Competition between silicifiers and non-silicifiers in the past and present ocean and its evolutionary impacts Katharine Hendry, Alan Marron, Flora Vincent, Daniel Conley, Marion Gehlen, Federico Ibarbalz, Bernard Queguiner, Chris Bowler To cite this version: Katharine Hendry, Alan Marron, Flora Vincent, Daniel Conley, Marion Gehlen, et al.. Competition between silicifiers and non-silicifiers in the past and present ocean and its evolutionary impacts. Fron- tiers in Marine Science, Frontiers Media, 2018, 5, pp.22. 10.3389/fmars.2018.00022. hal-01812492 HAL Id: hal-01812492 https://hal.archives-ouvertes.fr/hal-01812492 Submitted on 11 Jun 2018 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. REVIEW published: 06 February 2018 doi: 10.3389/fmars.2018.00022 Competition between Silicifiers and Non-silicifiers in the Past and Present Ocean and Its Evolutionary Impacts Katharine R. Hendry 1†, Alan O. Marron 2†, Flora Vincent 3†, Daniel J. Conley 4,5, Marion Gehlen 6, Federico M. Ibarbalz 3, Bernard Quéguiner 7 and Chris Bowler 3* 1 Department of Earth Sciences, Bristol University, Bristol, United Kingdom, 2 Department of Applied Mathematics and Theoretical Physics, Centre for Mathematical Sciences, University of Cambridge, Cambridge, United Kingdom, 3 Institut de Biologie de l’Ecole Normale Supérieure, Ecole Normale Supérieure, Centre National de la Recherche Scientifique, Institut National de la Santé et de la Recherche Médicale, PSL Research University, Paris, France, 4 Department of Geology, Lund University, Lund, Sweden, 5 Stellenbosch Institute for Advanced Study, Stellenbosch, South Africa, 6 Institut Pierre-Simon-Laplace, Laboratoire des Sciences du Climat et de l’Environnement, Gif-sur-Yvette, France, 7 Aix Marseille Univ, Edited by: Université de Toulon, Centre National de la Recherche Scientifique/INSU, IRD, MIO, UM 110, Marseille, France Eric ’Pieter Achterberg, GEOMAR Helmholtz Centre for Ocean Research Kiel (HZ), Germany Competition is a central part of the evolutionary process, and silicification is no exception: Reviewed by: between biomineralized and non-biomineralized organisms, between siliceous and Nils Kröger, Technische Universität Dresden, non-siliceous biomineralizing organisms, and between different silicifying groups. Here Germany we discuss evolutionary competition at various scales, and how this has affected Pascal Jean Lopez, biogeochemical cycles of silicon, carbon, and other nutrients. Across geological Centre National de la Recherche Scientifique (CNRS), France time we examine how fossils, sediments, and isotopic geochemistry can provide Mark Hildebrand, evidence for the emergence and expansion of silica biomineralization in the ocean, University of California, San Diego, United States and competition between silicifying organisms for silicic acid. Metagenomic data from *Correspondence: marine environments can be used to illustrate evolutionary competition between groups Chris Bowler of silicifying and non-silicifying marine organisms. Modern ecosystems also provide [email protected] examples of arms races between silicifiers as predators and prey, and how silicification † These authors are joint first authors can be used to provide a competitive advantage for obtaining resources. Through and have contributed equally to this work. studying the molecular biology of silicifying and non-silicifying species we can relate how they have responded to the competitive interactions that are observed, and how solutions Specialty section: have evolved through convergent evolutionary dynamics. This article was submitted to Marine Biogeochemistry, Keywords: diatoms, silicifiers, radiolarians, silicic acid transporters, silicification a section of the journal Frontiers in Marine Science Received: 22 September 2017 INTRODUCTION Accepted: 17 January 2018 Published: 06 February 2018 Biomineralization refers to the precipitation of minerals by living organisms (Simkiss and Citation: Wilbur, 1989). It may occur as a by-product of the normal metabolism of the organism under Hendry KR, Marron AO, Vincent F, indirect genetic control—related to the cellular processes that create the conditions for incidental Conley DJ, Gehlen M, Ibarbalz FM, biomineral formation—and with no pre-concentration of specific mineral ions. Alternatively, Quéguiner B and Bowler C (2018) the composition of the biominerals formed can be entirely dependent on the environmental Competition between Silicifiers and Non-silicifiers in the Past and Present conditions, for example, the formation of iron oxide by brown algae (Lee and Kugrens, 1989). Ocean and Its Evolutionary Impacts. By contrast, biologically controlled biomineralization requires direct genetic control, generates Front. Mar. Sci. 5:22. characteristically patterned structures, and involves selective uptake and pre-concentration of doi: 10.3389/fmars.2018.00022 mineral ions. Frontiers in Marine Science | www.frontiersin.org 1 February 2018 | Volume 5 | Article 22 Hendry et al. Competition between Silicifiers and Non-silicifiers in the Ocean In nature, we observe a wide array of biominerals (see biosilica has even been suggested to play a role as a pH buffer Figure 1), ranging from iron oxide to strontium sulfate (Raven for the enzymatic activity of carbonic anhydrase, aiding the and Knoll, 2010), with calcareous biominerals being particularly acquisition of inorganic carbon for photosynthesis (Milligan and notable (Knoll, 2003; Knoll and Kotrc, 2015). However, the most Morel, 2002). taxonomically widespread biomineral is silica (SiO2·nH2O), The myriad of functions and benefits of biomineralization being present in all eukaryotic supergroups (Marron et al., raises an important question: why do some organisms 2016b). Notwithstanding, the degree of silicification can vary biomineralize while others do not? Furthermore, why is even between closely related taxa, from being found in composite there such a diversity of biominerals besides silicon, when structures with other biominerals (e.g., limpet teeth; Sone silicon is so abundant, comprising 28% of the Earth’s crust? et al., 2007), to forming minor structures (e.g., ciliate granules; The answer to these questions lies in the evolutionary interplay Foissner et al., 2009) or being a major structural constituent between biomineralization and geochemistry, and in the of the organism (Preisig, 1994). The most extreme degree competitive interactions that have arisen from these dynamics. of silicification is evident in the diatoms, where almost all Fundamentally whether an organism produces silica or not species have an obligate requirement for silicon to complete involves evolutionary trade-offs and competition between cell wall formation and cell division (Darley and Volcani, 1969; silicifiers themselves, and with non-silicifying organisms (both Martin-Jézéquel et al., 2000). Biogeochemically and ecologically, those which utilize other biominerals, and non-mineralizing diatoms are believed to be the most important silicifiers in groups). Mathematical models and controlled experiments of modern marine ecosystems, with radiolarians (polycystine and resource competition in phytoplankton have demonstrated phaeodarian rhizarians), silicoflagellates (dictyochophyte and the rise to dominance of different algal species based on chrysophyte stramenopiles), and sponges with prominent roles nutrient backgrounds in defined media. These have been part of as well. In contrast, the major silicifiers in terrestrial ecosystems fundamental studies in ecology (Tilman, 1977; Sommer, 1994). are the land plants (embryophytes), with other silicifying groups However, the vast diversity of organisms that thrive in a complex (e.g., testate amoebae) having a minor role. array of biotic and abiotic interactions in oceanic ecosystems Broadly, biomineralized structures are believed to have are a challenge to such minimal models and experimental evolved and diversified where the energetic cost of biomineral designs, whose parameterization and possible combinations, production is less than the expense of producing an equivalent respectively, limit the interpretations that can be built on them. organic structure (Mann, 2001; Raven and Waite, 2004; Finkel Here we broadly extend our attention into other types of data and Kotrc, 2010). Raven (1983) calculated that the energetic from which competition can be inferred: the geological record, costs of silicic acid uptake and silica structure formation is the distribution of species in modern marine ecosystems, and substantially more efficient than forming the same volume phenomena at the cellular and molecular levels (summarized in of an organic structure (∼20x more for lignin and 10x for Table 1). polysaccharides like cellulose). Based on the structural model of biogenic silica of Hecky et al. (1973), Lobel et al. (1996) identified by biochemical modeling a low-energy reaction pathway for EVOLUTIONARY COMPETITION ACROSS nucleation and growth of silica. The combination of organic and GEOLOGICAL TIME inorganic components within biomineralized structures often results