Endosymbiotic theory in eukaryotic-cell evolution rests upon a foundation of three cornerstone partners—the plastid (a cyanobacterium), the mitochondrion (a proteobacterium), and its host (an archaeon)—and carries a corollary that, over time, the majority of genes once present in the organelle genomes were relinquished to the chromosomes of the host (endosymbiotic gene transfer). However, notwithstanding eukaryote-specific gene inventions, single-gene phylogenies have never traced eukaryotic genes to three single prokaryotic sources, an issue that hinges crucially upon factors influencing phylogenetic inference. In the age of genomes, single-gene trees, once used to test the predictions of endosymbiotic theory, now spawn new theories that stand to eventually replace endosymbiotic theory with descriptive, gene tree-based variants featuring supernumerary symbionts: prokaryotic partners distinct from the cornerstone trio and whose existence is inferred solely from single-gene trees. We reason that the endosymbiotic ancestors of mitochondria and chloroplasts brought into the eukaryotic—and plant and algal—lineage a genome-sized sample of genes from the proteobacterial and cyanobacterial pangenomes of their respective day and that, even if molecular phylogeny were artifact-free, sampling prokaryotic pangenomes through endosymbiotic gene transfer would lead to inherited chimerism. Recombination in prokaryotes (transduction, conjugation, transformation) differs from recombination in eukaryotes (sex). Prokaryotic recombination leads to pangenomes, and eukaryotic recombination leads to vertical inheritance. Viewed from the perspective of endosymbiotic theory, the critical transition at the eukaryote origin that allowed escape from Muller’s ratchet—the origin of eukaryotic recombination, or sex—might have required surprisingly little evolutionary innovation.

Emiliania huxleyi is a bloom-forming microalga that affects the global sulfur cycle by producing large amounts of dimethylsulfoniopropionate (DMSP) and its volatile metabolic product dimethyl sulfide. Top-down regulation of E. huxleyi blooms has been attributed to viruses and grazers; however, the possible involvement of algicidal bacteria in bloom demise has remained elusive. We demonstrate that a Roseobacter strain, Sulfitobacter D7, that we isolated from a North Atlantic E. huxleyi bloom, exhibited algicidal effects against E. huxleyi upon coculturing. Both the alga and the bacterium were found to co-occur during a natural E. huxleyi bloom, therefore establishing this host-pathogen system as an attractive, ecologically relevant model for studying algal-bacterial interactions in the oceans. During interaction, Sulfitobacter D7 consumed and metabolized algal DMSP to produce high amounts of methanethiol, an alternative product of DMSP catabolism. We revealed a unique strain-specific response, in which E. huxleyi strains that exuded higher amounts of DMSP were more susceptible to Sulfitobacter D7 infection. Intriguingly, exogenous application of DMSP enhanced bacterial virulence and induced susceptibility in an algal strain typically resistant to the bacterial pathogen. This enhanced virulence was highly specific to DMSP compared to addition of propionate and glycerol which had no effect on bacterial virulence. We propose a novel function for DMSP, in addition to its central role in mutualistic interactions among marine organisms, as a mediator of bacterial virulence that may regulate E. huxleyi blooms.

The literature harbors many claims for lateral gene transfer (LGT) from prokaryotes to eukaryotes. Such claims are typically founded in analyses of genome sequences. It is undisputed that many genes entered the eukaryotic lineage via the origin of mitochondria and the origin of plastids. Claims for lineage-specific LGT to eukaryotes outside the context of organelle origins and claims of continuous LGT to eukaryotic lineages are more problematic. If eukaryotes acquire genes from prokaryotes continuously during evolution, then sequenced eukaryote genomes should harbor evidence for recent LGT, like prokaryotic genomes do. Here we devise an approach to investigate 30,358 eukaryotic sequences in the context of 1,035,375 prokaryotic homologs among 2585 phylogenetic trees containing homologs from prokaryotes and eukaryotes. Prokaryote genomes reflect a continuous process of gene acquisition and inheritance, with abundant recent acquisitions showing 80–100 % amino acid sequence identity to their phylogenetic sister-group homologs from other phyla. By contrast, eukaryote genomes show no evidence for either continuous or recent gene acquisitions from prokaryotes. We find that, in general, genes in eukaryotic genomes that share ≥70 % amino acid identity to prokaryotic homologs are genome-specific; that is, they are not found outside individual genome assemblies. Our analyses indicate that eukaryotes do not acquire genes through continual LGT like prokaryotes do. We propose a 70 % rule: Coding sequences in eukaryotic genomes that share more than 70 % amino acid sequence identity to prokaryotic homologs are most likely assembly or annotation artifacts. The findings further uncover that the role of differential loss in eukaryote genome evolution has been vastly underestimated.

Background: Xylem, the most abundant tissue on Earth, is responsible for lateral growth in plants. Typical xylem has a radial system composed of ray parenchyma cells and an axial system of fusiform cells. In most angiosperms, fusiform cells comprise vessel elements for water transportation and libriform fibers for mechanical support, while both functions are performed by tracheids in other vascular plants such as gymnosperms. Little is known about the developmental programs and evolutionary relationships of these xylem cell types.Results: Through both single-cell and laser capture microdissection transcriptomic profiling, we determine the developmental lineages of ray and fusiform cells in stem-differentiating xylem across four divergent woody angiosperms. Based on cross-species analyses of single-cell clusters and overlapping trajectories, we reveal highly conserved ray, yet variable fusiform, lineages across angiosperms. Core eudicotsPopulus trichocarpaandEucalyptus grandisshare nearly identical fusiform lineages, whereas the more basal angiospermLiriodendron chinensehas a fusiform lineage distinct from that in core eudicots. The tracheids in the basal eudicotTrochodendron aralioides, an evolutionarily reversed trait, exhibit strong transcriptomic similarity to vessel elements rather than libriform fibers.Conclusions: This evo-devo framework provides a comprehensive understanding of the formation of xylem cell lineages across multiple plant species spanning over a hundred million years of evolutionary history.