Skip to main content Accessibility help
  • Get access
    Check if you have access via personal or institutional login
  • Cited by 9
  • Print publication year: 2011
  • Online publication date: August 2012

6 - Everything is everywhere: a twenty-first century de-/reconstruction with respect to protists

from Part III - Unicellular eukaryotes



The aphorism ‘Everything is everywhere, but the environment selects’ asserts that microbial taxa are found anywhere on earth that there is suitable habitat for them. It was crystallised in this form by Baas Becking (1934), who was in turn inspired by the ideas of Beijerinck (1913). The history of its establishment has been nicely summarised by O'Malley (2007) and its incorporation into contemporary thought described by de Wit and Bouvier (2006). It was further contextualised in terms of free-living protists by Fenchel and Finlay (2004). This concept (which we refer to hereafter as EiE) has recently been the focus of much heated debate in microbiology and protistology. This chapter will reassess the fundamental principles behind the EiE concept with respect to free-living protists in the light of recent findings and insights from twenty-first century molecular biology and microbial ecology. We do not intend to provide a survey of studies/taxa that apparently do or do not meet its predictions; work in this field is proceeding rapidly and such a survey would soon become obsolete. The studies cited here were not selected because we agree or disagree particularly strongly with them, but because they illustrate points of our discussion.

Amato, A., Kooistra, W.H., Ghiron, J.H. et al. (2007). Reproductive isolation among sympatric cryptic species in marine diatoms. Protist 158, 193–207.
Baas Becking, L.G.M. (1934). Geobiologie of inleiding tot de milieukunde. The Hague: Van Stockum and Zoon.
Barth, D., Krenek, S., Fokin, S.I., Berendonk, T.U. (2006). Intraspecific genetic variation in Paramecium revealed by mitochondrial cytochrome c oxidase I sequences. Journal of Eukaryotic Microbiology 53, 20–25.
Bass, D., Cavalier-Smith, T. (2004). Phylum-specific environmental DNA analysis reveals remarkably high global biodiversity of Cercozoa (Protozoa). International Journal of Systematic and Evolutionary Microbiology 54, 2393–2404.
Bass, D., Richards, T.A., Matthai, L., Marsh, V., Cavalier-Smith, T. (2007). DNA evidence for global dispersal and probable endemicity of protozoa. BMC Evolutionary Biology 7, 162.
Bass, D., Howe, A.T., Mylnikov, A.P. et al. (2009a). Phylogeny and classification of Cercomonadida: Cercomonas, Eocercomonas, Paracercomonas, and Cavernomonas gen. n. Protist 160, 483–521.
Bass, D., Chao, E.E., Nikolaev, S. et al. (2009b). Phylogeny of novel naked filose and reticulose Cercozoa: Granofilosea cl. n. and Proteomyxidea revised. Protist 160, 75–109.
Bass, D., Brown, N., Mackenzie-Dodds, J. et al. (2009c). A molecular perspective on ecological differentiation and biogeography of cyclotrichiid ciliates. Journal of Eukaryotic Microbiology 56, 559–567.
Beijerinck, M.W. (1913). De infusies en de ontdekking der backteriën. Jaarboek van de Koninklijke Akademie voor Wetenschappen. Amsterdam: Müller. (Preprinted in Verzamelde geschriften van M.W. Beijerinck, vijfde deel, pp. 119–140. Delft, 2921).
Berney, C., Fahrni, J., Pawlowski, J. (2004). How many novel eukaryotic ‘kingdoms’? Pitfalls and limitations of environmental DNA surveys. BMC Biology 2, 13.
Boenigk, J. (2008a). Nanoflagellates: functional groups and intraspecific variation. Denisia 23, 331–335.
Boenigk, J. (2008b). The past and present classification problem with nanoflagellates exemplified by the genus Monas. Protist 159, 319–337.
Boenigk, J., Pfandl, K., Stadler, P., Chatzinotas, A. (2005). High diversity of the ‘Spumella-like’ flagellates: an investigation based on the SSU rRNA gene sequences of isolates from habitats located in six different geographic regions. Environmental Microbiology 7, 685–697.
Boenigk, J., Pfandl, K., Garstecki, T. et al. (2006). Evidence for geographic isolation and signs of endemism within a protistan morphospecies. Applied and Environmental Microbiology 72, 5159–5164.
Boenigk, J., Jost, S., Stoeck, T., Garstecki, T. (2007). Differential thermal adaptation of clonal strains of a protist morphospecies originating from different climatic zones. Environmental Microbiology 9, 593–602.
Buée, M., Reich, M., Murat, C. et al. (2009). 454 pyrosequencing analyses of forest soils reveals an unexpectedly high fungal diversity. New Phytologist 184, 449–456.
Caron, D.A. (2009). Past President's address: protistan biogeography: why all the fuss?Journal of Eukaryotic Microbiology 56, 105–112.
Cavalier-Smith, T. (2004). Only six kingdoms of life. Proceedings of the Royal Society of London B Biological Sciences 271, 1251–1262.
Chao, A., Li, P.C., Agatha, S. et al. (2006). A statistical approach to estimate soil ciliate diversity and distribution based on data from five continents. Oikos 114, 479–493.
Coesel, P.F.M., Krienitz, L. (2008). Diversity and geographic distribution of desmids and other coccooid green algae. Biodiversity and Conservation 17, 381–392.
Coleman, A.W. (2007). Pan-eukaryote ITS2 homologies revealed by RNA secondary structure. Nucleic Acids Research 35, 3322–3329.
Corliss, J.O. (2000). Biodiversity, classification, and numbers of species of protists. In Raven, P.H., Williams, T. (eds.), Nature and Human Society. The Quest for a Sustainable World, pp. 130–155. Washington, DC: National Academy Press.
Countway, P.D., Gast, R.J., Savai, P., Caron, D.A. (2005). Protistan diversity estimates based on 18S rDNA from seawater incubations in the western North Atlantic. Journal of Eukaryotic Microbiology 52, 95.
Creer, S., Fonseca, V.G., Porazinska, D.L. et al. (2010). Ultrasequencing of the meiofaunal biosphere: practice, pitfalls and promises. Molecular Ecology 19, 4–20.
Darling, K.F., Wade, C.M., Stewart, I.A. et al. (2004). Molecular evidence for genetic mixing of Arctic and Antarctic subpolar populations of planktonic foraminifers. Nature 405, 43–47.
Darling, K.F., Kucera, M., Wade, C.M. (2007). Global molecular phylogeography reveals persistent Arctic circumpolar isolation in marine planktonic protist. Proceedings of the National Academy of Sciences USA 104, 5002–5007.
Darling, K.F., Wade, C.M. (2008). The genetic diversity of planktic foraminifera and the global distribution of ribosomal RNA genotypes. Marine Micropaleontology 67, 216–238.
Jonckheere, J.F. (1998). Sequence variation in the ribosomal internal transcribed spacers, including the 5.8S rDNA, of Naegleria spp. Protist 149, 221–228.
Wit, R., Bouvier, T. (2006). ‘Everything is everywhere, but the environment selects’; what did Baas Becking and Beijerinck really say?Environmental Microbiology 8, 755–758.
Fenchel, T., Finlay, B.J. (2004). The ubiquity of small species: patterns of local and global diversity. BioScience 54, 777–784.
Fierer, N. (2008). Microbial biogeography: patterns in microbial diversity across space and time. In Zengler, K. (ed.), Accessing Uncultivated Microorganisms: from the Environment to Organisms and Genomes and Back, pp. 95–115. Washington, DC: ASM Press.
Finlay, B.J. (2002). Global dispersal of free-living microbial eukaryote species. Science 296, 1061–1063.
Finlay, B.J. (2004). Protist taxonomy: an ecological perspective. Philosophical Transactions of the Royal Society of London B 359, 599–610.
Finlay, B.J., Clarke, K.J. (1999). Apparent global ubiquity of species in the protist genus Paraphysomonas. Protist 150, 419–430.
Finlay, B.J., Fenchel, T. (1999). Divergent perspectives on protist species richness. Protist 150, 229–233.
Finlay, B.J., Fenchel, T. (2004). Cosmopolitan metapopulations of free-living microbial eukayotes. Protist 155, 237–244.
Finlay, B.J., Corliss, J.O., Esteban, G., Fenchel, T. (1996). Biodiversity at the microbial level: the number of free-living ciliates in the biosphere. Quaternary Review of Biology 71, 221–237.
Finlay, B.J., Esteban, G.F., Brown, S., Fenchel, T., Hoef-Emden, K. (2006). Multiple cosmopolitan ecotypes within a microbial eukaryote morphospecies. Protist 157, 377–390.
Foissner, W. (1999). Protist diversity: estimates of the near-imponderable. Protist 150, 363–368.
Foissner, W. (2004a). Ubiquity and cosmopolitanism of protists questioned. SIL News 43, 6–7.
Foissner, W. (2004b). Two new “flagship” ciliates (Protozoa. Ciliophora) from Venezuela: Sleighophrys pustulata and Luporinophrys micelae. European Journal of Protistology 41, 99–117.
Foissner, W. (2006). Biogeography and dispersal of micro-organisms: a review emphasizing protists. Acta Protozoologica 45, 111–136.
Foissner, W. (2008). Protist diversity and distribution: some basic considerations. Biodiversity and Conservation 17, 235–242.
Foissner, W., Strüde-Kypke, M., Staay, G.W.M., Moon-van der Staay, S.-Y., Hackstein, J.H.P. (2003). Endemic ciliates (Protozoa, Ciliophora) from tank bromeliads (Bromeliaceae): a combined morphological, molecular, and ecological study. European Journal of Protistology 39, 365–372.
Fontaneto, D., Barraclough, T.G., Chen, K., Ricci, C., Herniou, E.A. (2008). Molecular evidence for broad-scale distributions in bdelloid rotifers: everything is not everywhere but most things are very widespread. Molecular Ecology 17, 3136–3146.
Foulon, E., Not, F., Jalabert, F. et al. (2008). Ecological niche partitioning in the picoplanktonic green alga Micromonas pusilla: evidence from environmental surveys using phylogenetic probes. Environmental Microbiology 10, 2433–2443.
Frezal, L., Leblois, R. (2008). Four years of DNA barcoding: current advances and prospects. Infection Genetics and Evolution 8, 727–736.
Gilbert, J.A., Field, D., Swift, P. et al. (2009). The seasonal structure of microbial communities in the Western English Channel. Environmental Microbiology 11, 3132–3139.
Guillou, L., Eikrem, W., Chrétiennot-Dinet, M.J. et al. (2004) Diversity of picoplanktonic prasinophytes assessed by direct nuclear SSU rDNA sequencing of environmental samples and novel isolates retrieved from oceanic and coastal marine ecosystems. Protist 155, 193–214.
Habura, A., Pawlowski, J., Hanes, S.D., Bowser, S.S. (2004). Unexpected foraminiferal diversity revealed by small-subunit rDNA analysis of Antarctic sediment. Journal of Eukaryotic Microbiology 51, 173–179.
Hoef-Emden, K. (2007). Revision of the genus Cryptomonas (Cryptophyceae) II: incongruences between the classical morphospecies concept and molecular phylogeny in smaller pyrenoid-less cells. Phycologia 46, 402–428.
Hoef-Emden, K. (2008). Molecular phylogeny of phycocyanin-containing cryptophytes: evolution of biliproteins and geographical distribution. Journal of Phycology 44, 985–993.
Howe, A.T., Bass, D., Vickerman, K., Chao, E.E., Cavalier-Smith, T. (2009). Phylogeny, taxonomy, and astounding genetic diversity of Glissomonadida ord. nov., the dominant gliding zooflagellates in soil (Protozoa: Cercozoa). Protist 160, 159–189.
Hughes Martiny, J.B., Bohannan, B.J.M., Brown, J.H. et al. (2006). Microbial biogeography: putting microorganisms on the map. Nature Reviews Microbiology 4, 102–112.
Johnson, M.D., Tengs, T., Oldach, D.W., Delwiche, C.F., Stoecker, D.K. (2004). Highly divergent SSU rRNA genes found in the marine ciliates Myrionecta rubra and Mesodinium pulex. Protist 155, 347–359.
Kemp, P.F., Aller, J.Y. (2004). Estimating prokaryotic diversity: when are 16S rDNA libraries large enough?Limnology and Oceanography: Methods 2, 114–125.
Koch, T.A., Ekelund, F. (2005). Strains of the heterotrophic flagellate Bodo designis from different environments vary considerably with respect to salinity preference and SSU rRNA gene composition. Protist 156, 97–112.
Kristiansen, J. (2008). Dispersal and biogeography of silica-scaled chrysophytes. Biological Conservation 17, 419–426.
Lawton, J.H. (2004). Japan Prize commemorative lecture: biodiversity, conservation and sustainability. Notes and Records of the Royal Society of London 58, 321–333.
Leclerc, M.C., Barriel, V., Lecointre, G., Reviers, B. (1998). Low divergence in rDNA ITS sequences among five species of Fucus (Phaeophyceae) suggests a very recent radiation. Journal of Molecular Evolution 46, 115–120.
Lilly, E.L., Halanych, K.M., Anderson, D.M. (2007). Species boundaries and global biogeography of the Alexandrium tamarense complex (Dinophyceae). Journal of Phycology 43, 1329–1338.
Logares, R., Rengefors, K., Kremp, A. et al. (2007). Phenotypically different microalgal morphospecies with identical ribosomal DNA: a case of rapid adaptive evolution?Microbial Ecology 53, 549–561.
Logares, R., Boltovskoy, A., Bensch, S., Laybourn-Parry, J., Rengefors, K. (2009). Genetic diversity patterns in five protist species occurring in lakes. Protist 160, 301–317.
Lowe, C.D., Day, A., Kemp, S.J., Montagnes, D.J.S. (2005). There are high levels of functional and genetic diversity in Oxyrrhis marina. Journal of Eukaryotic Microbiology 52, 250–257.
Medinger, R., Nolte, V., Vinay Pandey, R. et al. (2010). Diversity in a hidden world: potential and limitation of next-generation sequencing for surveys of molecular diversity of eukaryotic microorganisms. Molecular Ecology 19, 32–40.
Mindell, D.P., Honeycutt, R.L. (1990). Ribosomal RNA in vertebrates: evolution and phylogenetic applications. Annual Review of Ecology and Systematics 21, 541–566.
Mitchell, E.A.D., Meisterfeld, C. (2005). Taxonomic confusion blurs the debate on cosmopolitanism versus local endemism of free-living protists. Protist 156, 263–267.
Moreira, D., López-García, P. (2002). The molecular ecology of microbial eukaryotes unveils a hidden world. Trends in Microbiology 10, 31–38.
Müller, T., Philippi, N., Dandekar, T., Schultz, J., Wolf, M. (2007). Distinguishing species. RNA 13, 1469–1472.
Nanney, D.L., Park, C., Preparata, R., Simon, E.M. (1998). Comparison of sequence differences in a variable 23S rRNA domain among sets of cryptic species of ciliated protozoa. Journal of Eukaryotic Microbiology 45, 91–100.
Nikolaev, S.I., Berney, C., Fahrni, J.F. et al. (2004). The twilight of Heliozoa and rise of Rhizaria, an emerging supergroup of amoeboid eukaryotes. Proceedings of the National Academy of Sciences USA 101, 8066–8071.
Nolte, V., Pandey, R.V., Jost, S. et al. (2010). Contrasting seasonal niche separation between rare and abundant taxa conceals the extent of protist diversity. Molecular Ecology 79, 2908–2915.
O'Malley, M.A. (2007). The nineteenth-century roots of ‘everything is everywhere’. Nature Reviews Microbiology 5, 647–651.
Pawlowski, J., Berney, C. (2003). Episodic evolution of nuclear small subunit ribosomal RNA gene in the stem-lineage of Foraminifera. In Donoghue, P.C.J., Smith, M.P. (eds.), Telling the Evolutionary Time: Molecular Clocks and The Fossil Record, pp. 107–118. Systematics Association special volume 66. London: Taylor and Francis.
Pedrós-Alió, C. (2006). Marine microbial diversity: can it be determined?Trends in Microbiology 14, 257–263.
Pfandl, K., Chatzinotas, A., Dyal, P., Beonigk, J. (2009). SSU rRNA gene variation resolves population heterogeneity and ecophysiological differentiation within a morphospecies (Stramenopiles, Chrysophyceae). Limnology and Oceanography 54, 171–181.
Pither, J. (2007). Comment on “Dispersal limitations matter for microbial morphospecies”. Science 316, 1124. Author reply 1124.
Przybos, E., Tarcz, S., Fokin, S. (2009). Molecular polymorphism of Paramecium tetraurelia (Ciliophora, Protozoa) in strains originating from difference continents. Folia Biologica 57, 57–63.
Richards, T.A., Bass, D. (2005). Molecular screening of free-living microbial eukaryotes: diversity and distribution using a meta-analysis. Current Opinion in Microbiology 8, 240–253.
Richards, T.A., Dacks, J.B., Jenkinson, J.M., Thornton, C.R., Talbot, N.J. (2006). Evolution of filamentous plant pathogens: Gene exchange across eukaryotic kingdoms. Current Biology 16, 1857–1864.
Rodriguez Zaragoza, S., Mayzlish, E., Steinberger, Y. (2005). Seasonal changes in free-living amoeba species in the root canopy of Zygophyllum dumosum in the Negev Desert, Israel. Microbial Ecology 49, 134–141.
Scheckenbach, F., Wylezich, C., Mylnikov, A.P., Weitere, M., Arndt, H. (2006). Molecular comparisons of freshwater and marine isolates of the same morphospecies of heterotrophic flagellates. Applied and Environmental Microbiology 72, 6638–6643.
Simon, E.M., Nanney, D.L., Doerder, F.P. (2008). The “Tetrahymena pyriformis” complex of cryptic species. Biodiversity and Conservation 17, 365–380.
Slapeta, J., Moreira, D., López-García, P. (2005). The extent of protist diversity: insights from molecular ecology of freshwater eukaryotes. Proceedings of the Royal Society of London B 272, 2073–2081.
Slapeta, J., López-García, P., Moreira, D. (2006). Global dispersal and ancient cryptic species in the smallest marine eukaryotes. Molecular Biology and Evolution 23, 23–29.
Smirnov, A.V. (2003). Optimizing methods of the recovery of gymnamoebae from environmental samples: a test of ten popular enrichment media, with some observations on the development of cultures. Protistology 3, 47–57.
Smith, H.G., Wilkinson, D.M. (2007). Not all free-living microorganisms have cosmopolitan distributions – the case of Nebela (Apodera) vas Certes (Protozoa: Amoebozoa: Arcellinida). Journal of Biogeography 34, 1822–1831.
Smith, H.G., Bobrov, A., Lara, E., (2008). Diversity and biogeography of testate amoebae. Biodiversity and Conservation 17, 329–343.
Sogin, M., Morrison, H.G., Huber, J.A. et al. (2006). Microbial diversity in the deep sea and underexplored “rare biosphere”. Proceedings of the National Academy of Sciences USA 103, 12115–12120.
Stoeck, T., Hayward, B., Taylor, G.T., Varela, R., Epstein, S.S. (2006). A multiple PCR primer approach to access the microeukaryotic diversity in environmental samples. Protist 157, 31–43.
Stoeck, T., Bruemmer, F., Foissner, W. (2007a). Evidence for local ciliate endemism in an Alpine anoxic lake. Microbial Ecology 54, 478–486.
Stoeck, T., Zuendorf, A., Breiner, H.-W., Behnke, A. (2007b). A molecular approach to identify active microbes in environmental eukaryote clone libraries. Microbial Ecology 53, 328–339.
Stoeck, T., Bass, D., Nebel, M. et al. (2010). Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Molecular Ecology 19 (s1), 21–31.
Telford, R.J., Vandvik, V., Birks, H.J. (2006). Dispersal limitations matter for microbial morphospecies. Science 312, 1015.
Thackeray, S.J., Jones, I.D., Maberly, S.C. (2008). Long-term change in the phenology of spring phytoplankton: species-specific responses to nutrient enrichment and climate change. Journal of Ecology 96, 523–535.
Vanormelingen, P., Verleyen, E., Vyverman, W. (2008). The diversity and distribution of diatoms: from cosmopolitanism to narrow endemism. Biodiversity and Conservation 17, 393–405.
der Heyden, S., Chao, E.E., Cavalier-Smith, T. (2004). Genetic diversity of goniomonads: an ancient divergence between marine and freshwater species. European Journal of Phycology 39, 343–350.
der Heyden, S., Cavalier-Smith, T. (2005). Culturing and environmental DNA sequencing uncover hidden kinetoplastid biodiversity and a major marine clade within ancestrally freshwater Neobodo designis. International Journal of Systematics and Evolutionary Microbiology 55, 2605–2621.
Vyverman, W., Verleyen, E., Sabbe, K. et al. (2007). Historical processes constrain patterns in global diatom diversity. Ecology 88, 1924–1931.
Ward, R.D., Hanner, R., Hebert, P.D.N. (2009). The campaign to DNA barcode all fishes. Journal of Fish Biology 74, 329–356.
Wilkinson, D.M. (2010). Have we underestimated the importance of humans in the biogeography of free-living terrestrial microorganisms?Journal of Biogeography 37, 393–397.
Worden, A.Z. (2006). Picoeukaryote diversity in coastal waters of the Pacific Ocean. Aquatic Microbial Ecology 43, 165–175.
Wuyts, J., Rijk, P., Peer, Y. et al. (2000). Comparative analysis of more than 3000 sequences reveals the existence of two pseudoknots in area V4 of eukaryotic small subunit ribosomal RNA. Nucleic Acids Research 28, 4698–4708.
Wylezich, C., Mylnikov, A.P., Weitere, M., Arndt, H. (2007). Distribution and phylogenetic relationships of freshwater thaumatomonads with a description of the new species Thaumatomonas coloniensis n. sp. Journal of Eukaryotic Microbiology 54, 347–357.
Yang, J., Smith, H.G., Sherratt, T.N., Wilkinson, D.M. (2010). Is there a size limit for cosmopolitan distribution in free-living microorganisms? A biogeographical analysis of testate amoebae from polar areas. Microbial Ecology 59, 635–645.