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Iridocytes Mediate Photonic Cooperation Between Giant Clams (Tridacninae) and Their Photosynthetic Symbionts

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Iridocytes Mediate Photonic Cooperation Between Giant Clams (Tridacninae) and Their Photosynthetic Symbionts Iridocytes Mediate Photonic Cooperation Between Giant Clams (Tridacninae) and Their Photosynthetic Symbionts Item Type Article Authors Rossbach, Susann; Subedi, Ram Chandra; Ng, Tien Khee; Ooi, Boon S.; Duarte, Carlos M. Citation Rossbach, S., Subedi, R. C., Ng, T. K., Ooi, B. S., & Duarte, C. M. (2020). Iridocytes Mediate Photonic Cooperation Between Giant Clams (Tridacninae) and Their Photosynthetic Symbionts. Frontiers in Marine Science, 7. doi:10.3389/fmars.2020.00465 Eprint version Publisher's Version/PDF DOI 10.3389/fmars.2020.00465 Publisher Frontiers Media SA Journal Frontiers in Marine Science Rights Copyright © 2020 Rossbach, Subedi, Ng, Ooi and Duarte. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. Download date 29/09/2021 22:29:26 Item License https://creativecommons.org/licenses/by/4.0/ Link to Item http://hdl.handle.net/10754/663708 fmars-07-00465 June 17, 2020 Time: 19:0 # 1 ORIGINAL RESEARCH published: 19 June 2020 doi: 10.3389/fmars.2020.00465 Iridocytes Mediate Photonic Cooperation Between Giant Clams (Tridacninae) and Their Photosynthetic Symbionts Susann Rossbach1*†, Ram Chandra Subedi2†, Tien Khee Ng2, Boon S. Ooi2 and Carlos M. Duarte1 1 Red Sea Research Centre and Computational Bioscience Research Center, Biological and Environmental Science and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia, 2 Photonics Laboratory, Computer, Electrical and Mathematical Sciences and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia Edited by: Carla Zilberberg, Iridocytes, containing multiple stacks of proteinaceous platelets and crystalized guanine, Federal University of Rio de Janeiro, Brazil alternating with thin cytoplasm sheets, are specialized cells that act as multilayer nano- Reviewed by: reflectors. Convergence evolution led to their arising across a broad range of organisms, Miguel Mies, including giant clams of the Tridacninae subfamily – the only sessile and photosymbiotic University of São Paulo, Brazil Anthony William Larkum, organism, among animals known to possess iridocytes. Through the interference of University of Technology Sydney, light with their nanoscale architecture, iridocytes generate “structural colors,” which are Australia reported to serve different purposes, from intra-species communication to camouflage. *Correspondence: In giant clams, iridocytes were previously reported to promote a lateral- and forward Susann Rossbach [email protected]; scattering of photosynthetically productive radiation (PAR) into the clam tissue, as well [email protected] as the back reflection of non-productive wavelengths. Hence, they are assumed to †These authors have contributed promote an increased efficiency in the use of available solar energy, while simultaneously equally to this work preventing photodamage of the algal symbionts. We report the use of guanine crystals Specialty section: within Tridacna maxima giant clam iridocytes as a basis for photonic cooperation This article was submitted to between the bivalve host and their photosynthetic symbionts. Our results suggest Coral Reef Research, a section of the journal that, in addition to the previously described scattering processes, iridocytes absorb Frontiers in Marine Science potentially damaging UV radiation (UVR) and, through successive emission, emit light at Received: 30 January 2020 longer wavelengths, which is then absorbed by the photosynthetic pigments of the algal Accepted: 25 May 2020 symbionts. Consequently, both, host and algal symbionts are sheltered from (potentially) Published: 19 June 2020 damaging UVR, while the available solar energy within the PAR spectrum increases, Citation: Rossbach S, Subedi RC, Ng TK, thereby potentially enhancing photosynthetic and calcification rates in this large bivalve. Ooi BS and Duarte CM (2020) Further, our results suggest that this photonic cooperation could be responsible for Iridocytes Mediate Photonic Cooperation Between Giant Clams the broad repertoire of colors that characterizes the highly diverse mantle patterns (Tridacninae) and Their Photosynthetic found in T. maxima. Symbionts. Front. Mar. Sci. 7:465. doi: 10.3389/fmars.2020.00465 Keywords: Tridacna, photosynthesis, iridocyte, symbiosis, light, giant clam Frontiers in Marine Science | www.frontiersin.org 1 June 2020 | Volume 7 | Article 465 fmars-07-00465 June 17, 2020 Time: 19:0 # 2 Rossbach et al. Iridocytes in Giant Clams INTRODUCTION Iridocytes (also called iridophores, guanophores, or interference cells) are multilayer nano-reflectors with alternating high and low refractive indices, generating interference of light waves. They contain multiple stacks of thin proteinaceous platelets (Kamishima, 1990; Griffiths et al., 1992; Kim et al., 2017) and crystalized guanine (Morrison et al., 1996; Teyssier et al., 2015) (an essential component of DNA and RNA), alternating with thin sheets of cytoplasm (Ide and Hama, 1972; Rohrlich and Rubin, 1975; Kim et al., 2017). Convergence evolution has led to their arising across a broad range of organisms, including reptiles, such as chameleons (Rohrlich and Rubin, 1975), amphibians, such as tree frogs (Setoguti, 1967), fish (Lythgoe et al., 1984), FIGURE 1 | Variations of mantle tissue colorations in Tridacninae, here exemplarily shown for Tridacna maxima. Specimens in the top row (A–C) are and mollusks such as cephalopods (Cloney and Brocco, 1983; examples for brown color variants and those in the bottom (D–F) for blue DeMartini et al., 2013a) and giant clams of the Tridacninae appearing mantle colorations. Panels (C,F), respectively, are equivalents for subfamily (Kamishima, 1990; Griffiths et al., 1992; Holt et al., the brown and blue variation used in this study. 2014; Ghoshal et al., 2016a). Iridocytes display a variety of different functions in organisms, from the prevention of gas diffusion (Scholander, 1954), substrate for epibionts (Vicentuan-Cabaitan et al., 2014), and protection against extreme heat (Kobelt and Linsenmair, 1992), also have been harvested by humans for food and ornamental as mirror components of visual systems (Locket, 1970) and the purposes (Mies et al., 2017). Further, they are even considered manipulation of light (Fox, 1976; Holt et al., 2014; Ghoshal et al., an ecosystem-engineering species (Neo et al., 2015) as they may 2016a; Kim et al., 2017). Through the interference of light with a form reef-like structures (Andréfouët et al., 2005). combination of their nanoscale architectures, iridocytes generate Giant clams are one of the few molluscan groups that some of the liveliest colorations across these organisms (Holt live in symbiotic relationship with unicellular algae of the et al., 2014; Teyssier et al., 2015).The resulting “structural colors” Symbiodiniaceae family (Taylor, 1969; Yonge, 1975; Norton et al., (Fox, 1976) are reported to serve different purposes, from intra- 1992; Fitt, 1993). Among all the animals that are currently species communication (Chae and Nishida, 1994) to camouflage known to possess iridocytes, this symbiosis makes them the only (Théry and Casas, 2002; Ikeda and Kohshima, 2009). organism capable of photosynthesis, through the activity of their Recent research mainly focused on “how nanostructures, algal symbionts. These symbionts are located intercellularly in a such as Iridocytes, regulate the optical properties of biological special tubular system, originating in digestive diverticular ducts materials” (Sun et al., 2013). However, photonic structures in of the stomach and extending into the outer mantle (Norton biological systems were recently reported to also potentially affect et al., 1992). As the algal symbionts can deliver up to 100% of the physiological processes in plants and phototrophic organisms respiratory carbon demand of giant clams (Trench et al., 1981; in general (Gkikas et al., 2015; Goessling et al., 2018). The Klumpp et al., 1992; Klumpp and Griffiths, 1994), some species structural nature of iridocytes allows them to reflect any are even considered to be net (photo)-autotrophs (Klumpp and waveband of the visible light spectrum from near UV to Griffiths, 1994; Jantzen et al., 2008). This successful photo- deep red (400–700 nm) (Mäthger and Hanlon, 2007). Further, symbiotic relationship is considered to be the main reason why there is evidence that organisms may be able to change the Tridacninae are among the largest (Beckvar, 1981) and fastest- optical properties of these cells from non-iridescent (Rayleigh- growing (Bonham, 1965) bivalves on Earth, and why bleaching scattering) to iridescent (structural reflection) by ultrastructural (i.e., the loss of their symbiotic algae) (Glynn, 1993; Norton et al., changes, thereby allowing rapidly shifts in skin colors (Mäthger 1995) is known to significantly decrease their fitness, resulting and Hanlon, 2007; DeMartini et al., 2013a,b). in reduced growth, fecundity, and survival (Leggat et al., 2003; Giant clams of the Tridacninae subfamily stand out among Maboloc et al., 2015). Besides their contribution to the gross all other organisms containing iridocytes as the sole sessile physiological performance
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