The dispersed archaeal eukaryome and the complex archaeal ancestor of eukaryotes

Abstract

The ancestral set of eukaryotic genes is a chimera composed of genes of archaeal and bacterial origins thanks to the endosymbiosis event that gave rise to the mitochondria and apparently antedated the last common ancestor of the extant eukaryotes. The proto-mitochondrial endosymbiont is confidently identified as an α-proteobacterium. In contrast, the archaeal ancestor of eukaryotes remains elusive, although evidence is accumulating that it could have belonged to a deep lineage within the TACK (Thaumarchaeota, Aigarchaeota, Crenarchaeota, Korarchaeota) superphylum of the Archaea. Recent surveys of archaeal genomes show that the apparent ancestors of several key functional systems of eukaryotes, the components of the archaeal "eukaryome," such as ubiquitin signaling, RNA interference, and actin-based and tubulin-based cytoskeleton structures, are identifiable in different archaeal groups. We suggest that the archaeal ancestor of eukaryotes was a complex form, rooted deeply within the TACK superphylum, that already possessed some quintessential eukaryotic features, in particular, a cytoskeleton, and perhaps was capable of a primitive form of phagocytosis that would facilitate the engulfment of potential symbionts. This putative group of Archaea could have existed for a relatively short time before going extinct or undergoing genome streamlining, resulting in the dispersion of the eukaryome. This scenario might explain the difficulty with the identification of the archaeal ancestor of eukaryotes despite the straightforward detection of apparent ancestors to many signature eukaryotic functional systems.

Figure 1.

A reconstruction of the evolution of archaeal gene complements and the inferred origins of the eukaryome components. The boxes show the approximate maximum-likelihood estimates for the number of genes in extant and reconstructed ancestral genomes according to the color code shown on the right. The reconstruction was performed using the COUNT software (Csurös 2010). The tree topology is from the phylogenetic tree of concatenated ribosomal proteins (Wolf et al. 2012; Yutin et al. 2012). The inferred origins of some key eukaryotic genes and functional systems are indicated by arrows (see text); S30, L25, and L13 are ribosomal proteins. (From Wolf et al. 2012; modified, with permission, from the author.)

Figure 2.

The patterns of the evolutionary relationships between Archaea and eukaryotes. A total of 8440 eukaryotic protein families derived from the KOD (cluster of eukaryotic orthologous domains) data set (Yutin et al. 2008) were used for a PSI-BLAST search (Altschul et al. 1997) against 113 archaeal and 1285 bacterial genomes. Then, 5365 of the 8440 families that had prokaryotic hits with an e-value better than 0.01 were subjected to the detailed phyletic analysis. Each number in a cell represents the number of eukaryotic protein families that had putative homologs (hits) in the given number of bacterial or archaeal taxonomic groups. Prokaryotic genomes were grouped into taxonomic groups as follows (numbers in parentheses represent the numbers of the genomes in the respective group). Bacteria: Alpha(proteobacteria) (143); Gamma(proteobacteria) (292); Beta(proteobacteria) (98); Delta(proteobacteria) (41); Nitrospirae (2); Deferribacteres (4); Epsilon (36); Acidobacteria (5); Elusimicrobia (2); Spirochaetes (28); Planctomycetes (5); Chlamydiae_Verrucomicrobia (22); Bacteroidetes_Chlorobi (64); Gemmatimonadetes (1); Fibrobacteres (1); Deinococci (13); Actinobacteria (132); Chloroflexi (16); Cyanobacteria (40); Fusobacteria (5); Mollicutes (36); Firmicutes (272); Synergistetes (2); Coprothermobact (1); Dictyoglomi (2); Thermotogae (11); Aquificae (9); unclassified_Cloacamonas (1); and Chrysiogenetes (1). Archaea: Methanomicrobia (16); Halobacteria (14); Archaeoglobi (4); Thermoplasmata (4); Methanobacteria (8); Methanococci (14); Methanopyri (1); Thermococci (9); Nanoarchaeota (1); Sulfolobales (13); Desulfurococcales (10); Thermoproteales (10); Thaumarchaeota (2); Korarchaeota (1); Caldiarchaeum (1); and “small Euryarchaeota” (5). “Small Euryarchaeota” consist of Candidatus Micrarchaeum acidiphilum ARMAN_2, Candidatus Parvarchaeum acidiphilum ARMAN_4, Candidatus Parvarchaeum acidiphilus ARMAN_5, Candidatus Nanosalinarum sp. J07AB56, and Candidatus Nanosalina sp. J07AB43.

Figure 3.

The apparent archaeal ancestor of the ubiquitin system. The operon organization of the Ub system components in Ca. Caldiarchaeum subterraneum and similar operon structures in Bacteria. (A) A maximum-likelihood tree for the E1 component of the Ub ligase. (B) A maximum-likelihood tree for the MPN deubiquitinating enzyme. The sequences for the tree construction were retrieved from GenBank nr and env_nr databases (NCBI, NIH) and aligned using the MUSCLE program (Edgar 2004). Positions that included gaps in more than one-third of the sequences and positions with low information content were removed before tree computation (Yutin et al. 2008), which left 133 unambitious positions in the E1 alignment and 103 positions in the MPN alignment. Maximum-likelihood trees were constructed using the TreeFinder program (WAG matrix,G[Optimum]:4, 1000 replicates, Search Depth 2) (Jobb et al. 2004). The bootstrap values (shown for selected branches) represent expected-likelihood weights from 1000 local rearrangements. Branches with bootstrap support <0.5 were collapsed. For each sequence, the species name abbreviation and the gene identification numbers are indicated; (env) marine metagenome. Species: Acibo, Aciduliprofundum boonei T469; Acisa, Acidilobus saccharovorans 345-15; Aerpe, Aeropyrum pernix K1; Arath, Arabidopsis thaliana; Arcfu, Archaeoglobus fulgidus DSM 4304; Arcpr, Archaeoglobus profundus DSM 5631; Bacce, Bacillus cereus G9241; Barhe, Bartonella henselae str. Houston-1; Caebr, Caenorhabditis briggsae AF16; Cafro, Methanocella arvoryzae MRE50; Can_Csub, Candidatus Caldiarchaeum subterraneum; CanKo, Candidatus Korarchaeum cryptofilum OPF8; Censy, Cenarchaeum symbiosum A; Cloph, Clostridium phytofermentans ISDg; Dicdi, Dictyostelium discoideum AX4; Dicze, Dickeya zeae Ech1591; Drome, Drosophila melanogaster; Enthi, Entamoeba histolytica HM-1:IMSS; Ferac, Ferroplasma acidarmanus fer1; Ferpl, Ferroglobus placidus DSM 10642; Fraal, Frankia alni ACN14a; Guith, Guillardia theta; Halbo, Halogeometricum borinquense DSM 11551; Halla, Halorubrum lacusprofundi ATCC 49239; Halma, Haloarcula marismortui ATCC 43049; Halwa, Haloquadratum walsbyi DSM 16790; Helmo, Heliobacterium modesticaldum Ice1; Heman, Hemiselmis andersenii; Homsa, Homo sapiens; Isopa, Isosphaera pallida ATCC 43644; Metar, Methanocella arvoryzae MRE50; Metbo, Methanoregula boonei 6A8; Metbu, Methanococcoides burtonii DSM 6242; Methu, Methanospirillum hungatei JF-1; Metma, Methanohalophilus mahii DSM 5219; Metpa, Methanosphaerula palustris E1-9c; Metru, Methanobrevibacter ruminantium M1; Metth, Methanosaeta thermophila PT; Naegr, Naegleria gruberi strain NEG-M; Natph, Natronomonas pharaonis DSM 2160; Nemve, Nematostella vectensis; Nitma, Nitrosopumilus maritimus SCM1; Parte, Paramecium tetraurelia; Phatr, Phaeodactylum tricornutum CCAP 1055/1; Picto, Picrophilus torridus DSM 9790; Pirst, Pirellula staleyi DSM 6068; Playo, Plasmodium yoelii yoelii 17XNL; Proma, Prochlorococcus marinus str. MIT 9303; Pyrab, Pyrococcus abyssi GE5; Pyrar, Pyrobaculum arsenaticum DSM 13514; Pyrca, Pyrobaculum calidifontis JCM 11548; Pyrfu, Pyrococcus furiosus DSM 3638; Rotde, Rothia dentocariosa M567; Sacce, Saccharomyces cerevisiae S288c; Stahe, Staphylothermus hellenicus DSM 12710; Strpu, Strongylocentrotus purpuratus; Strsv, Streptomyces sviceus ATCC 29083; Tetth, Tetrahymena thermophila; Theko, Thermococcus kodakarensis KOD1; Thene, Pyrobaculum neutrophilum V24Sta; Theon, Thermococcus onnurineus NA1; Thesi, Thermococcus sibiricus MM 739; Thesp, Thermococcus sp. AM4; Thevo, Thermoplasma volcanium GSS1; Triva, Trichomonas vaginalis G3; uncar, uncultured archaeon GZfos18C8; uncCa, uncultured Candidatus Nitrosocaldus sp.; unccr, uncultured crenarchaeote; uncma, uncultured marine crenarchaeote KM3-86-C1; Ustma, Ustilago maydis 521. Taxa: Ac, Crenarchaeota; Ae, Euryarchaeota; Ak, Korarchaeota; At, Taumarchaeota; Ax, environmental samples; Ba, Actinobacteria; Bc, Cyanobacteria; Bf, Firmicutes; Bo, Planctomycetes; Bp, Proteobacteria; E8, Stramenopiles; E9, Viridiplantae; Ea, Amoebozoa; Ec, Alveolata; Eh, Cryptophyta; El, Opisthokonta; Eq, Heterolobosea; Ew, Parabasalia.

Figure 3.

The apparent archaeal ancestor of the ubiquitin system. The operon organization of the Ub system components in Ca. Caldiarchaeum subterraneum and similar operon structures in Bacteria. (A) A maximum-likelihood tree for the E1 component of the Ub ligase. (B) A maximum-likelihood tree for the MPN deubiquitinating enzyme. The sequences for the tree construction were retrieved from GenBank nr and env_nr databases (NCBI, NIH) and aligned using the MUSCLE program (Edgar 2004). Positions that included gaps in more than one-third of the sequences and positions with low information content were removed before tree computation (Yutin et al. 2008), which left 133 unambitious positions in the E1 alignment and 103 positions in the MPN alignment. Maximum-likelihood trees were constructed using the TreeFinder program (WAG matrix,G[Optimum]:4, 1000 replicates, Search Depth 2) (Jobb et al. 2004). The bootstrap values (shown for selected branches) represent expected-likelihood weights from 1000 local rearrangements. Branches with bootstrap support <0.5 were collapsed. For each sequence, the species name abbreviation and the gene identification numbers are indicated; (env) marine metagenome. Species: Acibo, Aciduliprofundum boonei T469; Acisa, Acidilobus saccharovorans 345-15; Aerpe, Aeropyrum pernix K1; Arath, Arabidopsis thaliana; Arcfu, Archaeoglobus fulgidus DSM 4304; Arcpr, Archaeoglobus profundus DSM 5631; Bacce, Bacillus cereus G9241; Barhe, Bartonella henselae str. Houston-1; Caebr, Caenorhabditis briggsae AF16; Cafro, Methanocella arvoryzae MRE50; Can_Csub, Candidatus Caldiarchaeum subterraneum; CanKo, Candidatus Korarchaeum cryptofilum OPF8; Censy, Cenarchaeum symbiosum A; Cloph, Clostridium phytofermentans ISDg; Dicdi, Dictyostelium discoideum AX4; Dicze, Dickeya zeae Ech1591; Drome, Drosophila melanogaster; Enthi, Entamoeba histolytica HM-1:IMSS; Ferac, Ferroplasma acidarmanus fer1; Ferpl, Ferroglobus placidus DSM 10642; Fraal, Frankia alni ACN14a; Guith, Guillardia theta; Halbo, Halogeometricum borinquense DSM 11551; Halla, Halorubrum lacusprofundi ATCC 49239; Halma, Haloarcula marismortui ATCC 43049; Halwa, Haloquadratum walsbyi DSM 16790; Helmo, Heliobacterium modesticaldum Ice1; Heman, Hemiselmis andersenii; Homsa, Homo sapiens; Isopa, Isosphaera pallida ATCC 43644; Metar, Methanocella arvoryzae MRE50; Metbo, Methanoregula boonei 6A8; Metbu, Methanococcoides burtonii DSM 6242; Methu, Methanospirillum hungatei JF-1; Metma, Methanohalophilus mahii DSM 5219; Metpa, Methanosphaerula palustris E1-9c; Metru, Methanobrevibacter ruminantium M1; Metth, Methanosaeta thermophila PT; Naegr, Naegleria gruberi strain NEG-M; Natph, Natronomonas pharaonis DSM 2160; Nemve, Nematostella vectensis; Nitma, Nitrosopumilus maritimus SCM1; Parte, Paramecium tetraurelia; Phatr, Phaeodactylum tricornutum CCAP 1055/1; Picto, Picrophilus torridus DSM 9790; Pirst, Pirellula staleyi DSM 6068; Playo, Plasmodium yoelii yoelii 17XNL; Proma, Prochlorococcus marinus str. MIT 9303; Pyrab, Pyrococcus abyssi GE5; Pyrar, Pyrobaculum arsenaticum DSM 13514; Pyrca, Pyrobaculum calidifontis JCM 11548; Pyrfu, Pyrococcus furiosus DSM 3638; Rotde, Rothia dentocariosa M567; Sacce, Saccharomyces cerevisiae S288c; Stahe, Staphylothermus hellenicus DSM 12710; Strpu, Strongylocentrotus purpuratus; Strsv, Streptomyces sviceus ATCC 29083; Tetth, Tetrahymena thermophila; Theko, Thermococcus kodakarensis KOD1; Thene, Pyrobaculum neutrophilum V24Sta; Theon, Thermococcus onnurineus NA1; Thesi, Thermococcus sibiricus MM 739; Thesp, Thermococcus sp. AM4; Thevo, Thermoplasma volcanium GSS1; Triva, Trichomonas vaginalis G3; uncar, uncultured archaeon GZfos18C8; uncCa, uncultured Candidatus Nitrosocaldus sp.; unccr, uncultured crenarchaeote; uncma, uncultured marine crenarchaeote KM3-86-C1; Ustma, Ustilago maydis 521. Taxa: Ac, Crenarchaeota; Ae, Euryarchaeota; Ak, Korarchaeota; At, Taumarchaeota; Ax, environmental samples; Ba, Actinobacteria; Bc, Cyanobacteria; Bf, Firmicutes; Bo, Planctomycetes; Bp, Proteobacteria; E8, Stramenopiles; E9, Viridiplantae; Ea, Amoebozoa; Ec, Alveolata; Eh, Cryptophyta; El, Opisthokonta; Eq, Heterolobosea; Ew, Parabasalia.

Figure 3.

The apparent archaeal ancestor of the ubiquitin system. The operon organization of the Ub system components in Ca. Caldiarchaeum subterraneum and similar operon structures in Bacteria. (A) A maximum-likelihood tree for the E1 component of the Ub ligase. (B) A maximum-likelihood tree for the MPN deubiquitinating enzyme. The sequences for the tree construction were retrieved from GenBank nr and env_nr databases (NCBI, NIH) and aligned using the MUSCLE program (Edgar 2004). Positions that included gaps in more than one-third of the sequences and positions with low information content were removed before tree computation (Yutin et al. 2008), which left 133 unambitious positions in the E1 alignment and 103 positions in the MPN alignment. Maximum-likelihood trees were constructed using the TreeFinder program (WAG matrix,G[Optimum]:4, 1000 replicates, Search Depth 2) (Jobb et al. 2004). The bootstrap values (shown for selected branches) represent expected-likelihood weights from 1000 local rearrangements. Branches with bootstrap support <0.5 were collapsed. For each sequence, the species name abbreviation and the gene identification numbers are indicated; (env) marine metagenome. Species: Acibo, Aciduliprofundum boonei T469; Acisa, Acidilobus saccharovorans 345-15; Aerpe, Aeropyrum pernix K1; Arath, Arabidopsis thaliana; Arcfu, Archaeoglobus fulgidus DSM 4304; Arcpr, Archaeoglobus profundus DSM 5631; Bacce, Bacillus cereus G9241; Barhe, Bartonella henselae str. Houston-1; Caebr, Caenorhabditis briggsae AF16; Cafro, Methanocella arvoryzae MRE50; Can_Csub, Candidatus Caldiarchaeum subterraneum; CanKo, Candidatus Korarchaeum cryptofilum OPF8; Censy, Cenarchaeum symbiosum A; Cloph, Clostridium phytofermentans ISDg; Dicdi, Dictyostelium discoideum AX4; Dicze, Dickeya zeae Ech1591; Drome, Drosophila melanogaster; Enthi, Entamoeba histolytica HM-1:IMSS; Ferac, Ferroplasma acidarmanus fer1; Ferpl, Ferroglobus placidus DSM 10642; Fraal, Frankia alni ACN14a; Guith, Guillardia theta; Halbo, Halogeometricum borinquense DSM 11551; Halla, Halorubrum lacusprofundi ATCC 49239; Halma, Haloarcula marismortui ATCC 43049; Halwa, Haloquadratum walsbyi DSM 16790; Helmo, Heliobacterium modesticaldum Ice1; Heman, Hemiselmis andersenii; Homsa, Homo sapiens; Isopa, Isosphaera pallida ATCC 43644; Metar, Methanocella arvoryzae MRE50; Metbo, Methanoregula boonei 6A8; Metbu, Methanococcoides burtonii DSM 6242; Methu, Methanospirillum hungatei JF-1; Metma, Methanohalophilus mahii DSM 5219; Metpa, Methanosphaerula palustris E1-9c; Metru, Methanobrevibacter ruminantium M1; Metth, Methanosaeta thermophila PT; Naegr, Naegleria gruberi strain NEG-M; Natph, Natronomonas pharaonis DSM 2160; Nemve, Nematostella vectensis; Nitma, Nitrosopumilus maritimus SCM1; Parte, Paramecium tetraurelia; Phatr, Phaeodactylum tricornutum CCAP 1055/1; Picto, Picrophilus torridus DSM 9790; Pirst, Pirellula staleyi DSM 6068; Playo, Plasmodium yoelii yoelii 17XNL; Proma, Prochlorococcus marinus str. MIT 9303; Pyrab, Pyrococcus abyssi GE5; Pyrar, Pyrobaculum arsenaticum DSM 13514; Pyrca, Pyrobaculum calidifontis JCM 11548; Pyrfu, Pyrococcus furiosus DSM 3638; Rotde, Rothia dentocariosa M567; Sacce, Saccharomyces cerevisiae S288c; Stahe, Staphylothermus hellenicus DSM 12710; Strpu, Strongylocentrotus purpuratus; Strsv, Streptomyces sviceus ATCC 29083; Tetth, Tetrahymena thermophila; Theko, Thermococcus kodakarensis KOD1; Thene, Pyrobaculum neutrophilum V24Sta; Theon, Thermococcus onnurineus NA1; Thesi, Thermococcus sibiricus MM 739; Thesp, Thermococcus sp. AM4; Thevo, Thermoplasma volcanium GSS1; Triva, Trichomonas vaginalis G3; uncar, uncultured archaeon GZfos18C8; uncCa, uncultured Candidatus Nitrosocaldus sp.; unccr, uncultured crenarchaeote; uncma, uncultured marine crenarchaeote KM3-86-C1; Ustma, Ustilago maydis 521. Taxa: Ac, Crenarchaeota; Ae, Euryarchaeota; Ak, Korarchaeota; At, Taumarchaeota; Ax, environmental samples; Ba, Actinobacteria; Bc, Cyanobacteria; Bf, Firmicutes; Bo, Planctomycetes; Bp, Proteobacteria; E8, Stramenopiles; E9, Viridiplantae; Ea, Amoebozoa; Ec, Alveolata; Eh, Cryptophyta; El, Opisthokonta; Eq, Heterolobosea; Ew, Parabasalia.

Figure 4.

Evolutionary scenario for the origin of the proto-eukaryote from a complex archaeal ancestor. M, Mitochondria; N, nucleus.