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Lens Eyes in Protists Current Biology Magazine Observations of other algal species as this fascinating organelle emerges Quick guide suggest that their pyrenoids have from obscurity. similar properties. Lens eyes in protists Where can I fi nd out more? Can the pyrenoid be engineered into Atkinson, N., Feike, D., Mackinder, L.C., Meyer, M.T., Griffi ths, H., Jonikas, M.C., Smith, A.M., Dan-E. Nilsson1,* and Justin Marshall2 other organisms? Modeling studies and McCormick, A.J. (2016). Introducing an suggest that the transfer of a pyrenoid algal carbon-concentrating mechanism into higher plants: location and incorporation of into C3 crops such as wheat and rice key components. Plant Biotechnol. J. 14, Which protists have eyes? A group of could improve water and nitrogen- 1302–1315. dinofl agellates, the warnowiids, carry a use effi ciencies, and increase yields Freeman Rosenzweig, E.S., Xu, B., Cuellar, L.K., unique structure that resembles a lens Martinez-Sanchez, A., Schaffer, M., Strauss, M., by up to 60%. Pyrenoid engineering Cartwright, H.N., Ronceray, P., Plitzko, J.M., and a retina (Figure 1). The eye-like efforts are still at an early stage; but Forster, F., et al. (2017). The eukaryotic CO2- structure is called an ocelloid and is concentrating organelle is liquid-like and exhibits already, encouraging results have been dynamic reorganization. Cell 171, 148–162. obviously surprising to see in a single- obtained. First, nearly all algal proteins Hennacy, J.H., and Jonikas, M.C. (2020). Prospects celled organism. The lens clearly refracts for engineering biophysical CO concentrating tested localize to the correct sub- 2 light and it is placed such that it will mechanisms into land plants to enhance yields. cellular compartment in higher plants Annu. Rev. Plant Biol. 71, 10.1146. pass light to the retina-like structure. without any changes to their protein Long, S.P., Marshall-Colon, A., and Zhu, X. (2015). These facts, along with the shape of Meeting the global food demand of the future sequence, suggesting that transferring by engineering crop photosynthesis and yield the whole structure, and its orientation the pyrenoid will not require extensive potential. Cell 161, 56–66. during directional swimming strongly protein-engineering work. Second, the Mackinder, L.C.M., Meyer, M.T., Mettler-Altmann, T., suggest that the ocelloid is a visual Chen, V.K., Mitchell, M.C., Caspari, O., fi rst steps of reconstituting a pyrenoid Freeman Rosenzweig, E.S., Pallesen, L., organ guiding behaviours in a unicellular matrix in higher plants are well Reeves, G., Itakura, A., et al. (2016). A repeat organism. This says something about protein links Rubisco to form the eukaryotic underway. In order to form a pyrenoid carbon-concentrating organelle. Proc. Natl. how constrained eye evolution is. Animal matrix, it is thought that the small Acad. Sci. USA 113, 5958–5963. eyes are made of many different types of subunit of Rubisco found in higher Mackinder, L.C.M., Chen, C., Leib, R.D., Patena, W., tissue that form the essential structures Blum, S.R., Rodman, M., Ramundo, S., plants needs to be exchanged for the Adams, C.M., and Jonikas, M.C. (2017). for catching pictorial information. In Chlamydomonas homolog to enable A spatial interactome reveals the protein warnowiid dinofl agellates, almost organization of the algal CO2-concentrating its binding to the EPYC1 linker protein. mechanism. Cell 171, 133–147. identical structures have evolved as Excitingly, this exchange of Rubisco Meyer, M.T., Whittaker, C., and Griffi ths, H. (2017). organelles within the single cell. small subunits is tolerated by the The algal pyrenoid: key unanswered questions. J. Exp. Bot. 14, 3739–3749. vascular plant Arabidopsis. These early Mukherjee, A., Lau, C.S., Walker, C.E., Rai, A., What are dinofl agellates? They are a advances may pave the way for crops Prejean, C.I., Yates, G., Emrich-Mills, T., diverse phylum of unicellular eukaryotes Lemoine, S.G., Vinyard, D.J., Mackinder, L.C.M., with synthetic pyrenoids that produce et al. (2019). Thylakoid localized bestrophin-like that are ecologically important more food with fewer resources to proteins are essential for the CO2 concentrating components of phytoplankton. Some enable a more sustainable world. mechanism of Chlamydomonas reinhardtii. Proc. species cause red tides and others, Natl. Acad. Sci. USA 116, 16915–16920. Schmitz, F.K.J. (1882). Die Chromatophoren der such as Noctiluca, make water glow What major questions remain Algen. (Bonn: Max Cohen & Sohn). with bioluminescence at night. Many Toyokawa, C., Yamano, T., and Fukuzawa, H. unanswered? Despite recent (2020). Pyrenoid starch sheath is required for are armoured with cellulose plates progress, we are only beginning LCIB localization and the CO2-concentrating that give the cells species-specifi c to understand how the pyrenoid mechanism in green algae. Plant Physiol. https:// shapes, whereas other groups, such doi.org/10.1104/pp.19.01587. works at a molecular level. What Wang, L., Yamano, T., Takane, S., Niikawa, Y., as the eye-bearing warnowiids, is the structural basis for pyrenoid Toyokawa, C., Ozawa, S.I., Tokutsu, R., belong to the naked dinofl agellates. Takahashi, Y., Minagawa, J., Kanesaki, Y., et al. matrix formation? How are the phase (2016). Chloroplast-mediated regulation of A distinctive feature of dinofl agellates 2+ transitions of the matrix catalyzed and CO2-concentrating mechanism by Ca -binding is their fl agellar arrangement with one regulated? How are pyrenoid tubules protein CAS in the green alga Chlamydomonas ribbon-like transverse fl agellum and reinhardtii. Proc. Natl. Acad. Sci. USA 113, shaped and what are their molecular 12586–12591. one longitudinal fl agellum of more functions? How is the starch sheath Wang, Y., Stessman, D.J., and Spalding, M.H. conventional appearance. Many species (2015). The CO2 concentrating mechanism and nucleated and shaped? How are photosynthetic carbon assimilation in limiting contain chloroplasts and are autotrophic, proteins targeted to the pyrenoid? CO2: how Chlamydomonas works against the whereas others are heterotrophic or How are the pyrenoid’s three sub- gradient. Plant J. 82, 429–448. mixotrophic. Wunder, T., Cheng, S.L.H., Lai, S.-K., Li, H.-Y., and compartments held together? How Mueller-Cajar, O. (2018). The phase separation is the pyrenoid positioned to its underlying the pyrenoid-based microalgal In which ways are warnowiids Rubisco supercharger. Nat. Commun. 9, 5076. canonical location? What is the full Zhan, Y., Marchand, C.H., Maes, A., Mauries, A., special? Apart from containing the set of proteins required for a minimal Sun, Y., Dhaliwal, J.S., Uniacke, J., Arragain, S., unique ocelloid, warnowiids possess pyrenoid to operate? If pyrenoids Jiang, H., Gold, N.D., et al. (2018). Pyrenoid various types of mechanical equipment functions revealed by proteomics in evolved multiple times through Chlamydomonas reinhardtii. PLoS One 13, of extreme complexity in their cells, convergent evolution, what common e0185039. such as pistons for propulsion and structural and functional principles harpoon-like nematocysts for impaling do they share? These and other Department of Molecular Biology, Princeton other cells. The nematocysts, which questions are sure to yield exciting University, Princeton, NJ 08544-1014, USA. are also found in a sister group to discoveries over the coming years *E-mail: [email protected] warnowiids, are at least superfi cially R458 Current Biology 30, R451–R520, May 18, 2020 Crown Copyright © 2020 Published by Elsevier Inc. Current Biology Magazine similar to the stinging nematocysts of jellyfi sh and other cnidarians. Warnowiids have been demonstrated to use nematocysts to attack and catch prey. Despite the heterotrophic lifestyle typical for warnowiids, they often contain photosynthetic chloroplasts. Surprisingly, these chloroplasts may not be their own, but rather stolen ‘kleptochloroplasts’ maintained from the µ prey they have caught and metabolised. 10 µm 5 m 10 mm They often engulf phototrophic species of dinofl agellates, and apparently Figure 1. Dinofl agellate and owl eyes. sometimes hijack the chloroplasts and The warnowiid dinofl agellate Erythropsidinium with its forward-pointing ocelloid (left). An electron use them as power stations for as long microscopic view of the ocelloid with its lens and retina-like body (middle). For comparison, the eye as they last. of an Eagle owl (Bubo bubo) which has a similar layout, although the diameter is 2000 times larger (right). Left and middle images courtesy of F. Gómez and T. Gojobori, respectively; right image modi- What is the ocelloid made of? Being fi ed from Walls (1942) with permission from Cranbrook Institute of Science. a unicellular organism, warnowiids have to use organelles, not cells, to How similar are the ocelloids to it is not predation because their typical build their eyes. There is a cornea, a animal eyes? Compared to animal eyes, ‘prey’ are photosynthetic species, in lens, a retinal body and a dark pigment warnowiid ocelloids are small, with a food webs equivalent to plants, which screen that stops light from entering the lens diameter rarely more than 10 µm. means that warnowiids are in fact retinal body from behind (Figure 1). It Despite and indeed because of this size herbivores. It just so happens that in turns out that the cornea is formed by difference, it is striking how similar their their world, the grass swims and has to modifi ed mitochondria and the retinal ‘eye’ design is to that of several animals. be hunted down. Studying warnowiids body is a highly modifi ed chloroplast. This includes the two-thousand-times is like joining Alice in Wonderland in Where the photoreceptors would have larger eyes of owls (Figure 1) and eyes a strange world down the rabbit hole been located in an animal eye there are of intermediate size in spiders, beetle where everything gets curiouser and densely packed and strangely modifi ed larvae and deep-sea fi sh.
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