Skip to main content

Protistan Skeletons: A Geologic History of Evolution and Constraint

  • Chapter
  • First Online:
Evolution of Lightweight Structures

Part of the book series: Biologically-Inspired Systems ((BISY,volume 6))

Abstract

The tests and scales formed by protists may be the epitome of lightweight bioconstructions in nature. Skeletal biomineralization is widespread among eukaryotes, but both predominant mineralogy and stratigraphic history differ between macroscopic and microscopic organisms. Among animals and macroscopic algae, calcium minerals, especially carbonates, predominate in skeleton formation, with most innovations in skeletal biomineralization concentrated in and around the Cambrian Period. In contrast, amorphous silica is widely used in protistan skeletons, and a majority of the geologically recorded origins of silica biomineralization took place in the Mesozoic and early Cenozoic eras. Amorphous silica may be favored in protist biomineralization because of the material properties of both silica itself and the organic molecules that template its precipitation. The predominace of carbonates and phosphates in macroscopic skeletons may, in turn, reflect the low quantities of dissolved silica in fresh and marine waters. The evolutionary success of diatoms has depleted silica levels in surficial waters since the Cretaceous Period, and fossils show that other biological participants in the silica cycle have responded both through altered habitat preferences and reduced use of silica in test construction. These natural instances of doing more with less might serve to inspire continuing innovations in biomimetic design.

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

Access this chapter

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
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

Similar content being viewed by others

References

  • Allison CW, Hilgert JW (1986) Scale microfossils from the early Cambrian of northwest Canada. J Paleontol 60:973–1015

    Google Scholar 

  • Andersen RA (2004) Biology and systematics of heterokont and haptophyte algae. Amer J Bot 91:1508–1522

    Article  Google Scholar 

  • Anderson OR (1983) Radiolaria. Springer, New York

    Book  Google Scholar 

  • Antcliffe JB, Callow RHT, Brasier MD (2014) Giving the early fossil record of sponges a squeeze. Biol Rev. doi:10.1111/brv.12090

    Google Scholar 

  • Armstrong H, Brasier M (2005) Microfossils. Blackwell Publishing, Malden

    Google Scholar 

  • Barron J, Baldauf J (1995) Cenozoic marine diatom biostratigraphy and applications to paleoclimatology and paleoceanography. (In: Blome CD, Whalen PM, Reed KM (eds) Siliceous Microfossils.) Paleontol Soc Short Courses Paleontol 8:107–118

    Google Scholar 

  • Bengtson S, Conway Morris S (1992) Early radiation of biomineralizing phyla. In: Lipps JH, Signor PW (eds) Origin and early evolution of the Metazoa. Plenum, New York, pp 447–481

    Google Scholar 

  • Bentov S, Brownlee C, Erez J (2009) The role of seawater endocytosis in the biomineralization process in calcareous foraminifera. Proc Nat Acad Sci USA 51:21500–21504

    Article  Google Scholar 

  • Bentov S, Zaslansky P, Al-Sawalmih A et al (2012) Enamel-like apatite crown covering amorphous mineral in a crayfish mandible. Nature Comm 3:839. doi:10.1038/ncomms1839

    Article  Google Scholar 

  • Berney C, Pawlowski J (2006) A molecular time-scale for eukaryote evolution recalibrated with the continuous microfossil record. Proc R Soc Lond Ser B 273:1867–1872

    Article  Google Scholar 

  • Brown JW, Sorhannus U (2010) A molecular genetic timescale for the diversification of autotrophic stramenopiles (Ochrophyta): Substantive underestimation of putative fossil ages. PLOS ONE 5(9). doi:10.1371/journal.pone.0012759

    Google Scholar 

  • Bukry D (1981) Synthesis of silicoflagellate stratigraphy for Maestrichtian to Quaternary marine sediment. Soc of Econ Paleont Min Spec Pub 32:433–444

    Google Scholar 

  • Burki F, Shalchian-Tabrizi K, Pawlowski J (2008) Phylogenomics reveals a new ‘megagroup’ including most photosynthetic eukaryotes. Biology Lett 4:366–369

    Article  Google Scholar 

  • Carrera MG, Botting JR (2008) Evolutionary history of cambrian spiculate sponges: implications for the Cambrian evolutionary fauna. Palaios 23:124–138

    Article  Google Scholar 

  • Creveling JC, Knoll AH, Fernández Remolar D et al (2013) Geobiology of a Lower Cambrian carbonate platform, Pedroche Formation, Spain. Palaeogeogr Palaeoclimatol Palaeoecol 386:459–478

    Article  Google Scholar 

  • Cohen PA, Knoll AH (2012) Neoproterozoic scale microfossils from the Fifteen Mile Group, Yukon Territory. J Paleontol 86:775–800

    Article  Google Scholar 

  • Cohen PA, Schopf JW, Butterfield NJ et al (2011) Phosphate biomineralization in mid-Neoproterozoic protists. Geology 39:539–542

    Article  Google Scholar 

  • Cuif J-P, Dauphin Y, Sorauf JE (2011) Biominerals and fossils through time. Cambridge University Press, Cambridge

    Google Scholar 

  • Debrenne F (2007) Lower Cambrian archaeocyathan bioconstructions. Comptes Rendus Palevol 6:5–19

    Article  Google Scholar 

  • Decelle J, Suzuki N, Mahe F et al (2012) Molecular phylogeny and morphological evolution of the Acantharia (Radiolaria). Protist 163:435–450

    Article  Google Scholar 

  • Decelle J, Martin P, Paborstava K et al (2013) Diversity, ecology and biogeochemistry of cyst-forming Acantharia (Radiolaria) in the oceans. PLoS ONE 8:(Article Number)e53598

    Article  Google Scholar 

  • De Decker P (2004) On the celestite-secreting Acantharia and their effects on seawater strontium to calcium ratios. Hydrobiologia 517:1–13

    Article  Google Scholar 

  • Domozych D, Wells B, Shaw P (1991) Basket scales of the green-alga, Mesostigma viride—chemistry and ultrastructure. J Cell Sci 100:397–407

    Google Scholar 

  • Ehrlich H (2010) Chitin and collagen as universal and alternative templates in biomineralization. Int Geol Rev 52:661–699

    Article  Google Scholar 

  • Erez J (2003) The source of ions for biomineralization in foraminifera and their implications for paleoceanographic proxies. Rev Mineral Geochem 54:115–149

    Article  Google Scholar 

  • Ernissee JJ, McCartney K (1992) Ebridians. In: Lipps JH (ed) Fossil prokaryotes and protists. Blackwell Scientific, Oxford, pp 131–140

    Google Scholar 

  • Falkowski P, Knoll H (eds) (2007) The evolution of primary producers in the sea. Elsevier, Burlington

    Google Scholar 

  • Falkowski PG, Katz ME, Knoll AH et al (2004) The evolution of modern eukaryotic phytoplankton. Science 305:354–360

    Article  Google Scholar 

  • Finkel ZV, Kotrc B (2010) Silica use through time: macroevolutionary change in the morphology of the diatom fustule. Geomicrobiol J 27:596–608

    Article  Google Scholar 

  • Finkel ZV, Matheson KA, Regan KS et al (2010) Genotypic and phenotypic variation in diatom silicification under paleo-oceanographic conditions. Geobiology 8:433–445

    Article  Google Scholar 

  • Foissner W, Weissenbacher B, Krautgartner W-D et al (2009) A cover of glass: first report of biomineralized silicon in a ciliate, Maryna umbrellata (Ciliophora: Colpodea). J Euk Microbiol 56:519–530

    Article  Google Scholar 

  • Fowler S, Fisher N (1983) Viability of marine phytoplankton in zooplankton fecal pellets. Deep-Sea Res 30:963–969

    Article  Google Scholar 

  • Frankel RB, Bazylinski DA, Schüler D (1998) Biomineralization of magnetic iron minerals in magnetotactic bacteria. J. Supramol Sci 5:383–390

    Article  Google Scholar 

  • Gong N, Wiens M, Schröder HC et al (2010) Biosilicification of loricate choanoflagellate: organic composition of the nanotubular siliceous costal strips of Stephanoeca diplocostata. J Exp Biol 213:3575–3585

    Article  Google Scholar 

  • Gordon R, Losic D, Tiffany MA et al (2009) The glass menagerie: diatoms for novel applications in nanotechnology. Trends Biotechnol 27:116–127

    Article  Google Scholar 

  • Grenne, T, Slack, JF (2003) Paleozoic and Mesozoic silica-rich seawater: evidence from hematitic chert (jasper) deposits. Geology 31:319–322

    Article  Google Scholar 

  • Grotzinger JP, Watters, Knoll AH (2000) Calcareous metazoans in thrombolitic bioherms of the terminal Proterozoic Nama Group, Namibia. Paleobiology 26:334–359

    Google Scholar 

  • Groussin M, Pawlowski J, Yang Z (2011) Bayesian relaxed clock estimation of divergence times in foraminifera. Mol Phyl Evol 61:157–166

    Article  Google Scholar 

  • Haeckel E (1887) Report on the Radiolaria collected by H.M.S. Challenger during the years 1873–1876. Rep Sci Results, Challenger, Zool. 18:clxxxviii + 1803 p

    Google Scholar 

  • Hamm CE (2005) The evolution of advanced mechanical defenses and potential technological applications of diatom shells. J Nanosci Nanotechnol 5:108–199

    Article  Google Scholar 

  • Hamm CE, Merkel R, Springer O et al (2003) Architecture and material properties of diatom shells provide effective mechanical protection. Nature 421:841–843

    Article  Google Scholar 

  • Harper HE Jr, Knoll AH (1975) Silica, diatoms, and Cenozoic radiolarian evolution. Geology 3:175–177

    Article  Google Scholar 

  • Hedley R, Ogden C, Mordan N (1977) Biology and fine structure of Cryptodifflugia oviformis (Rhizopdea: Protozoa). Bull Br Mus Nat Hist (Zool.) 30:313–328

    Google Scholar 

  • Hildebrand M (2000) Silicic acid transport and its control during cell wall silicification in diatoms. In: Bäuerlein E (ed) Biomineralization. Springer, Weinheim, pp 171–188

    Google Scholar 

  • Hoppenrath M, Leander BS (2006) Ebriid phylogeny and the expansion of the Cercozoa. Protist 157:279–290

    Article  Google Scholar 

  • Knoll AH (1994) Proterozoic and Early Cambrian protists: evidence for accelerating evolutionary tempo. Proc Nat Acad Sci USA 91:6743–6750

    Article  Google Scholar 

  • Knoll AH (2003) Biomineralization and evolutionary history. Rev Mineral Geochem 54:329–356

    Article  Google Scholar 

  • Knoll AH (2013) Systems paleobiology. Geol Soc Am Bull 125:3–13

    Article  Google Scholar 

  • Knoll AH, Fischer WW (2011) Skeletons and ocean chemistry: the long view. In: Gattuso JP, Hansson L (eds) Ocean acidification. Oxford University Press, Oxofrd, pp 67–82

    Google Scholar 

  • Konhauser KO, Riding R (2012) Bacterial biomineralization. In: Knoll AH, Canfield DE, Konhauser KO (eds) Fundamentals of geobiology. Wiley-Blackwell, Chichester, pp 105–130

    Book  Google Scholar 

  • Kooistra WHCF, Gersonde R, Medlin LK et al (2007) The origin and evolution of the diatoms: their adaptation to a planktonic existence. In: Falkowski P, Knoll AH (eds) The evolution of primary producers in the sea. Elsevier, Burlington, pp 207–249

    Google Scholar 

  • Krabberød AK, Brate J, Dolven JK et al (2011) Radiolaria divided into Polycystina and Spasmaria in combined 18S and 28S rDNA phylogeny. PLoS ONE 6:e23526

    Article  Google Scholar 

  • Kröger N, Poulsen N (2008) Diatoms-from cell wall biogenesis to nanotechnology. Ann Rev Genet 42:83–107

    Article  Google Scholar 

  • Kröger N, Sumper M (2004) Silica formation in diatoms: the function of long-chain polyamines and silaffins. J Mater Chem 14:2059–2065

    Article  Google Scholar 

  • Kunitomo Y, Sarashina I, Iijima M et al (2006) Molecular phylogeny of acantharian and polycystine radiolarians based on ribosomal DNA sequences, and some comparisons with data from the fossil record. European J Protistol 42:143–153

    Article  Google Scholar 

  • Lazarus DB, Kotrc B, Wulf G et al (2009) Radiolarians decreased silicification as an evolutionary response to reduced Cenozoic ocean silica availability. Proc Nat Acad Sci USA 106:9333–9338

    Article  Google Scholar 

  • Lipps JH (1973) Test structure in Foraminifera. Ann Rev Microbiol 27:471–488

    Article  Google Scholar 

  • Maldonado M, Carmona MC, Uriz MJ et al (1999) Decline in Mesozoic reef-building sponges explained by silicon limitation. Nature 401:785–788

    Article  Google Scholar 

  • Maldonado M, Riesgo A, Bucci A et al (2010) Revisiting silicon budgets at a tropical continental shelf: Silica standing stocks in sponges surpass those in diatoms. Limnol Oceanogr 55:2001–2010

    Article  Google Scholar 

  • Maldonado M, Navarro L, Grasa A et al (2011) Silicon uptake by sponges: a twist to understanding nutrient cycling on continental margins. Nature Sci Rep 1:1–8

    Google Scholar 

  • Maldonado M, Cao H, Cao X et al (2012) Experimental silicon demand by the sponge Hymeniacidon perlevis reveals chronic limitation in field populations. Hydrobiologia 687:251–257

    Article  Google Scholar 

  • Maliva R, Knoll AH, Siever R (1989) Secular change in chert distribution: a reflection of evolving biological participation in the silica cycle. Palaios 4:519–532

    Article  Google Scholar 

  • Maloof AC, Porter SM, Moore JL et al (2010) The earliest Cambrian record of animals and ocean geochemical change. Geol Soc Am Bull 122:1731–1774

    Article  Google Scholar 

  • Marron AO, Alston MJ, Heavens D, Akam M, Caccamo M, Holland PWH, Walker G (2013) A family of diatom-like silicon transporters in the siliceous loricate choanoflagellates. Proc Roy Soc Biol Sci 280:20122543

    Google Scholar 

  • Marsh ME (2003) Regulation of CaCO3 formation in coccolithophores. Comp Biochem Physiol B Biochem Mol Biol 136:743–754

    Article  Google Scholar 

  • Matsuoka A (2007) Living radiolarian feeding mechanisms: new light on past marine ecosystems. Swiss J Geosci 100:273–279

    Article  Google Scholar 

  • McIlroy D, Green OR, Brasier MD (2001) Palaeobiology and evolution of the earliest agglutinated Foraminifera: Platysolenites, Spirosolenites and related forms. Lethaia 34:13–29

    Article  Google Scholar 

  • Müller WEG, Li J, Schröder HC et al (2007) The unique skeleton of siliceous sponges (Porifera; Hexactinellida and Demospongiae) that evolved first from the Urmetazoa during the Proterozoic: a review. Biogeosciences 4:219–232

    Article  Google Scholar 

  • Parfrey LW, Grant J, Tekle YI et al (2010) Broadly sampled multigene analyses yield a well- resolved eukaryotic tree of life. Syst Biol 59:518–533

    Article  Google Scholar 

  • Park T-Y, Woo J, Lee D-J et al (2011) A stem-group cnidarian described from the mid-Cambrian of China and its significance for cnidarian evolution. Nature Comm. doi:10.1038/ncomms1457

    Google Scholar 

  • Paasche E (2002) A review of the coccolithophorid Emiliania huxleyi (Prymnesiophyceae), with particular reference to growth, coccolith formation and calcification—photosynthesis interactions. Phycologia 40:503–529

    Article  Google Scholar 

  • Porter SM (2010) Calcite and aragonite seas and the de novo acquisition of carbonate skeletons. Geobiology 8:256–277

    Article  Google Scholar 

  • Porter SM, Meisterfeld R, Knoll AH (2003) Vase-shaped microfossils from the Neoproterozoic Chuar Group, Grand Canyon: A classification guided by modern testate amoebae. J Paleontol 77:409–429

    Article  Google Scholar 

  • Pouille L, Obut O, Danelian T et al (2011) Lower Cambrian (Botomian) polycystine radiolaria from the Altai Mountains (southern Siberia, Russia). Comptes rendus Palevol 10:627–633

    Article  Google Scholar 

  • Preisig HR (1994) Siliceous structures and silicification in flagellated protists. Protoplasma 181:29–42

    Article  Google Scholar 

  • Pruss SA, Finnegan S, Fischer WW et al (2010) Carbonates in skeleton-poor seas: new insights from Cambrian and Ordovician strata of Laurentia. Palaios 25:73–84

    Article  Google Scholar 

  • Pruss SA, Clemente H, LaFlamme M (2012) Early (Series 2) Cambrian archaeocyathan reefs of southern Labrador as a locus for skeletal carbonate production. Lethaia 45:401–410

    Article  Google Scholar 

  • Racki G, Cordey F (2000) Radiolarian palaeoecology and radiolarites: is the present the key to the past? Earth-Sci Rev 52:83–120

    Article  Google Scholar 

  • Raven JA (1983) The transport and function of silicon in plants. Biol Rev 58:179–207

    Article  Google Scholar 

  • Raven JA, Giordano M (2009) Biomineralization by photosynthetic organisms: evidence of coevolution of the organisms and their environment? Geobiology 7:140–154

    Article  Google Scholar 

  • Raven JA, Knoll AH (2010) Non-skeletal biomineralization in protists: matters of moment and gravity. Geomicrobiol J 27:1–13

    Article  Google Scholar 

  • Raven JA, Waite AM (2004) The evolution of silicification in diatoms: inescapable sinking and sinking as escape? New Phytol 162:45–61

    Article  Google Scholar 

  • Richter FM, Rowley DB, Depaolo DJ (1992) Sr isotope evolution of seawater—the role of tectonics. Earth Planet Sci Lett 109:11–23

    Article  Google Scholar 

  • Round FE, Crawford RM, Mann DG (1990) The diatoms: biology & morphology of the genera. Cambridge Univ Press, Cambridge

    Google Scholar 

  • Siever R (1992) The silica cycle in the Precambrian. Geochim Cosmochim Acta 56:3265–3272

    Article  Google Scholar 

  • Sperling EA, Robinson JM, Pisani D et al (2010) Where’s the glass? Biomarkers, molecular clocks, and microRNAs suggest a 200-Myr missing Precambrian fossil record of siliceous sponge spicules. Geobiology 8:24–36

    Article  Google Scholar 

  • Strathern P (2005) A brief history of medicine: from Hippocrates’ four humours to Crick and Watson’s double helix. Robinson, London

    Google Scholar 

  • Thomas RDK, Shearman RM, Stewart CW (2000) Evolutionary exploitation of design options by the first animals with hard skeletons. Science 288:239–1242

    Article  Google Scholar 

  • Ujiié Y, Kimoto K, Pawlowski J (2008) Molecular evidence for an independent origin of modern triserial planktonic foraminifera from benthic ancestors. Mar Microapelontol 69:334–340

    Article  Google Scholar 

  • van Tol HM, Irwin AJ, Finkel ZV (2012) Macroevolutionary trends in silicoflagellate skeletal morphology: the costs and benefits of silicification. Paleobiology 38:391–402

    Article  Google Scholar 

  • Vermeij GJ (1977) The Mesozoic marine revolution: evidence from snails, predators and grazers. Paleobiology 3:245–258

    Google Scholar 

  • Vidal G, MoczydlowskaVidal M (1997) Biodiversity, speciation, and extinction trends of Proterozoic and Cambrian phytoplankton. Paleobiology 23:230–246

    Google Scholar 

  • Walker G, Dorrell RG, Schlacht A, Dacks JB (2011) Eukaryotic systematics: a user’s guide for cell biologists and parasitologists. Parasitology 138:1638–1663

    Google Scholar 

  • Wallace AF, Wang D, Hamm LM et al (2012) Skeletal formation in eukaryotes. In: Knoll AH, Canfield DE, Konhauser K (eds) Fundamentals of geobiology. Wiley-Blackwell, Chichester, pp 150–187

    Google Scholar 

  • Weiner S, Dove PM (2003) An overview of biomineralization processes and the problem of the vital effect. Rev Mineral Geochem 54:1–29

    Article  Google Scholar 

  • Won M-Z, Iams WJ (2011) Earliest Arenig radiolarians from the Cow Head Group, western Newfoundland. J Paleontol 85:156–177

    Article  Google Scholar 

  • Wood RA, Grotzinger JP, Dickson JAD (2002) Proterozoic modular biomineralized metazoan from the Nama Group, Namibia. Science 296:2383–2386

    Article  Google Scholar 

  • Yoshida M, Noel M, Nakayama T et al (2006) A haptophyte bearing siliceous scales: ultrastructure and phylogenetic position of Hyalolithus neolepis gen. et sp. nov. (Prymnesiophyceae, Haptophyta). Protist 157:213–234

    Article  Google Scholar 

  • Young J, Henriksen K (2003) Mineralization within vesicles: the calcite of coccoliths. Rev Mineral Geochem 54:189–215

    Article  Google Scholar 

  • Zeebe RE, Westbroek P (2003) A simple model for the CaCO3 saturation state of the ocean: the “Strangelove”, the “Neritan”, and the “Cretan” ocean. Geochem Geophy Geosystems. doi:10.1029/2003GC000538

    Google Scholar 

  • Zhuravlev AYu, Wood RA (2008) Eve of biomineralization: controls on skeletal mineralogy. Geology 36:923–926

    Article  Google Scholar 

  • Zlatogursky VV (2012) Raphidiophrys heterophryoidea sp nov (Centrohelida: Raphidiophryidae), the first heliozoan species with a combination of siliceous and organic skeletal elements. Eur J Protistol 48:9–16

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Andrew H. Knoll .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Knoll, A., Kotrc, B. (2015). Protistan Skeletons: A Geologic History of Evolution and Constraint. In: Hamm, C. (eds) Evolution of Lightweight Structures. Biologically-Inspired Systems, vol 6. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-9398-8_1

Download citation

Publish with us

Policies and ethics