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Biosilicification of Loricate Choanoflagellate: Organic Composition of the Nanotubular Siliceous Costal Strips of Stephanoeca Diplocostata

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Biosilicification of Loricate Choanoflagellate: Organic Composition of the Nanotubular Siliceous Costal Strips of Stephanoeca Diplocostata 3575 The Journal of Experimental Biology 213, 3575-3585 © 2010. Published by The Company of Biologists Ltd doi:10.1242/jeb.048496 Biosilicification of loricate choanoflagellate: organic composition of the nanotubular siliceous costal strips of Stephanoeca diplocostata Ningping Gong1, Matthias Wiens1, Heinz C. Schröder1, Enrico Mugnaioli2, Ute Kolb2 and Werner E. G. Müller1,* 1Institute for Physiological Chemistry and Pathobiochemistry, Johannes Gutenberg University, Medical School, Duesbergweg 6, D-55099 Mainz, Germany and 2Institute for Physical Chemistry, Johannes Gutenberg University, Welderweg 11, 55099 Mainz, Germany *Author for correspondence ([email protected]) Accepted 20 July 2010 SUMMARY Loricate choanoflagellates (unicellular, eukaryotic flagellates; phylum Choanozoa) synthesize a basket-like siliceous lorica reinforced by costal strips (diameter of approximately 100nm and length of 3m). In the present study, the composition of these siliceous costal strips is described, using Stephanoeca diplocostata as a model. Analyses by energy-dispersive X-ray spectroscopy (EDX), coupled with transmission electron microscopy (TEM), indicate that the costal strips comprise inorganic and organic components. The organic, proteinaceous scaffold contained one major polypeptide of mass 14kDa that reacted with wheat germ agglutinin. Polyclonal antibodies were raised that allowed mapping of the proteinaceous scaffold, the (glyco)proteins, within the costal strips. Subsequent in vitro studies revealed that the organic scaffold of the costal strips stimulates polycondensation of ortho-silicic acid in a concentration- and pH-dependent way. Taken together, the data gathered indicate that the siliceous costal strips are formed around a proteinaceous scaffold that supports and maintains biosilicification. A scheme is given that outlines that the organic template guides both the axial and the lateral growth of the strips. Key words: loricate choanoflagellate, biosilicification, structural analysis, organic composition. INTRODUCTION an organism. The composite biominerals can be deposited One of the major innovative steps in the evolution of uni- and extracellularly, as in Foraminifera or in shells of mollusks, multicellular animals was the acquisition of a hard, mineralized intercellularly as in some calcareous algae, or intracellularly, as in skeleton. The development of skeletal elements facilitated an bacteria (magnetosome formation), plants or animals (reviewed in increase in size of the organisms – a phyletic trend that is known Weiner and Dove, 2003). Besides calcium-based skeletons, silica- in metazoans as Cope’s rule (Nicol, 1966). As changes in body size based skeletal systems arose during the early evolution of uni- and affect almost every aspect of life (Schmidt-Nielsen, 1984), two multicellular eukaryotes in the Precambrian (Proterozoic), more than strategies have been developed in animals to circumvent any 542 million years ago (Müller et al., 2007). constraints arising from body size increase. First, the acquisition of Focusing on silica, the major taxa that use this monomeric a hydrostatic skeleton and, second, the development of rigid solid inorganic molecule to form solid skeletons through controlled skeletal elements (Biewener, 2005). Exclusively, the formation of silica deposition processes are some protozoans, diatoms, inorganic structures in uni- and multicellular organisms is guided choanoflagellates and silicoflagellates (Leadbeater and Jones, 1984), by organic templates (Lowenstam and Weiner, 1989). Those and metazoans, with the siliceous sponges (phylum Porifera) as the template-induced or controlled mineralization processes have been most prominent representative, as well as higher plants (see Müller termed biomineralization. The ubiquitous occurrence of template- et al., 2003; Perry, 2003). All of those organisms take up silica into induced biomineralization processes in nature became obvious with their cells as monomeric silicic acid in order to polymerize/ the discovery that even the formation of the polymetallic nodules polycondensate amorphous and hydrated bio-silica. It is amazing and crusts of the deep-sea is initiated and directed by biogenic that those organisms are able to deposit almost pure, amorphous templates (Wang and Müller, 2009). In 1924, Schmidt (Schmidt, quartz glass at ambient, physiological conditions from monomeric 1924), who was the first scientist to compile template- silicate (see Perry, 2003). There are two mechanisms by which bio- caused/controlled biomineralization processes (Weiner and Dove, silica is formed, first by oversaturation and second by enzymatic 2003), highlighted the importance of an inorganic skeleton in the synthesis. Oversaturation of mono-/oligo-silica results in establishment of a body plan. Two concepts of biomineralization polycondensation at concentrations above 100mmoll–1 at neutral/ were categorized by Weiner and Dove (Weiner and Dove, 2003), physiological pH and body temperature (Iler, 1979; Benning et al., based on earlier systematic studies (Lowenstam and Weiner, 1989). 2005). The rate of aggregation/polycondensation from the They distinguished between biologically induced mineralization, monomeric silica increases with temperature at an activation energy whereby biological structures act as causative agents for nucleation of approximately 10kcal/mol (Iler, 1979), a value that is about half and subsequent growth of biominerals, and biologically controlled of the average activation energy required for the breaking of an mineralization, a process during which cells/organisms direct both average covalent bond (Porter et al., 2009). In the second strategy, the nucleation/growth and final location of the minerals within the silica-depositing organisms use an enzyme, silicatein, to lower THE JOURNAL OF EXPERIMENTAL BIOLOGY 3576 N. Gong and others the activation energy required for lower silica concentrations to and demonstrate the existence of organic components within the deposit monomers and oligomers to polymerize amorphous silica strips. The respective proteins were isolated from costal strips and (Cha et al., 1999; Krasko et al., 2000). This enzyme shows an affinity their distribution within those strips was mapped using the constant (Km value) to the mono-/oligomeric substrate of immunogold labeling technique. Moreover, in vitro silica approximately 50moll–1 (Müller et al., 2008b), allowing the precipitation experiments were performed that led to the conclusion polymerization to proceed at environmental concentrations that in that the organic components exert a silica-inductive effect, resulting the sea amount to approximately 5moll–1 (Maldonado et al., 1999). in bio-silica polycondensation. It can be postulated that bio-silica deposition, irrespective of its way of formation, non-enzymatically or enzymatically, is facilitated if MATERIALS AND METHODS the guiding organic template remains surrounded by the inorganic Materials polymer formed. This assumption stems from the observations that, The choanoflagellate Stephanoeca diplocostata Ellis was obtained at interfaces between two phases, sudden and considerable changes from the ATCC (ATCC50456; Manassas; VA, USA). The following of the apparent activation energies occur (Wynn-Williams, 1976; materials were purchased: Percoll, polyvinylpyrrolidone (Mr Ben-Shooshan et al., 2002). Until now, only from the spicules of 360,000), biotinylated wheat germ agglutinin, alkaline phosphatase the siliceous sponges has a protein-bio-silica hybrid been described conjugated avidin, goat-anti-mouse serum coupled to 5nm gold (Müller et al., 2008a; Müller et al., 2008c). In sponge spicules, this particles, goat-anti-mouse IgG-conjugated alkaline phosphatase and hybrid composition provides them with unusually high toughness tetraethylorthosilicate from Sigma-Aldrich (Taufkirchen or combined with extreme flexibility, a feature that pushed sponge bio- Steinheim; Germany); blocking reagent and BCIP/NBT (5-bromo- silica to the forefront of material sciences (Mayer, 2005) (reviewed 4-chloro-3-indolyl-phosphate/4-nitro-blue tetrazolium chloride) in Schröder et al., 2008). were from Roche (Mannheim, Germany); peptone and yeast extract In the present study, the inorganic, siliceous skeletal framework were from Roth (Karlsruhe; Germany). Culture flasks were obtained of choanoflagellates was studied with the aim of clarifying whether from Greiner Bio-one (Frickenhausen, Germany). Artificial seawater their siliceous structures are composed of an inorganic [siliceous]: was prepared according to the recipe described by Harrison and organic [proteinaceous] composite, as well. Choanoflagellates colleagues (Harrison et al., 1980) and autoclaved. [phylum Choanozoa (Shalchian-Tabrizi et al., 2008)] are globally distributed free-living unicellular or colonial flagellate eukaryotes Cell culture living in marine and freshwater environments (Thomsen and Larsen, The choanoflagellate S. diplocostata cells were grown in an 1992; Buck and Garrison, 1988). The choanoflagellates are artificial-seawater-based medium, supplemented with bacteria subdivided into three families (based on the composition and (Klebsiella pneumoniae subsp. pneumoniae), at 16°C as described existence and/or structure of the extracellular matrix, the periplast) (Harrison et al., 1980; Leadbeater and Davies, 1984; Leadbeater the: Codonosigidae (lacking any periplast), Salpingoecidae and Jones, 1984; Leadbeater, 1985). The medium for this (encased/coated into a firm theca composed
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