The Origin and Evolution of Eukaryotes

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Index

A cell division and membrane remodeling ABA. See Abscisic acid systems, 123 Abscisic acid (ABA), 374 cytoskeleton, 119, 122–123 ACAP, 223 RNA interference system, 123–124 Acetabularia, 369 ubiquitin signaling system, 118–122 Acetobacter pomurum,33–34 microfossil records of eukaryogenesis, Acromyrmex echinatior,32 153–160 Actin phylogenomics study of evolutionary association dynamics with eukaryotes comparison of prokaryotes and eukaryotes, concatenated protein and ribosomal DNA data 207–208, 211 sets, 103–104 cooperation between filaments, 210 compositional bias effects, 107 dynamic instability, 208–210 data selection, 101–103 force generation, 210 discordant protein cluster removal, 104–106 nucleation, polymerization and capping, 208 prospects for study, 108–109 treadmilling, 208 taxon sampling effects, 107 origins, 203–205 Archaeplastida, 186–187 Actinobacteria, Neomura relationship, 52–53 ArfGAPs, 223–224, 226 Adaptin, 222, 226 Arp2/3, 44, 46, 203, 205 ADP-ribosyltransferase (ART), 284–285 ArsA, 239 African sleeping sickness, 224 ART. See ADP-ribosyltransferase Alb3, 241 Aspergillus, parasexuality, 345 Algoriphagus machipongonensis,34 ATP synthase, 258, 264 Alp7, 209 AT P /ADP translocase, 144, 258–259 Alp7A, 210 Auxin, rhizobacteria synthesis, 32–33 a-Proteobacterial component (APC), mitochondria origins, 254, 259–260 Alternative splicing. See Spliceosome B Alu, 321 Bacteria, animal origin influences Alveolates. See Stramenophiles, alveolates, biology of first animals, 395–398 and Rhizaria choanoflagellate colony as model, 398–399 Amoeba proteus,86 developmental switch regulation, 399–491 Amoebophilus, 288 genetic toolkit for animal multicellularity, Amoebozoa, 185 401–403 Anaphase promoting complex (APC), 60 overview, 393–395 AP-1, 226–227 prospects for study, 403–404 AP-2, 224 Bangiomorpha, 264 AP-3, 226 Bangiomorpha pubescens, 154, 157, 169, 172 AP-5, 226–227 Bigelowiella, 288 APC. See a-Proteobacterial component; Anaphase Bigelowiella natans, 228–229, 309 promoting complex Bioenergetics Apoptosis, threshold, 92 mitochondria and evolution of basal eukaryotic Arabidopsis, 372 traits ARAP, 224 mitonuclear coadaptation, 90–92 ARC6, 268 overview, 89–90 Archaea. See also TACK superphylum respiratory function and evolutionary eukaryome trade-offs, 92–93

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Bioenergetics (Continued) Coleochaete orbicularis, 370, 372 proton gradients and constraints on origin of life Collodictyon, 191 alkaline hydrothermal vents for Comparative biology, expectations in eukaryogenesis harvesting, 82–83 studies, 151–153 evolution of machinery, 83–85 COP coats, 47, 221, 239 overview, 81–82 CoRR hypothesis, 88 transition from prokaryotes to eukaryotes Cryptococcus neoformans, 352 core bioenergetic genome, 87 Cyanidoschyzon, 286 overview, 85 Cyanidoschyzon merolae, 143–144 prokaryote genomic asymmetry from Cytoskeleton endosymbiosis, 89 Archaea, 119, 122–123 scaling of cell volume and genome copy dynamics number, 85–87 comparison of prokaryotes and eukaryotes, Biological species concept (BSC), 3–4 207–208, 211 Biomarkers, evolutionary rate calibration cooperation between filaments, 210 estimation, 168–169 dynamic instability, 208–210 Bradyrhizobium,29 filament nucleation, polymerization and BSC. See Biological species concept capping, 208 BtubA, 205–206 force generation, 210 BtubB, 205–206 higher-order filament structures, 210–211 Bugula, 399 treadmilling, 208 Burkholderia,32 eukaryote organelle coevolution, 212–214 functional overview, 200–203 prokaryote homologs C actin origins, 203–205 C60-Poisson models, 174–176 microtubule origins, 205–206 Caenorhabditis,47 miscellaneous proteins, 206–207 Candida albicans, parasexuality, 345–346 motor proteins, 206 Candidatus Caldiarchaeum subterraneum, 116, 118, 120, 122 Candidatus Chloracidobacterium, 64 D Candidatus Korarchaeum cryptophylum, 106, 116 DegP, 238 Canis familiaris,4 Deinococcus, 62, 65 Carotenoids, biosynthesis, 31, 147 Dendroctonus ponderosae,32 Caulerpa, 369 Derlin, 50 Cdk8, 281 Diphylleia, 191 Cell division, Archaea system, 123 DNA methylation. See Epigenetics Cell kinds, 41–44 Doc, 285 Chagas disease, 224 Dot1, 279 Chara, 372–374, 376 DSCR3, 226, 229 Chemosynthesis, 30 Chimera, 17–19 Chlamydia, 264–265 E Chlamydiae, photosynthetic eukaryogenesis, EGT. See Endosymbiotic gene transfer 144–147 Elf1, 118 Chlamydomonas reinhardtii, 144, 377–384 ENCODE project, 321–322 Chloroflexi, 64–65, 68 Endoplasmic reticulum (ER) Chloroplast. See Plastids coevolution of mitochondrial, endoplasmic Chromera velia, 143–144 reticulum, and peroxisomal respiration Cilia, phagotrophy-related origin, 57–59 and segregation, 54–55 Ciona intestinalis, 399 origins, 235 Cladonia rangifera,32 Endoplasmic reticulum–associated degradation Cladophora, 369 (ERAD), 235, 239–240 CLMP1, 268 Endoplasmic reticulum–mitochondria encounter Closterium, 376 structure (ERMES), 133 Coleochaete, 375 Endorina, 377

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Endosymbiosis F ATP savings from endosymbiont proteins, 87 FECA. See First eukaryotic common ancestor photosynthesis FfH, 237 cryptic Chlamydiae in photosynthetic Fic, 285 eukaryogenesis, 144–147 Filarcheota, diverse cell biology, 55–57 cryptic green algal endosymbioses in diatoms First eukaryotic common ancestor (FECA), 129, and chromerids, 142–143 131, 134, 256 overview, 141–142 Fossils prospects for study, 147–148 Archaea eukaryogenesis microfossil taxonomic sampling and methods, 143–144 records, 153–160 prokaryote genomic asymmetry, 89 cross-validation for accuracy assessment, 176 Endosymbiosis. See also Mitochondria; Plastids; evolutionary rate calibration estimation, 168–169 Symbiosis molecular clock analysis constraints, 169–170 chimeras, 17–19 Frankia,29 order of discovery effect on interpretation, 19–21 FtsA, 203, 205, 207, 210–211 theories, 15–17, 21–23 FtsH, 207 Endosymbiotic gene transfer (EGT), 142–145, 147, FtsI, 202 250, 267 FtsW, 202 Energetics. See Bioenergetics FtsY, 237 Enteromorpha,34 FtsZ, 45, 50, 54, 123, 202, 205, 210, 213, 268 Eocyte model, 98–99, 115 Epigenetics bacterial conflict systems, 288–289 G biogeochemical considerations, 289 GA. See Gibberellic acid DNA modification, 286–287 GAR1, 383 encoding, resetting, and reading of GCN5, 279 marks, 274–278 Get3, 239 eukaryote evolution, 287–288 Giardia, 15, 278, 286 overview, 273–274 Gibberellic acid (GA), 374 prospects for study, 289–290 GIT, 224 protein domains, 276–277, 280 Glycosyltransferases, 285 protein modifications GOE. See Great oxygenation event acetylation, 279, 281 Gonium, 380–381 acylation, 286 Great oxygenation event (GOE), 289–290 ADP ribosylation, 284–285 Green algae. See Photosynthesis; Plant glycosylation, 285 multicellularity methylation, 278–279 Grypania, 264 miscellaneous modifications, 285–286 Grypania spiralis, 169 nucleotidylation, 285 GSM1, 356 phosphorylation, 281–282 GSP1, 356 ubiquitin system, 282–284 Guillardia theta, 228–228 reactions, 275 Epulopiscium, 86, 88 ER. See Endoplasmic reticulum H ERAD. See Endoplasmic reticulum–associated Heliobacterium,42 degradation HGT. See Horizontal gene transfer ERMES. See Endoplasmic reticulum–mitochondria Histones, 42, 50, 60 encounter structure modification. See Epigenetics ESCRT-0, 226 Homeostatic property cluster (HPC), 2, 7 ESCRT-I, 226 Horizontal gene transfer (HGT), 116, 118, 123–124, ESCRT-III, 45–46, 44, 123 147, 191, 205–206, 227, 229, 343 Ethylene, 374 Hotair, 332 Eubacterium rangifera,32 HPC. See Homeostatic property cluster Euglena,86 Human Microbiome Project, 27 Eukaryotic tree of life, 166–168, 182–183 Hydrogen Hypothesis, 10, 98–99 Excavata, 185–186 Hydroides elegans, 399

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I Markov chain Monte Carlo (MCMC), 176 IDA. See Initial Darwinian ancestor MAT, 351 Importin-b, 239 Mating-type determination (MTD), 350–353 Initial Darwinian ancestor (IDA), 318 MCM, 60 Intron. See Spliceosome MCMC. See Markov chain Monte Carlo ME. See Methylerythritol phosphate Meiosis. See Sexual reproduction J Membrane trafficking. See also Protein trafficking JAK, 282 ancient machinery, 221–223 JBP, 287, 289 complexity, 226–229 JOR/JmjC, 278, 286–287, 289 conserved and lineage-specific proteins, 223–225 nonendosymbiotic organ evolution, 222–223 overview, 219–221 K patchy proteins, 225–226 Katanin, 206–207 prospects for study, 229–230 Kif proteins, 211 Mesoprotozeroic era, eukaryote fossils, 155, 157, 169 Kinesin, 211 Mesotigma, 370 MetaHIT, 27 Methylerythritol phosphate (ME), synthesis, 52 L Mevalonate, synthesis, 52 LACA. See Last archaeal common ancestor MglA, 206 Last archaeal common ancestor (LACA), 116, 123 MglB, 206 Last eukaryotic common ancestor (LECA) Micrasterias, 375 Archaea, 114, 123 Microfossils. See Fossils dating, 171–174, 177 Microtubule, origins, 205–206 epigenetics, 278–279, 281–287 MID, 351, 383 membrane trafficking system, 222–223, 226–227, Midichloria mitochondrii, 136 234 MIR element, 323 mitochondria, 129–134, 136–137 Mitochondria overview, 7–10, 20 acquisition models, 135–137 proteome, 256 coevolution of mitochondrial, endoplasmic sexual reproduction, 343–344, 348, 355 reticulum, and peroxisomal respiration spliceosome, 299–308 and segregation, 54–55 tree of life, 166, 168 early versus late eukaryogenesis scenarios, 133–135 Last mitochondrial common ancestor (LMCA), 250, evolution of basal eukaryotic traits 252 mitonuclear coadaptation, 90–92 Last universal common ancestor (LUCA), 13, 20, 70, 318 overview, 89–90 Lateral gene transfer (LGT), 8, 43, 51–52, 63, 65, 69–70, respiratory function and evolutionary trade-offs, 80, 256, 259, 401–402 92–93 LBA. See Long branch attraction last eukaryotic common ancestor LECA. See Last eukaryotic common ancestor inference of mitochondria in, 131–132 Legionella, 288 symbiosis timing, 132–133 Leucaena leucocephala,32 pre-endosymbiont hypothesis Leucoprinus gongylophorus,32 implications, 258–260 LGT. See Lateral gene transfer premitochondrion, 256–258 LINEs, 321–322 proteome studies, 254–256 LMCA. See Last mitochondrial common ancestor Rumsfeldian view of origins Lolium,31 known knowns, 250–252 Long branch attraction (LBA), 165, 171 known unknowns, 252 LUCA. See Last universal common ancestor unknown unknowns, 252–253 symbiotic models, 253–254 Mitochondrion-related organelle (MRO), 15 M MIZ, 283 MADS, 376 Monosiga, 224 Malawimonas, 191 Monosiga brevicollis, 401 MamK, 205 Moranella endobia, 136

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MORC, 277 NPRS. See Nonparametric rate smoothing Most recent universal common ancestor (MRUCA), NTF2, 240 7–8, 256 Nuclear envelope, origins, 235 MreB, 45, 202–203, 205 Nuclear pore complex (NPC), 239 MRO. See Mitochondrion-related organelle MRUCA. See Most recent universal common ancestor MT loci, 350–352, 383 O MTD. See Mating-type-determination Odyssella, 288 Multicellularity. See Bacteria, animal origin inﬂuences; Omp85, 238, 240–241 Plant multicellularity OPH. See Organelle paralogy hypothesis Myo1, 203 Opisthokonta, 185 Organelle paralogy hypothesis (OPH), 222–223 Ostreococcus lucimarinus, 144 N Ostreococcus tauri, 144 Naegleria, 227, 286 Oxa1, 241 Natural kinds domains, two versus three, 4–6 eukaryote, 6–11 P shared history, 2–3 Paederus,31 shared properties, 2 Palmitoyltransferases, 286 species and domains, 3–4 Pandorina, 377 Negibacteria, cell envelope, 62–64 ParA, 50, 57, 202–203 Neomuran revolution Parasexuality. See Sexual reproduction actinobacteria relationship, 52–53 ParB, 50, 57 archaebacterial divergence, 51–52 PARC5, 268 cell cycle/structure coevolution, 50–51 ParM, 202–203, 205, 209 cell kinds, 41–44 PARP. See Poly(ADP-ribose) polymerase cilia, phagotrophy-related origin, 57–59 Paulinella, 265–266, 354 coevolution of mitochondrial, endoplasmic Paulinella chromataphora, 29, 244 reticulum, and peroxisomal respiration PDV1, 268 and segregation, 54–55 Peroxisome, coevolution of mitochondrial, coevolutionary theory of eukaryogenesis, 44–50, endoplasmic reticulum, and 234 peroxisomal respiration and cotranslational secretion, 53–54 segregation, 54–55 Filarcheota diverse cell biology, 55–57 Persiciverga, 287 green bacteria and origin of life, 64–65 Pex proteins, 239 methodological bias and molecular clock myths, Phaeodactylum tricornutum, 144 67–71 Phagocytosing Archaeon Theory (PhAT), 98–99, misunderstandings, 61–62 108–109, 136 multigene sequence trees and fossil data integration PhAT. See Phagocytosing Archaeon Theory for real timing of cell megaevolution, Photosynthesis. See also Plastids 65–67 endosymbiosis negibacteria cell envelope, 62–64 cryptic Chlamydiae in photosynthetic Neoprotozeroic era, eukaryotic diversiﬁcation, 156 eukaryogenesis, 144–147 NigE, 278–279 cryptic green algal endosymbioses in diatoms Nitella, 372–373 and chromerids, 142–143 Nitrosoarchaeum, 206 overview, 141–142 Nitrosopumilis maritimus, 123 prospects for study, 147–148 NMD. See Nonsense-mediated decay taxonomic sampling and methods, 143–144 Non-a-proteobacterial component (NPC), overview, 263 mitochondria origins, 252, 254–255, Phylogenomics 259–260 deep relationships among eukaryotes, 190–191 Nonparametric rate smoothing (NPRS), 170 eukaryotic supergroups Nonsense-mediated decay (NMD), 306, 308 Amoebozoa, 185 NPC. See Non-a-proteobacterial component; Nuclear Archaeplastida, 186–187 pore complex Excavata, 185–186

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Phylogenomics (Continued) Protein arginine methyltransferase (PRMT), 278 Opisthokonta, 185 Protein modification. See Epigenetics stramenophiles, alveolates, and Rhizaria, Protein trafficking 187–189 ancient machinery, 238–240 overview, 183–185 bacterial souvenirs, 236–238 rooting of eukaryote tree, 189–190 early eukaryogenesis models, 234–236 TACK superphylum study of evolutionary endosymbiotic organelles, 240–242 association with eukaryotes evolutionary variations of complexity, 244 compositional bias effects, 107 overview, 236 concatenated protein and ribosomal DNA data prospects for study, 244 sets, 103–104 signal evolution, 242–244 data selection, 101–103 Protochlamydia, 144, 288 discordant protein cluster removal, 104–106 Protozeroic eon prospects for study, 108–109 eukaryote establishment, 154–156 taxon sampling effects, 107 Neoprotozeroic era and eukaryotic diversification, Physcomitrella, 374, 376 156 Plant multicellularity Prp8, 302 cellular diversity in green lineage, 366–368 Pseudoalteromonas,34 green algae evolution Pseudomonas,31–32 charophyte algae and origins of land plant PTEN, 330 multicellularity, 369–376 PTENP1, 330 embryophyte genetic toolkit origins, 376 macroscopic complexity coenocytic algae, 369 R giant uninucleate algae, 369 Rab, 222–224, 226 multicellular algae, 369 RAN, 240 overview, 368 Relaxed molecular clock (RMC) analysis streptophyte transition to multicellularity calibration constraints, 172–173 closest unicellular relative of land plants, CIR model, 175 370–371 comparison with other models, 175–176 filamentous growth and cytokinesis, 371–372 dating deep events in eukaryotic evolution, 171–172 hormone signaling, 373–374 eukaryote root positioning, 173–174 matrotrophic support of zygote, 375 last eukaryotic common ancestor dating, 171 oogamous sexual reproduction, 374–375 overview, 170–171 regulated division plane, cell differentiation, prospects, 176–177 and polarized growth, 372–373 substitution model combination, 174–175 symplastic connections and intercellular UGam, 175 communication, 373 Reproduction. See Sexual reproduction volvocine algae Rhanella,32 Chlamydomonas cell biology, 377–379 Rhizaria. See Stramenophiles, alveolates, and Rhizaria multicellular innovations, 379–383 Rhizobium,29 overview, 376–377 Ribosomal DNA, plastid origin studies, 265 prospects for study, 384 Rickettsiales,27 innovations rooted in green lineage, 375–376 RIF-1, 398, 400–401 overview, 365–366 RING, 283–284 Plant-growth-promoting rhizobacteria, 32 RMC analysis. See Relaxed molecular clock analysis Plastids. See also Photosynthesis RNA endosymbiosis hypotheses, 264–268 chromosomal RNA, 320 gene transfer, 267 classification, 327–328 overview of origins, 142, 235–236 compartmentalization, 319 Paulinella studies, 265–266 competitive RNAs, 330 Pleodorina, 377, 379 history of study, 317–318 Poly(ADP-ribose) polymerase (PARP), 284–285 junk RNA as future gene module, 323 Prader–Willi syndrome, 324 noncoding functional RNA, 326 PRMT. See Protein arginine methyltransferase novel RNAs, 329–330 Profilin, 206 prospects for study, 330–333

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RNA world, 318–320 Sorting and assembly machinery (SAM), 241 signatures on extant DNA genomes, 320–323 Spastin, 206–207 transcriptional noise, 326, 328–329 SPB. See Spindle pole body transposable elements, 323–325 Sphingomonas paucimobilis, 400 RNAi. See RNA interference Spindle pole body (SPB), 203 RNA interference (RNAi), Archaea system, 123–124 Spliceosome RNA splicing. See Spliceosome alternative splicing origins, 307–309 RPB8, 118 evolution across eukaryotes, 306–307 RPC34, 118 history of study, 295–296 RPD3, 279, 281 intron classification RUBISCO, 278 group I self-splicing introns, 298 group II self-splicing introns, 298 spliceosomal introns, 296–298 S transfer RNA introns, 298–299 Salpingoeca rosetta, 397–398, 400 origin and establishment in eukaryogenesis SAM. See Sorting and assembly machinery group II intron proliferation in host genome, SAR. See Stramenophiles, alveolates, and Rhizaria 300–301 SCOP. See Structural Classification of Proteins group II intron transfer to host genome, 299 SEC, 237 major and minor spliceosome systems, 302–303 Sec systems, 54, 237–238, 240, 243 trans-complementation, 301–302 Serial Endosymbiosis Theory, 98–99 reconstruction in last eukaryotic common ancestor, Serratia,32 303–306 SET, 279 Spo11, 346, 348 Sexual reproduction SRP. See Signal recognition particle cell–cell fusion regulation SRY, 351 recognition/fusion molecule expression, Stramenophiles, alveolates, and Rhizaria (SAR), 349–350 187–189 restricting to self interactions, 349 Streptophyte. See Plant multicellularity LECA, 343–344 Strigolactones, 374 mating type Structural Classification of Proteins (SCOP), 256 coupling of diploidy to resting spore formation, Stu2, 203 352–354 STY kinases, 281–282 mating-type-determination system, 350–353 Substitution, 174–175 multiple mating types and homothallism, 352 Sulfur Syntrophy, 98–99 organelle genome transmission regulation SUMO, 283 theory, 354–355 SWI2, 277 UP systems, 355–356 Symbiosis. See also Endosymbiosis origins, 350 health promotion, 32–35 meiosis evolution, 346–349 metabolism parasexuality ancient evolutionary roots, 28–29 Aspergillus, 345 primary metabolism, 29–31 Candida albicans, 345–346 secondary metabolism, 31–32 ploidy alteration via cell–cell fusion and meiosis, Synechoccus,29 344–345 Synechocystis,88 sex and speciation, 356–357 Shuiyousphaeridium macroreticulatum, 169 Signal recognition particle (SRP), 53, 237–238, 242 T SINEs, 321–322, 324 TACK superphylum Sir2, 279 eukaryogenesis, 124–125 SKL, 54 evidence for, 103, 116–118 Skp, 238 phylogenomics study of evolutionary association SMAP, 223 with eukaryotes SNAREs, 221, 239 compositional bias effects, 107 SNF2, 277 concatenated protein and ribosomal DNA data Snord116, 331–332 sets, 103–104 SopA, 203, 209 data selection, 101–103

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TACK superphylum (Continued) TTL, 284 discordant protein cluster removal, 104–106 TubA, 205 prospects for study, 108–109 TubZ, 47, 202, 208 taxon sampling effects, 107 TAF1, 281 Tappania plana, 169 U TAT, 54, 237 U2 intron. See Spliceosome TBP, 43 U12 intron. See Spliceosome TCA cycle, 259, 265, 289 Ubiquitin TE. See Transposable element Archaea signaling system, 118–122 TEM. See Transmission electron microscopy epigenetics, 282–284 TET, 289 UP systems, 355–356 TFII, 60 Urm1, 118 TFIIB, 45 TFIID, 281 Thalassiosira pseudomana, 144 V Thermoplasma, 18, 115 VARL,382 Thiomargarita, 86, 88 VDAC, 240 TIC, 241–242, 268 Volvox carteri, 379, 381–384 TIM, 244 Vps1, 203 TIM23, 241 Vps26, 226 TIR, 395–396 Vps29, 239 TLS. See Trilaminar wall structure TOC, 240–242, 244, 268 TOM, 240–241 W Transmission electron microscopy (TEM), microfossils, Walker ATPases, 203, 209 155 WGA. See Wheat germ agglutinin Transposable element (TE), 323–325 Wheat germ agglutinin (WGA), 399 Trc40, 239 Tremblaya princeps, 136 Trichomonas vaginalis, 213, 278 Y Trilaminar wall structure (TLS), chlorophytes, 155 YidC, 237–238, 241

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