Gene flow and biological conflict systems in the origin and evolution of eukaryotes

Abstract

The endosymbiotic origin of eukaryotes brought together two disparate genomes in the cell. Additionally, eukaryotic natural history has included other endosymbiotic events, phagotrophic consumption of organisms, and intimate interactions with viruses and endoparasites. These phenomena facilitated large-scale lateral gene transfer and biological conflicts. We synthesize information from nearly two decades of genomics to illustrate how the interplay between lateral gene transfer and biological conflicts has impacted the emergence of new adaptations in eukaryotes. Using apicomplexans as example, we illustrate how lateral transfer from animals has contributed to unique parasite-host interfaces comprised of adhesion- and O-linked glycosylation-related domains. Adaptations, emerging due to intense selection for diversity in the molecular participants in organismal and genomic conflicts, being dispersed by lateral transfer, were subsequently exapted for eukaryote-specific innovations. We illustrate this using examples relating to eukaryotic chromatin, RNAi and RNA-processing systems, signaling pathways, apoptosis and immunity. We highlight the major contributions from catalytic domains of bacterial toxin systems to the origin of signaling enzymes (e.g., ADP-ribosylation and small molecule messenger synthesis), mutagenic enzymes for immune receptor diversification and RNA-processing. Similarly, we discuss contributions of bacterial antibiotic/siderophore synthesis systems and intra-genomic and intra-cellular selfish elements (e.g., restriction-modification, mobile elements and lysogenic phages) in the emergence of chromatin remodeling/modifying enzymes and RNA-based regulation. We develop the concept that biological conflict systems served as evolutionary "nurseries" for innovations in the protein world, which were delivered to eukaryotes via lateral gene flow to spur key evolutionary innovations all the way from nucleogenesis to lineage-specific adaptations.

Keywords: RNAi; antibiotics; biological conflict; endosymbiosis; immunity proteins; restriction-modfication; selfish elements; toxins.

Figure 1

Animal domains and animal-type O-glycosylation systems in apicomplexa. (A) Domain architectures of apicomplexan proteins containing adhesion domains of animal origin. Proteins are labeled by their gene names/common names and species abbreviation separated by an underscore, and are grouped based on their conservation in apicomplexans. If a domain architecture is present in more than one distinct apicomplexan lineage, the additional lineages are shown in brackets. Domains of animal origin are marked with an asterisk above the domain. If a domain is present in multiple copies in a protein, only one (the first) instance of it is labeled with an asterisk. Domains not present in all orthologs of a protein are enclosed in square brackets. Standard abbreviations are used for domains. Species abbreviations are as follows: Cpar: Cryptosporidium parvum, Pl: Plasmodium, Pfal: Plasmodium falciparum, Th: Theileria, Tgon: Toxoplasma gondii. (B) Protein O-linked glycosylation pathways of animal provenance in apicomplexans. Gene names of enzymes involved in these pathways are shown to the right of the enzyme, along with examples of orthologous proteins from animals. The reconstructed oligosaccharide chain is represented using abbreviations for various sugars and functional groups. Speculative parts are marked with a “?”. GalNAc: N-acetylgalactosamine, GlcNAc: N-acetylglucosamine, X? indicates an uncharacterized sugar added by the LPS glycosyltransferase. Enzymes of animal origin are marked with an asterisk. Species abbreviations are as in (A).

Figure 2

Domain architectures of effectors deployed by endosymbiotic/parasitic bacteria illustrating certain common functional strategies. Proteins are labeled by their gene names, species abbreviations and genbank index (GI) numbers separated by underscores. Non-standard domain names and expansion of species abbreviations are given in the key below the figure. Additionally, Amoebophilus prodomain 1 (APD1) and Amoebophilus prodomain 2 (APD2) are Amoebophilus-specific N-terminal domains that are present immediately downstream of a signal peptide and a lipobox. These domains are likely to help in the specific localization and/or clustering of effectors from this organism.

Figure 3

Evolutionary relationships of various families of enzymes illustrating the origin of eukaryotic versions within radiations of systems involved in inter- and intra-genomic conflicts. Reconstructed phylogenetic trees are shown for (A) The bacterial radiation of the SWI2/SNF2 ATPases. (B) MORC-like ATPases and (C) The Double-psi beta barrel containing RNA polymerases. Certain clades with multiple families such as the eukaryotic SWI2/SNF2 ATPases, the Topoisomerase ATPase subunits, the cellular DDRP and eukaryotic RdRPs are collapsed into triangles for clarity. Illustrative domain architectures or gene neighborhoods are shown next to the leaf. Genes in gene neighborhoods are shown in block arrows with the arrow head pointing from the 5′ to the 3′ gene. Proteins and gene neighborhoods are labeled by the gene name and species name separated by underscores. The trees represent only the overall topology because they were obtained by a combination of conventional phylogenetic tree construction and structure-based determination of higher-order relationships.

Figure 4

A tree of the eukaryotic relationships illustrating the points of recruitment in eukaryotes in different functional systems of various domains from different biological conflict systems. With a eukaryotic tree as reference, the source and reconstructed point of transfer of various domains recruited from different conflict systems and symbiogenic events are shown. The transfers are shown as dashed arrows with the arrow head pointing to the ancestor in which the transfer is proposed to have taken place. The dashed lines are labeled either with a single gene or a set of genes enclosed in a box. The conflict systems are shown in the key at the bottom left.