Endosymbiotic origin and differential loss of eukaryotic genes

Abstract

Chloroplasts arose from cyanobacteria, mitochondria arose from proteobacteria. Both organelles have conserved their prokaryotic biochemistry, but their genomes are reduced, and most organelle proteins are encoded in the nucleus. Endosymbiotic theory posits that bacterial genes in eukaryotic genomes entered the eukaryotic lineage via organelle ancestors. It predicts episodic influx of prokaryotic genes into the eukaryotic lineage, with acquisition corresponding to endosymbiotic events. Eukaryotic genome sequences, however, increasingly implicate lateral gene transfer, both from prokaryotes to eukaryotes and among eukaryotes, as a source of gene content variation in eukaryotic genomes, which predicts continuous, lineage-specific acquisition of prokaryotic genes in divergent eukaryotic groups. Here we discriminate between these two alternatives by clustering and phylogenetic analysis of eukaryotic gene families having prokaryotic homologues. Our results indicate (1) that gene transfer from bacteria to eukaryotes is episodic, as revealed by gene distributions, and coincides with major evolutionary transitions at the origin of chloroplasts and mitochondria; (2) that gene inheritance in eukaryotes is vertical, as revealed by extensive topological comparison, sparse gene distributions stemming from differential loss; and (3) that continuous, lineage-specific lateral gene transfer, although it sometimes occurs, does not contribute to long-term gene content evolution in eukaryotic genomes.

Early Microbial Evolution: The Age of Anaerobes

“…We emphasize that the new trees are classifying the cytosolic ribosome of eukaryotes, not the phylogenetic position of eukaryotes as a whole, which is a more difficult undertaking. The vast majority of eukaryotic genes that have prokaryotic homologs (a condition necessary for classification of eukaryotes relative to prokaryotes) come from bacteria (Gupta 1998;Esser et al 2004;Timmis et al 2004;Cotton and McInerney 2010;Ku et al 2015). That is particularly true in the plant lineage (Martin et al 2002;Ku et al 2015).…”

“…The vast majority of eukaryotic genes that have prokaryotic homologs (a condition necessary for classification of eukaryotes relative to prokaryotes) come from bacteria (Gupta 1998;Esser et al 2004;Timmis et al 2004;Cotton and McInerney 2010;Ku et al 2015). That is particularly true in the plant lineage (Martin et al 2002;Ku et al 2015). Until methods emerge that permit eukaryotes to be classified on the basis of all genes, we will have to be content with classifications based on ribosomes, keeping in mind that eukaryotes have either one set of ribosomes (lineages with hydrogenosomes or mitosomes) (Embley et al 2003), two sets (lineages with respiring mitochondria), three sets ( plants), or four sets (complex algae) (Maier et al 2013) of evolutionarily distinct ribosomes operating simultaneously, because of endosymbiosis (Zimorski et al 2014).…”

“…Until methods emerge that permit eukaryotes to be classified on the basis of all genes, we will have to be content with classifications based on ribosomes, keeping in mind that eukaryotes have either one set of ribosomes (lineages with hydrogenosomes or mitosomes) (Embley et al 2003), two sets (lineages with respiring mitochondria), three sets ( plants), or four sets (complex algae) (Maier et al 2013) of evolutionarily distinct ribosomes operating simultaneously, because of endosymbiosis (Zimorski et al 2014). Methods to investigate the evolution of all genes in eukaryote genomes are emerging, and the data indicate endosymbiotic origins of eukaryotic genes (Ku et al 2015), hence, of eukaryote cells, whereby the formal classification issue remains unresolved.…”

“…Oxygen provides a roughly sixfold increase in the amount of ATP per glucose that eukaryotes with aerobic respiration in mitochondria-right at maximally 30 ATP per glucose in mammals (Rich 2013)-obtain relative to eukaryotic anaerobes, which glean 4 -5 ATP per glucose (Müller et al 2012). But if oxygen respiration were the key to eukaryote complexity, Escherichia coli and other respiring prokaryotes would have become complex for the same reasons, which clearly did not happen, meaning that O 2 was not the key to eukaryote complexity, while mitochondria more probably were Ku et al 2015;Lane 2015).…”

“…Both evolutionary processes drive microbial diversity, but the two do not strictly coevolve over the fullness of geological time. This is seen in the assortment of bacterial photosynthesis with three kinds of CO 2 fixation pathways (Hohmann-Marriott and Blankenship 2011): the variation and the patchy distribution of sulfur reduction across microbial lineages (Pereira et al 2011), the evolutionary transition from methanogenesis to aerotolerant heterotrophy in the halophiles (Nelson-Sathi et al 2012), or in the association of archaeal ribosomes with bacterial energy metabolism in eukaryotes (Ku et al 2015).…”