown as vertical grey bars. For the molecular clock estimates, the bars display the highest credibility intervals (95%) for the age of LECA, with the diamonds indicating the mean age estimates from each analysis. For Berney & Pawlowski [48], these values were obtained from fig. 1 (node 1). For Chernikova et al. [49], these values were obtained from the first set of values reported in table 2, where Bangiomorpha—then dated to 1.2 Ga—was used a fossil calibration constraint. The values from Parfrey et al. [50] come from fig. 2, listed in table S1 under analysis ‘a’, while the values from Betts et al. [25] come from fig. 3. The range reported for Eme et al. [51] covers a variety of analyses exploring the impact of using different tree topologies, fossil calibration constraints and substitution models on estimating the age of LECA—hence no reported mean estimate for this overall range. Given that modern type phagocytosis may not have facilitated the capture of the ancestral plastid [1,26], Bangiomorpha may or may not serve as indirect evidence for bacterivory—hence the question mark in the key. While the lower Shaler Supergroup microfossils and the vase-shaped microfossils both preserve perforations likely sourced from eukaryotic predators, it is unclear if these punctures resulted from protoplast feeding, myzocytosis, or some other form of predatory piercing. While the apatitic scale microfossils are reasonably interpreted as having been adapted to deter predation, the relatively indirect nature of this evidence, as discussed in the main text, is reflected by the question mark in the key.