Functional Chloroplasts Inside Animal Cells

Impact Objectives • Relevance of autotrophic versus heterotrophic components in the fitness of mixotrophic sacoglossan sea slugs • Fate of photosynthesis-derived carbon and nitrogen inside these animal cells • Impact of photoprotection mechanisms on the functionality of acquired chloroplasts Functional chloroplasts inside animal cells Dr Sónia Cruz and her collaborators, Drs Paulo Cartaxana, Bruno Jesus, Gonçalo Calado, João Serôdio, Anders Meibom, Cédric Hubas, and Michael Kühl are providing new insights into the biological significance of kleptoplasty. Cruz talks about their pioneering work on kleptoplasty Your latest work vary according to the algal food source. The What have been your key findings so far? looks at kleptoplasty. first step here is to answer that question for Are there any that you are particularly Can you explain the chloroplast in the algae. Then one must pleased with? this animal-plant verify if the same processes are working I am particularly keen on the investigation interaction? in the kleptoplast inside the sea slug and of the fate of photosynthetically fixed carbon for how long will these mechanisms be and nitrogen, along with showing that My current research supported. This is relevant because it is photosynthesis is indeed relevant for the Doctor Sónia Cruz focus on both known that many of these photoprotective sea slug E. viridis’ performance. We have understanding processes require synthesis of components unequivocally proven that photosynthesis the algae physiology and the particular coded by genes that are located in the algal is used to provide metabolites to the interaction where the animal (host), nucleus. Hence, if the animal digests the host and we are currently investigating instead of living symbiotically with the algae nucleus and does not incorporate other sea slug species. We also have whole microalgae, digests the algae cellular algal nuclear genes into its genome, how enough information to advance a possible components except for the chloroplasts. can the animal sustain some of these function of these metabolites in the host Because they are ‘stolen’ plastids, they photoprotective mechanisms and repair the metabolism, which is a huge step forward were named ‘kleptoplasts’. In the animal photosynthetic machinery? This is one of in this field. Additionally, we are introducing kingdom, kleptoplasty is only known to the research lines we are following. new methodologies in this field of research take place in some sea slugs of the order (lipidomic tools, hyperspectral reflectance Sacoglossa (molluscs). In this case, the We were very surprised when we discovered analysis, NanoSIMS studies). chloroplasts are incorporated and kept that Elysia viridis’ main food source, the functional inside cells of the sea slug’s algae Codium tomentosum, does not Furthermore, we have found strong digestive diverticula for some days, weeks or have a functional xanthophyll cycle for evidence for a link between kleptoplasty several months. instance. The xanthophyll cycle is one of and the sea slug’s behaviour in response to the main photoprotective mechanisms in light. As yet we have not been able to show Chloroplasts are known to be very sensitive algae and plants. C. tomentosum, as other how the kleptoplasts communicate with to oxidative stress. What mechanisms Bryosidales as we have recently shown, the host, but our results in this field so far protect these organelles upon their does not possess this capacity. Instead, they strongly imply this communication. We have incorporation by the sea slug? might rely on a more efficient repair of the also made interesting findings regarding photosynthetic machinery or depend to a novel photoprotection mechanisms in the In principle, the same mechanisms that large extent on chloroplast movement inside algae food sources but this is still on-going protect the chloroplasts inside the algae the algae. We are currently working on this work that can take many directions. could protect the kleptoplast inside the sea topic to understand which mechanisms slug. These mechanisms will depend on and protect the chloroplast from excessive light. 56 www.impact.pub Autotrophy driving animal fitness In the HULK project, scientists from the universities of Aveiro, Lisbon and Lusófona in Portugal are collaborating with academic groups in Denmark, Switzerland and France to combine biochemical, molecular and state-of-the art imaging techniques Understanding more about the processes is made up of researchers, Sónia Cruz, STATE-OF-THE-ART ANALYSIS of why and how an animal feeds itself both Paulo Cartaxana, Bruno Jesus, Gonçalo Based on previous observations on the from the sun’s energy and from other Calado, João Serôdio, Anders Meibom, physiology of kleptoplastic sea slugs, Cruz organisms is driving a research project Cédric Hubas, and Michael Kühl, who explains that the researchers participating underway in Portugal called ‘Functional have a strong background in photobiology in the HULK project hypothesised that Chloroplasts inside Animal cells: cracking studies in algae and symbiotic associations. the ‘autotrophic nutritional component the puzzle’ (HULK). Project Coordinator provided by the kleptoplasts is relevant Dr Sónia Cruz says the team is employing SOLAR-POWERED SEA SLUGS for their metabolism, thereby turning their ‘experimental procedures that have so far Kleptoplasty (from the Greek kléptes, model organism into a mixotroph, and that not been used in an attempt to explore the meaning thief) is the sequestration of algal the chloroplast’s inherent photoprotective only known case of kleptoplasty in the animal chloroplasts and their maintenance in a capacity plays an important role in kingdom: that of sacoglossan sea slugs’. functional status by host organisms such maintaining kleptoplasts photosynthetically as ciliates, dinoflagellates or foraminifera. active in the long term’. Their aim is to learn more about the Cruz points out that within metazoans balance of autotrophic and heterotrophic this phenomenon is only present among The first hypothesis is being investigated components in these animals. ‘We want certain sea slugs in the order Sacoglossa. by combining NanoSIMS and fatty acid to know to what extent the autotrophic ‘As opposed to other sea animals such profiles, which enables the scientists to component is relevant for the animal as corals, which establish a symbiotic address the fate of photosynthesis-derived survival and fitness, as well as how the interaction with the whole microalgae, carbon and nitrogen inside host cells. ‘In animal (host) is capable of retaining kleptoplastic sea slugs digest the rest of order to address the second question, a functional chloroplasts after ‘stealing’ algal components and keep the ‘stolen’ combination of methodologies commonly them,’ she explains. chloroplasts inside their digestive employed to investigate photoprotective diverticula, where they remain functional’, mechanisms in algae and plants, but never HULK is a 36 month research project, she says. applied to the study of kleptoplasts so far, which commenced in June 2016 and is used’, notes Cruz. has the main goals of understanding Intriguingly, although many of the both the fate of photosynthesis-derived mechanisms preventing chloroplasts The photoprotective component of non- carbon and nitrogen inside the animal degradation require the synthesis of photochemical processes is quantified host and the impact of photoprotection new proteins encoded in the nucleus of through chlorophyll fluorescence analysis mechanisms on kleptoplast longevity. This the microalgae, some slug species can techniques. ‘In turn, energy dissipation is a multidisciplinary collaboration with top keep functional kleptoplasts over several capacities are assessed through High- researchers in areas such as photobiology, months. ‘Much as photosynthesis by performance liquid chromatography gastropoda taxonomy, animal biology, kleptoplasts alone is not sufficient to (HPLC) pigment analysis of the xanthophyll NanoSIMS technology and lipidomic sustain host growth, previous studies point cycle combined with the quantification analysis. to an essential role of kleptoplasty’, Cruz of accumulating reactive oxygen species observes. Yet, the results on the relevance (ROS)’, she says. ‘Finally, the repair There are three Portuguese institutions of this process for sea slug survival have so capacity of the photosynthetic apparatus is involved: University of Aveiro; University of far remained controversial. evaluated by quantifying the accumulation Lisboa; and, University Lusófona. The team of D1 protein.’ www.impact.pub 57 The unravelling of the underlying mechanisms could Project Insights lead to practical biotechnological applications FUNDING R&D project (PTDC/BIA- ANM/4622/2014 – POCI-01-0145- FEDER-016754) and CESAM support (UID/AMB/50017 – POCI-01-0145- FEDER-007638) through Fundação para Cruz points out that they have some during the development of the HULK a Ciência e Tecnologia (FCT, Portugal), experiments planned which will analyse project and would not have been possible if Programa Operacional Regional de kleptoplast gene expression levels Dr Cruz could not count on a team of ‘great Lisboa (POR Lisboa), and Fundo Europeu de Desenvolvimento Regional and kleptoplast lipidome during food people that have always found time for (FEDER), within the Portugal 2020 deprivation to better understand which discussion and planning, including meeting Partnership Agreement and COMPETE components are responsible for

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