Skip to main content
SpringerLink
Log in

Prokaryote/Eukaryote Dichotomy and Bacteria/Archaea/Eukarya Domains: Two Inseparable Concepts

  • Chapter
  • First Online:
Prokaryotes and Evolution

Abstract

The various schemes proposed to classify microorganisms in the living world have long been subject of heated debates. The classical dichotomic distinction between Prokaryotae (cells without nucleus) and Eukaryotae (cells with nucleus) functional and phenotypic categories was deeply changed by rRNA gene-based analysis that divided the living world into three phylogenetic domains: the Bacteria, the Archaea (originally Archaebacteria), and the Eukarya. In this chapter, we review the terms of this debate between the prokaryotic/eukaryotic functional and phenotypic dichotomy and the 16S/18S phylogenetic dichotomy that separates prokaryotes into two distinct domains. The specific characteristics that emphasize the organizational and functional complexity of prokaryotes and justify maintaining this terminology are discussed. We conclude that the organizational and functional concept of a prokaryotes/eukaryotes dichotomy can be easily supplemented by the phylogenetic concept Bacteria/Archaea/Eukarya. The two concepts are not irreconcilable but complementary, resulting in a consensual proposal that integrates both phenotypic and genotypic criteria.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 119.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abreu F, Silva K, Martins J, Lins U (2006) Cell viability in magnetotactic multicellular prokaryotes. Int Microbiol 9:267–272

    CAS  PubMed  Google Scholar 

  • Bapteste E, O’Malley M, Beiko R, Ereshefsky M, Gogarten J, Franklin-Hall L, Lapointe F, Dupré J, Dagan T, Boucher Y et al (2009) Prokaryotic evolution and the tree of life are two different things. Biol Direct 4:34

    Article  Google Scholar 

  • Bertrand J-C, Brochier-Armanet C, Gouy M, Westall F (2015) For three billion years, microorganisms were the only inhabitants of the earth. In: Bertrand J, Caumette P, Lebaron P, Matheron R, Normand P, Sime-Ngando T (eds) Environmental microbiology: fundamentals and aplications. Springer, Dordrecht/Heidelberg/New York/London, pp 75–106

    Google Scholar 

  • Best D, Higgins I (1981) Methane-oxidizing activity and membrane morphology in a methanol- grown obligate methanotroph, Methylosinus trichosporium OB3b. J Gen Microbiol 125:73–84

    CAS  Google Scholar 

  • Brochier-Armanet C, Moreira D (2015) Horizontal gene transfer in microbial ecosystems. In: Bertrand J, Caumette P, Lebaron P, Matheron R, Normand P, Sime-Ngando T (eds) Environmental microbiology: fundamentals and applications. Springer, Dordrecht/Heidelberg/New York/London, pp 471–512

    Google Scholar 

  • Cabeen M, Jacobs-Wagner C (2010) The bacterial cytoskeleton. Annu Rev Genet 44:365–392

    Article  CAS  Google Scholar 

  • Chatton E (1925) Pansporella perplexa. Réflexions sur la biologie et la phylogénie des protozoaires. Annales des Sciences Naturelles Zoologie et Biologie Animale 10-VII: 1–84

    Google Scholar 

  • Cho H (2015) The role of cytoskeletal elements in shaping bacterial cells. J Microbiol Biotechnol 25:307–316

    Article  CAS  Google Scholar 

  • Chowdhury C, Chun S, Pang A, Sawaya M, Sinha S, Yeates T, Bobik T (2015) Selective molecular transport through the protein shell of a bacterial microcompartment organelle. Proc Natl Acad Sci U S A 112:2990–2995

    Article  CAS  Google Scholar 

  • Claessen D, Rozen D, Kuipers O, Søgaard-Anderson L, van Wezel G (2014) Bacterial solutions to multicellularity: a tale of biofilms, filaments and fruiting bodies. Nature Rev Microbiol 12:115–124

    Article  CAS  Google Scholar 

  • Courties C, Vaquer A, Troussellier M, Lautier J, Chrétiennot-Dinet M, Neveux J, Machado C, Claustre H (1994) Smallest eukaryotic organism. Nature 370:255

    Article  Google Scholar 

  • De Boer W, Hazeu W (1972) Observations on the fine structure of a methane-oxidizing bacterium. Antonie Van Leeuwenhoek 38:33–47

    Article  Google Scholar 

  • De Duve C (2007) The origin of eukaryotes: a reappraisal. Nature Rev 8:395–403

    Article  Google Scholar 

  • Derelle E, Ferraz C, Rombauts S, Rouzé P, Worden AZ, Robbens S, Partensky F, Degroeve S, Echeynié S, Cooke R et al (2006) Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci U S A 103:11647–11652

    Article  CAS  Google Scholar 

  • DeRosa M, Gambacorta A, Huber R, Lanzotti V, Nicolaus B, Stetter K, Trincone A (1988) A new 15,16-diméthyl-30-glyceryloxy-triacontanoic acid from lipids of Thermotoga maritima. J Soc Chem Commun 1988:1300–1301

    Article  Google Scholar 

  • Devos D (2014a) PVC bacteria: variation of, but not exception to, the gram-negative cell plan. Trends Microbiol 22:14–20

    Article  CAS  Google Scholar 

  • Devos D (2014b) Re-interpretation of the evidence for PVC cell plan supports a gram-negative origin. Antonie Van Leeuwenhoek 105:271–274

    Article  Google Scholar 

  • Dolan M, Margulis L (2007) Advances in biology reveal truth about prokaryotes. Nature 445:21

    Article  CAS  Google Scholar 

  • Duggin I, Aylett C, Walsh J, Michie K, Wang Q, Turnbull L, Dawson E, Harry E, Whitchurch C, Amos L et al (2015) CetZ tubulin-like proteins control archaeal cell shape. Nature 519:362–365

    Article  CAS  Google Scholar 

  • Embley T, Williams T (2015) Steps on the road to eukaryotes. Nature 521:169–170

    Article  CAS  Google Scholar 

  • Fuerst J, Sagulenko E (2011) Beyond the bacterium: planctomycetes challenge our concepts of microbial structure and function. Nature Rev Microbiol 9:403–413

    Article  CAS  Google Scholar 

  • Ghai R, Mizuno CM, Picazo A, Camacho A, Rodriguez-Valera F (2013) Metagenomics uncovers a new group of low GC and ultra-small marine Actinobacteria. Sci Rep 3:2471

    Article  Google Scholar 

  • Gottshall E, Seebart C, Gatlin J, Ward N (2014) Spatially segregated transcription and translation in cells of the endomembrane-containing bacterium Gemmata obscuriglobus. Proc Natl Acad Sci U S A 111:11067–11072

    Article  CAS  Google Scholar 

  • Graumann P (2007) Cytoskeletal elements in bacteria. Annu Rev Microbiol 61:589–618

    Article  CAS  Google Scholar 

  • Grossi V, Mollex D, Vinçon-Laugier A, Hakil F, Pacton M, Cravo-Laureau C (2015) Mono- and dialkyl glycerol ether lipids in anaerobic bacteria: biosynthetic insights from the mesophilic sulfate reducer Desulfatibacillum alkenivorans PF2803T. Appl Environ Microbiol 81:3157–3168

    Article  CAS  Google Scholar 

  • Hanson R, Hanson T (1996) Methanotrophic bacteria. Microbiol Rev 60:439–471

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ingerson-Mahar M, Gitai Z (2012) A growing family: the expanding universe of the bacterial cytoskeleton. FEMS Microbiol Rev 36:256–266

    Article  CAS  Google Scholar 

  • Jeske O, Schüler M, Schumann P, Schneider A, Boedeker C, Jogler M, Bollschweiler D, Rohde M, Mayer C, Engelhardt H et al (2015) Planctomycetes do possess a peptidoglycan cell wall. Nat Commun 6:7116

    Article  CAS  Google Scholar 

  • Kerfeld C, Heinhorst S, Cannon G (2010) Bacterial microcomparments. Ann Rev Microbiol 64:391–408

    Article  CAS  Google Scholar 

  • Lewis P, Thaker S, Errington J (2000) Compartmentalization of transcription and translation in Bacillus subtilis. EMBO J 19:710–718

    Article  CAS  Google Scholar 

  • Liberton M, Berg R, Heuser J, Roth R, Himadri B, Pakrasi H (2006) Ultrastructure of the membrane systems in the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. Protoplasma 227:129–138

    Article  Google Scholar 

  • Lin L, Thanbichler M (2013) Nucleotide-independent cytoskeletal scaffolds in Bacteria. Cytoskeleton 70:409–423

    Article  CAS  Google Scholar 

  • Lonhienne T, Sagulenko E, Webb R, Lee K-C, Franke J, Devos D, Nouwens A, Caroll B, Fuerst J (2010) Endocytosis-like protein uptake in the bacterium Gemmata obscuriglobus. Proc Natl Acad Sci U S A 107:12883–12888

    Article  CAS  Google Scholar 

  • Lundgren M, Andersson A, Chen L, Nilsson P, Bernander R (2004) Three replication origins in Sulfolobus species: synchronous initiation of chromosome replication and asynchronous termination. Proc Natl Acad Sci U S A 101:7046–7051

    Article  CAS  Google Scholar 

  • Lyons N, Kolter R (2015) On the evolution of multicellularity. Curr Opinion Microbiol 24:21–28

    Article  CAS  Google Scholar 

  • Madigan M, Bender K, Buckley D, Sattley W, Stahl D (2015) Brock biology of microorganisms. Pearson, New York

    Google Scholar 

  • Mahat R, Seebart C, Basile F, Ward N (2016) Global and targeted lipid analysis of Gemmata obscuriglobus reveals the presence of lipopolysaccharide, a signature of the classical gram- negative outer membrane. J Bacteriol 198:221–236

    Article  CAS  Google Scholar 

  • Margolin W (2005) FtsZ and the division of prokaryotic cells and organelles. Nat Rev Mol Cell Biol 6: 862–871

    Article  CAS  Google Scholar 

  • Martin W, Koonin E (2006) A positive definition of prokaryotes. Nature 442:868

    Article  CAS  Google Scholar 

  • Massana R, Logares R (2013) Eukaryotic versus prokaryotic marine picoplankton ecology. Environ Microbiol 15:1254–1261

    Article  Google Scholar 

  • Mayr E (1998) Two empires or three ? Proc Natl Acad Sci U S A 95:9720–9723

    Article  CAS  Google Scholar 

  • Murat D, Byrne M, Komeili A (2010) Cell biology of prokaryotic organelles. Cold Spring Harb Perspect Biol 2:a000422

    Article  Google Scholar 

  • Nevo R, Charuvi D, Shimoni E, Schwarz R, Kaplan A, Ohad I, Reich Z (2007) Thylakoid membrane perforations and connectivity enable intracellular traffic in cyanobacteria. EMBO J 26:1467–1473

    Article  CAS  Google Scholar 

  • Nevo-Dinur K, Nussbaum-Shochat A, Ben-Yehuda S, Amster-Choder O (2011) Translation-independent localization of mRNA in E. coli. Science 331:1081–1084

    Article  CAS  Google Scholar 

  • Oren A, Garrity G (2014) Then and now: a systematic review of the systematics of prokaryotes in the last 80 years. Antonie Van Leeuwenhoek 106:43–56

    Article  Google Scholar 

  • Orlandini V, Emiliani G, Fondi M, Maida I, Perrin E, Fani R (2014) Network analysis of plasmidomes: The Azospirillum brasilense Sp245 case. Int J Evol Biol:951035

    Google Scholar 

  • Ozyamak E, Kollman J, Komeili A (2013) Bacterial actins and their diversity. Biochemistry 52:6928–6939

    Article  CAS  Google Scholar 

  • Pace N (2006) Time for change. Nature 44:289

    Article  Google Scholar 

  • Pace N (2009a) Problems with “Procaryote”. J Bacteriol 191:2008–2010

    Article  CAS  Google Scholar 

  • Pace N (2009b) Rebuttal: the modern concept of the prokaryote. J Bacteriol 191:2006–2007

    Article  CAS  Google Scholar 

  • Pereira S, Reeve J (1998) Histones and nucleosomes in archaea and eukarya: a comparative analysis. Extremophiles 2:141–148

    Article  CAS  Google Scholar 

  • Petersen MØ, Linnanto J, Frigard N-U, Nielsen N, Miller M (2010) A model of the protein-pigment baseplate complex in chlorosomes of photosynthetic bacteria. Photosynth Res 104:233–243

    Article  Google Scholar 

  • Rappe MS, Connon S, Vergin K, Giovannoni S (2002) Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature 418:630–633

    Article  CAS  Google Scholar 

  • Rosenberg E (2014) The prokaryotes; Alphaproteobacteria and Betaproteobacteria. Springer, Berlin

    Google Scholar 

  • Sagulenko E, Morgan G, Webb R, Yee B, Lee K-C, Fuerst J (2014) Structural studies of Planctomycete Gemmata obscuriglobus support cell compartmentalisation in a bacterium. PLoS One 9:3

    Article  Google Scholar 

  • Saier M, Bogdanov M (2013) Membranous organelles in bacteria. J Mol Microbiol Biotechnol 23:5–12

    Article  CAS  Google Scholar 

  • Samson R, Obita T, Freund S, Williams R, Bell S (2008) A role for the ESCRT system in cell division in archaea. Science 322:1710–1713

    Article  CAS  Google Scholar 

  • Santarella-Mellwig R, Pruggnaller S, Roos N, Mattaj I, Devos D (2013) Three-dimensional reconstruction of bacteria with a complex endomembrane system. PLoS Biol 11:e1001565

    Article  CAS  Google Scholar 

  • Sapp J (2006) Two faces of the prokaryote concept. Int Microbiol 9:163–172

    CAS  PubMed  Google Scholar 

  • Sinninghe DJ, Rijpstra W, Hopmans E, Shouten S, Balk M, Stams AJ (2007) Structural characterization of diabolic acid-based tetraester, tetraether and mixed ether/ester, membrane-spanning lipids of bacteria from the order Thermotogales. Arch Microbiol 188:629–641

    Article  Google Scholar 

  • Sinninghe DJ, Rijpstra W, Hopmans E, Foesel B, Wüst P, Overmann J, Tank M, Bryant D, Dunfield P, Houghton K et al (2014) Ether- and ester-bound iso-diabolic acid and other lipids in members of Acidobacteria subdivision 4. Appl Environ Microbiol 80:5207–5218

    Article  Google Scholar 

  • Soppa J (2014) Evolutionary advantages of polyploidy in halophilic archaea. Biochem Soc Trans 41:339–343

    Article  Google Scholar 

  • Spang A, Saw JH, Jorgensen SL, Zaremba-Niedzwiedzka K, Martijn J, Lind AE, van Eijk R, Schleper C, Guy L, Ettema TJ (2015) Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521:173–179

    Article  CAS  Google Scholar 

  • Stanier R, van Niel C (1962) The concept of a bacterium. Arch Mikrobiol 42:17–35

    Google Scholar 

  • Tindall B, Rosselló-Móra R, Busse H-J, Ludwig W, Kämpfer P (2010) Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 60:249–266

    Article  CAS  Google Scholar 

  • Trachtenberg S, Dorward L, Speransky V, Jaffe H, Andrews S, Leapman R (2008) Structure of the cytoskeleton of Spiroplasma melliferum BC3 and its interactions with the cell membrane. J Mol Biol 378:778–789

    Article  Google Scholar 

  • van der Giezen M (2009) Hydrogenosomes and mitosomes: conservation and evolution of functions. J Eukaryot Microbiol 56: 221–231

    Google Scholar 

  • van Gestel J, Vlamakis H, Kolter R (2015) From cell differentiation to cell collectives: Bacillus subtilis uses division of labor to migrate. PLoS Biol 13:e1002141

    Article  Google Scholar 

  • van Gool A (1972) Ultrastructure of Nitrosomonas europaea cells as revealed by freeze-etching. Archiv Mikrobiol 82:120–127

    Article  Google Scholar 

  • van Niftrik L, Jetten M (2012) Anaerobic ammonium-oxidizing bacteria: unique microorganisms with exceptional properties. Microbiol Mol Biol Rev 76: 585–596

    Article  Google Scholar 

  • van Teeseling MC, de Almeida NM, Klingl A, Speth D, Op den Camp H, Rachel R, Jetten M, van Niftrik L (2013) A new addition to the cell plan of anammox bacteria: “Candidatus Kuenenia stuttgartiensis” has a protein surface layer as the outermost layer of the cell. J Bacteriol 196:80–89

    Article  Google Scholar 

  • Vaulot D, Eikrem W, Viprey M, Moreau H (2008) The diversity of small eukaryotic phytoplankton (< or =3 microm) in marine ecosystems. FEMS Microbiol Rev 32:795–820

    Article  CAS  Google Scholar 

  • Whitman W (2009) The modern concept of the prokaryote. J Bacteriol 191:2000–2020

    Article  CAS  Google Scholar 

  • Woese C (1994) There must be a prokaryote somewhere: microbiology’s search for itself. Microbiol Rev 58:1–9

    CAS  PubMed  PubMed Central  Google Scholar 

  • Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci U S A 74:5088–5090

    Article  CAS  Google Scholar 

  • Zhang R, Chen Y-R, Du H-J, Zhang W-Y, Pan H-M, Xiao T, Wu L-F (2014) Characterization and phylogenetic identification of a species of spherical multicellular magnetotactic prokaryotes that produces both magnetite and greigite crystals. Res Microbiol 165:481–489

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Unité Mixte de Service, UMS 3470, OSU Pythéas, Aix Marseille Université, Marseille Cedex, France

    Jean-Claude Bertrand

  2. Institut des Sciences Analytiques et de Physico-Chimie pour l’Environnement et les Matériaux, UMR 5254, CNRS, Université de Pau et des Pays de l’Adour, Pau, France

    Pierre Caumette

  3. Laboratoire d’Ecologie Microbienne, UMR 5557, Université Claude Bernard Lyon 1, Villeurbanne, France

    Philippe Normand

  4. Aix Marseille Université, Université de Toulon, CNRS, IRD, MIO UM 110, Marseille, France

    Bernard Ollivier

  5. Laboratoire “Microorganismes: Génome et Environnement” (LMGE), CNRS UMR 6023, Université Clermont Auvergne, Clermont-Ferrand, France

    Télesphore Sime-Ngando

Authors
  1. Jean-Claude Bertrand
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pierre Caumette
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Philippe Normand
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bernard Ollivier
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Télesphore Sime-Ngando
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jean-Claude Bertrand .

Editor information

Editors and Affiliations

  1. Unité Mixte de Service, UMS 3470, OSU Pythéas, Aix Marseille Université, Marseille Cedex, France

    Jean-Claude Bertrand

  2. Laboratoire d’Ecologie Microbienne, UMR 5557, Université Claude Bernard Lyon 1, Villeurbanne, France

    Philippe Normand

  3. Aix Marseille Université, Université de Toulon, CNRS, IRD, MIO UM 110, Marseille, France

    Bernard Ollivier

  4. Laboratoire “Microorganismes: Génome et Environnement” (LMGE), CNRS UMR 6023, Université Clermont Auvergne, Clermont-Ferrand, France

    Télesphore Sime-Ngando

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Bertrand, JC., Caumette, P., Normand, P., Ollivier, B., Sime-Ngando, T. (2018). Prokaryote/Eukaryote Dichotomy and Bacteria/Archaea/Eukarya Domains: Two Inseparable Concepts. In: Bertrand, JC., Normand, P., Ollivier, B., Sime-Ngando, T. (eds) Prokaryotes and Evolution. Springer, Cham. https://doi.org/10.1007/978-3-319-99784-1_1

Download citation

Publish with us

Policies and ethics

Search

Navigation