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Kleptoplasty, the process by which a host organism sequesters and retains algal chloroplasts, is relatively common in protists. The origin of the plastid varies, as do the length of time it is retained in the host and the functionality of the association. In metazoa, the capacity for long-term (several weeks to months) maintenance of photosynthetically active chloroplasts is a unique characteristic of a handful of sacoglossan sea slugs. This capability has earned these slugs the epithets "crawling leaves" and "solar-powered sea slugs." This Unsolved Mystery explores the basis of chloroplast maintenance and function and attempts to clarify contradictory results in the published literature. We address some of the mysteries of this remarkable association. Why are functional chloroplasts retained? And how is the function of stolen chloroplasts maintained without the support of the algal nucleus?, Competing Interests: The authors have declared that no competing interests exist., (Copyright: © 2022 Cruz, Cartaxana. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)

Sea slugs increase the longevity of the chloroplasts they steal from algae by limiting the harmful side-effects of photosynthesis., Competing Interests: PC, SC No competing interests declared, (© 2020, Cartaxana and Cruz.)

Absorption of excessive light by photosymbiotic organisms leads to the production of reactive oxygen species that can damage both symbiont and host. This is highly relevant in sacoglossan sea slugs that host functional chloroplasts 'stolen' from their algal foods (kleptoplasts), because of limited repair capacities resulting from the absence of algal nuclear genes. Here, we experimentally demonstrate (i) a host-mediated photoprotection mechanism in the photosynthetic sea slug Elysia timida , characterized by the closure of the parapodia under high irradiance and the reduction of kleptoplast light exposure; and (ii) the activation of a reversible xanthophyll cycle in kleptoplasts, which allows excessive energy to be dissipated. The described mechanisms reduce photoinactivation under high irradiance. We conclude that both host-mediated behavioural and plastid-based physiological photoprotective mechanisms can mitigate oxidative stress induced by high light in E. timida These mechanisms may play an important role in the establishment of long-term photosynthetically active kleptoplasts., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2019. Published by The Company of Biologists Ltd.)

The optical properties of diatom silicate frustules inspire photonics and nanotechnology research. Whether light interaction with the nano-structure of the frustule also affects diatom photosynthesis has remained unclear due to lack of information on frustule optical properties under more natural conditions. Here we demonstrate that the optical properties of the frustule valves in water affect light harvesting and photosynthesis in live cells of centric diatoms (Coscinodiscus granii). Microscale cellular mapping of photosynthesis around localized spot illumination demonstrated optical coupling of chloroplasts to the valve wall. Photonic structures of the three-layered C. granii valve facilitated light redistribution and efficient photosynthesis in cell regions distant from the directly illuminated area. The different porous structure of the two sides of the valve exhibited photon trapping and forward scattering of blue light enhancing photosynthetic active radiation inside the cell. Photonic structures of diatom frustules thus alter the cellular light field with implications on diatom photobiology., (© 2018 The Authors. New Phytologist © 2018 New Phytologist Trust.)

Diatom-dominated microphytobenthos (MPB) is the main primary producer of many intertidal and shallow subtidal environments, being therefore of critical importance to estuarine and coastal food webs. Owing to tidal cycles, intertidal MPB diatoms are subjected to environmental conditions far more variable than the ones experienced by pelagic diatoms (e.g. light, temperature, salinity, desiccation and nutrient availability). Nevertheless, benthic diatoms evolved adaptation mechanisms to these harsh conditions, including the capacity to move within steep physical and chemical gradients, allowing them to perform photosynthesis efficiently. In this contribution, we will review present knowledge on the effects of dissolved inorganic carbon (DIC) availability on photosynthesis and productivity of diatom-dominated MPB. We present evidence of carbon limitation of photosynthesis in benthic diatom mats and highly productive MPB natural communities. Furthermore, we hypothesize that active vertical migration of epipelic motile diatoms could overcome local depletion of DIC in the photic layer, providing the cells alternately with light and inorganic carbon supply. The few available longer-term experiments on the effects of inorganic carbon enrichment on the productivity of diatom-dominated MPB have yielded inconsistent results. Therefore, further studies are needed to properly assess the response of MPB communities to increased CO 2 and ocean acidification related to climate change.This article is part of the themed issue 'The peculiar carbon metabolism in diatoms'., (© 2017 The Author(s).)

Several sacoglossan sea slug species feed on macroalgae and incorporate chloroplasts into tubular cells of their digestive diverticula. We investigated the role of the "stolen" chloroplasts (kleptoplasts) in the nutrition of the sea slug Elysia viridis and assessed how their abundance, distribution and photosynthetic activity were affected by light and starvation. Elysia viridis individuals feeding on the macroalga Codium tomentosum were compared with starved specimens kept in dark and low light conditions. A combination of variable Chl a fluorescence and hyperspectral imaging, and HPLC pigment analysis was used to evaluate the spatial and temporal variability of photopigments and of the photosynthetic capacity of kleptoplasts. We show increased loss of weight and body length in dark-starved E. viridis as compared to low light-starved sea slugs. A more pronounced decrease in kleptoplast abundance and lower photosynthetic electron transport rates were observed in dark-starved sea slugs than in low light-starved animals. This study presents strong evidence of the importance of kleptoplast photosynthesis for the nutrition of E. viridis in periods of food scarcity. Deprived of photosynthates, E. viridis could accelerate the breakdown of kleptoplasts in the dark to satisfy its' energy requirements.

The effects of dissolved inorganic carbon (DIC) availability on photosynthesis were studied in two estuarine intertidal microphytobenthos (MPB) communities and in the model diatom species Phaeodactylum tricornutum. Kinetics of DIC acquisition, measured with a liquid-phase oxygen electrode, showed higher K(1/2)(DIC) (0.31 mM) and Vm (7.78 nmol min(-1) µg (Chl a)(-1)) for MPB suspensions than for P. tricornutum (K(1/2)(DIC) = 0.23 mM; Vm = 4.64 nmol min(-1) µg (Chl a)(-1)), suggesting the predominance of species with lower affinity for DIC and higher photosynthetic capacity in the MPB. The net photosynthetic rate of the MPB suspensions reached saturation at a DIC concentration of 1-1.5 mM. This range was lower than the concentrations found in the interstitial water of the top 5-mm sediment layer, suggesting no limitation of photosynthesis by DIC in the MPB communities. Accordingly, carbon isotope discrimination revealed a moderate activity of CO2-concentrating mechanisms in the MPB. However, addition of NaHCO3 to intact MPB biofilms caused a significant increase in the relative maximum photosynthetic electron transport rate (rETR max) measured by imaging pulse-amplitude modulated chlorophyll a fluorescence. These results suggest local depletion of DIC at the photic layer of the sediment (the first few hundred µm), where MPB cells accumulate during diurnal low tides. This work provides the first direct experimental evidence of DIC limitation of photosynthesis in highly productive intertidal MPB communities.

Some sea slugs are capable of retaining functional sequestered chloroplasts (kleptoplasts) for variable periods of time. The mechanisms supporting the maintenance of these organelles in animal hosts are still largely unknown. Non-photochemical quenching (NPQ) and the occurrence of a xanthophyll cycle were investigated in the sea slugs Elysia viridis and E. chlorotica using chlorophyll fluorescence measurements and pigment analysis. The photoprotective capacity of kleptoplasts was compared to that observed in their respective algal source, Codium tomentosum and Vaucheria litorea. A functional xanthophyll cycle and a rapidly reversible NPQ component were found in V. litorea and E. chlorotica but not in C. tomentosum and E. viridis. To our knowledge, this is the first report of the absence of a functional xanthophyll cycle in a green macroalgae. The absence of a functional xanthophyll cycle in C. tomentosum could contribute to the premature loss of photosynthetic activity and relatively short-term retention of kleptoplasts in E. viridis. On the contrary, E. chlorotica displays one of the longest functional examples of kleptoplasty known so far. We speculate that different efficiencies of photoprotection and repair mechanisms of algal food sources play a role in the longevity of photosynthetic activity in kleptoplasts retained by sea slugs.

Kleptoplasty is a remarkable type of photosynthetic association, resulting from the maintenance of functional chloroplasts--the 'kleptoplasts'--in the tissues of a non-photosynthetic host. It represents a biologically unique condition for chloroplast and photosynthesis functioning, occurring in different phylogenetic lineages, namely dinoflagellates, ciliates, foraminiferans and, most interestingly, a single taxon of metazoans, the sacoglossan sea slugs. In the case of sea slugs, chloroplasts from macroalgae are often maintained as intracellular organelles in cells of these marine gastropods, structurally intact and photosynthetically competent for extended periods of time. Kleptoplasty has long attracted interest owing to the longevity of functional kleptoplasts in the absence of the original algal nucleus and the limited number of proteins encoded by the chloroplast genome. This review updates the state-of-the-art on kleptoplast photophysiology, focusing on the comparative analysis of the responses to light of the chloroplasts when in their original, macroalgal cells, and when sequestered in animal cells and functioning as kleptoplasts. It covers fundamental but ecologically relevant aspects of kleptoplast light responses, such as the occurrence of photoacclimation in hospite, operation of photoprotective processes and susceptibility to photoinhibition. Emphasis is given to host-mediated processes unique to kleptoplastic associations, reviewing current hypotheses on behavioural photoprotection and host-mediated enhancement of photosynthetic performance, and identifying current gaps in sacoglossan kleptoplast photophysiology research.

Some species of sacoglossan sea slugs can maintain functional chloroplasts from specific algal food sources in the cells of their digestive diverticula. These 'stolen' chloroplasts (kleptoplasts) can survive in the absence of the plant cell and continue to photosynthesize, in some cases for as long as one year. Within the Metazoa, this phenomenon (kleptoplasty) seems to have only evolved among sacoglossan sea slugs. Known for over a century, the mechanisms of interaction between the foreign organelle and its host animal cell are just now starting to be unravelled. In the study of sacoglossan sea slugs as photosynthetic systems, it is important to understand their relationship with light. This work reviews the state of knowledge on autotrophy as a nutritional source for sacoglossans and the strategies they have developed to avoid excessive light, with emphasis to the behavioural and physiological mechanisms suggested to be involved in the photoprotection of kleptoplasts. A special focus is given to the advantages and drawbacks of using pulse amplitude modulated fluorometry in photobiological studies addressing sacoglossan sea slugs. Finally, the classification of photosynthetic sacoglossan sea slugs according to their ability to retain functional kleptoplasts and the importance of laboratory culturing of these organisms are briefly discussed.

Imaging pulse amplitude modulated (Imaging-PAM) fluorometry is a breakthrough in the study of spatial heterogeneity of photosynthetic assemblages. However, Imaging and conventional PAM uses a different technology, making comparisons between these techniques doubtful. Thereby, photosynthetic processes were comparatively assessed using conventional (Junior PAM and PAM 101) and Imaging-PAM on intertidal microphytobenthos (MPB; mud and sand) and on cork oak leaves. Lower values of α (initial slope of the rETR, relative photosynthetic electron transport rate) vs E (incident photosynthetic active radiation) curve), ETR(max) (maximum relative ETR), E(k) (light saturation parameter) and F(v)/F(m) (maximum quantum efficiency of photosystem II of dark-adapted samples) were obtained using the Imaging-PAM. The level of discrepancy between conventional and Imaging-PAM systems was dependent on the type of sample, being more pronounced for MPB muddy sediments. This may be explained by differences in the depth integration of the fluorescence signal related to the thickness of the photosynthetic layer and in the light attenuation coefficients of downwelling irradiance. An additional relevant parameter is the taxonomic composition of the MPB, as cyanobacteria present in sandy sediments rendered different results with red and blue excitation light fluorometers. These findings emphasize the caution needed when interpreting chlorophyll fluorescence data of MPB communities., (© 2012 Wiley Periodicals, Inc. Photochemistry and Photobiology © 2012 The American Society of Photobiology.)

Simple Summary: Kleptoplasty is the capacity of a non-photosynthetic organism to acquire and maintain structurally intact chloroplasts from its algal food source(s), thereafter termed kleptoplasts. In animals, the capacity for long-term (several weeks to months) maintenance of photosynthetic active kleptoplasts is a unique characteristic in a handful of sea slugs, mostly within the genus Elysia. In this study, we investigated the role of kleptoplast photosynthesis on mucus production by the tropical sea slug Elysia crispata. Mucus secretion is paramount for mollusks, playing a role in locomotion, feeding, reproduction and protection. Limiting photosynthesis by rearing animals under reduced light led to lower mucus production and lower carbohydrate concentrations in the secreted mucus. This study indicates that production of mucus by kleptoplast-bearing sea slugs is supported by photosynthesis, confirming the biological relevance of kleptoplasty to the fitness of these peculiar mollusks. A handful of sea slugs of the order Sacoglossa are able to steal chloroplasts—kleptoplasts—from their algal food sources and maintain them functionally for periods ranging from several weeks to a few months. In this study, we investigated the role of kleptoplast photosynthesis on mucus production by the tropical sea slug Elysia crispata. Animals reared for 5 weeks in quasi dark (5 μmol photons m−2 s−1) showed similar growth to those under regular light (60–90 μmol photons m−2 s−1), showing that kleptoplast photosynthesis was not relevant for growth when sea slugs were fed ad libitum. However, when subjected to short-term desiccation stress, animals reared under regular light produced significantly more mucus. Furthermore, the carbohydrate content of secreted mucus was significantly lower in slugs limited in the photosynthetic activity of their kleptoplasts by quasi-dark conditions. This study indicates that photosynthesis supports the synthesis of protective mucus in kleptoplast-bearing sea slugs. [ABSTRACT FROM AUTHOR]

Some sea slugs are able to steal functional chloroplasts (kleptoplasts) from their algal food sources, but the role and relevance of photosynthesis to the animal host remain controversial. While some researchers claim that kleptoplasts are slowly digestible 'snacks', others advocate that they enhance the overall fitness of sea slugs much more profoundly. Our analysis shows light-dependent incorporation of 13C and 15N in the albumen gland and gonadal follicles of the sea slug Elysia timida, representing translocation of photosynthates to kleptoplast-free reproductive organs. Long-chain polyunsaturated fatty acids with reported roles in reproduction were produced in the sea slug cells using labelled precursors translocated from the kleptoplasts. Finally, we report reduced fecundity of E. timida by limiting kleptoplast photosynthesis. The present study indicates that photosynthesis enhances the reproductive fitness of kleptoplast-bearing sea slugs, confirming the biological relevance of this remarkable association between a metazoan and an algal-derived organelle. [ABSTRACT FROM AUTHOR]

Elysia crispata is a sacoglossan sea slug that retains intracellular, functional chloroplasts stolen from their macroalgal food sources. Elysia crispata juveniles start feeding on the algae following metamorphosis, engulfing chloroplasts and turning green. In laboratory-reared animals, we report one juvenile "albino" specimen unable to retain chloroplasts. Within 6 weeks post-metamorphosis, the aposymbiotic sea slug was significantly smaller than its chloroplast-bearing siblings. This evidence highlights that chloroplast acquisition is required for the normal development of E. crispata. [ABSTRACT FROM AUTHOR]

Some sacoglossan sea slugs incorporate intracellular functional algal chloroplasts, a process termed kleptoplasty. "Stolen" chloroplasts (kleptoplasts) can remain photosynthetically active up to several months, contributing to animal nutrition. Whether this contribution occurs by means of translocation of photosynthesis-derived metabolites from functional kleptoplasts to the animal host or by simple digestion of such organelles remains controversial. Imaging of 13C and 15N assimilation over a 12-h incubation period of Elysia viridis sea slugs showed a light-dependent incorporation of carbon and nitrogen, observed first in digestive tubules and followed by a rapid accumulation into chloroplast-free organs. Furthermore, this work revealed the presence of 13C-labeled long-chain fatty acids (FA) typical of marine invertebrates, such as arachidonic (20:4n-6) and adrenic (22:4n-6) acids. The time frame and level of 13C- and 15N-labeling in chloroplast-free organs indicate that photosynthesis-derived primary metabolites were made available to the host through functional kleptoplasts. The presence of specific 13C-labeled long-chain FA, absent from E. viridis algal food, indicates animal based-elongation using kleptoplast-derived FA precursors. Finally, carbon and nitrogen were incorporated in organs and tissues involved in reproductive functions (albumin gland and gonadal follicles), implying a putative role of kleptoplast photosynthesis in the reproductive fitness of the animal host. [ABSTRACT FROM AUTHOR]

Diatom-dominated microphytobenthos (MPB) is the main primary producer of many intertidal and shallow subtidal environments, being therefore of critical importance to estuarine and coastal food webs. Owing to tidal cycles, intertidal MPB diatoms are subjected to environmental conditions far more variable than the ones experienced by pelagic diatoms (e.g. light, temperature, salinity, desiccation and nutrient availability). Nevertheless, benthic diatoms evolved adaptation mechanisms to these harsh conditions, including the capacity to move within steep physical and chemical gradients, allowing them to perform photosynthesis efficiently. In this contribution, we will review present knowledge on the effects of dissolved inorganic carbon (DIC) availability on photosynthesis and productivity of diatom-dominated MPB. We present evidence of carbon limitation of photosynthesis in benthic diatom mats and highly productive MPB natural communities. Furthermore, we hypothesize that active vertical migration of epipelic motile diatoms could overcome local depletion of DIC in the photic layer, providing the cells alternately with light and inorganic carbon supply. The few available longer-term experiments on the effects of inorganic carbon enrichment on the productivity of diatom-dominated MPB have yielded inconsistent results. Therefore, further studies are needed to properly assess the response of MPB communities to increased CO2 and ocean acidification related to climate change. [ABSTRACT FROM AUTHOR]

Background Microphytobenthos (MPB) are the main primary producers of many intertidal and shallow subtidal environments. Although these coastal ecosystems are particularly vulnerable to anthropogenic activities, little is known on the effects of climate change variables on the structure and productivity of MPB communities. In this study, the effects of elevated temperature and CO2 on intertidal MPB biomass, species composition and photosynthetic performance were studied using a flow-through experimental life support system.Results Elevated temperature had a detrimental effect on MPB biomass and photosynthetic performance under both control and elevated CO2. Furthermore, elevated temperature led to an increase of cyanobacteria and a change in the relative abundance of major benthic diatom species present in the MPB community. The most abundant motile epipelic species Navicula spartinetensis and Gyrosigma acuminatum were in part replaced by tychoplanktonic species (Minidiscus chilensis and Thalassiosira cf. pseudonana) and the motile epipelic Nitzschia cf. aequorea and N. cf. aurariae. Elevated CO2 had a beneficial effect on MPB biomass, but only at the lower temperature. It is possible that elevated CO2 alleviated local depletion of dissolved inorganic carbon resulting from high cell abundance at the sediment photic layer. No significant effect of elevated CO2 was detected on the relative abundance of major groups of microalgae and benthic diatom species. Conclusions The interactive effects of elevated temperature and CO2 may have an overall detrimental impact on the structure and productivity of intertidal MPB, and eventually in related ecosystem services. [ABSTRACT FROM AUTHOR]

The article reports the application of laser-induced fluorescence (LIF) for the assessment of macroalgae communities of estuarine intertidal areas. The method was applied for the characterisation of fifteen intertidal macroalgae species of the Tagus estuary, Portugal, and adjacent coastal area. Three bands characterised the LIF spectra of red macroalgae with emission maxima in the ranges 577–583 nm, 621–642 nm and 705–731 nm. Green and brown macroalgae showed one emission maximum in the red region (687–690 nm) and/or one in the far-red region (726–732 nm). Characteristics of LIF emission spectra were determined by differences in the main fluorescing pigments: phycoerythrin, phycocyanin and chlorophyll a (Chl a ). In the green and brown macroalgae groups, the relative significance of the two emission maxima seems to be related to the thickness of the photosynthetic layer. In thick macroalgae, like Codium tomentosum or Fucus vesiculosus , the contribution of the far-red emission fluorescence peak was more significant, most probably due to re-absorption of the emitted red Chl a fluorescence within the dense photosynthetic layer. Similarly, an increase in the number of layers of the thin-blade green macroalgae Ulva rigida caused a shift to longer wavelengths of the red emission maximum and the development of a fluorescence peak at the far-red region. Water loss from Ulva 's algal tissue also led to a decrease in the red/far-red Chl fluorescence ratio (F 685 /F 735 ), indicating an increase in the density of chloroplasts in the shrinking macroalgal tissue during low tide exposure. [ABSTRACT FROM AUTHOR]

Abstract: Intertidal microphytobenthos (MPB) has been found to maintain high productivity rates despite the variability in various key environmental parameters, namely rapid temperature changes during emersion. The effects of short-term (30 min and 2 h) changes in temperature (15, 25, 35 and 42 °C) on the photosynthetic activity of two intertidal MPB communities (Trancão and Alcochete) of the Tagus estuary were studied using imaging pulse amplitude modulated (Imaging-PAM) fluorometry. MPB communities differed in species composition and size-class distribution: Trancão was dominated by diatoms of the size-class 100–250 μm3, particularly Navicula cf. phyllepta, whereas Alcochete had higher relative abundances for size-class 250–1000 μm3, dominated by a mixture of diatom species of the genera Navicula, Thalassiosira and Gyrosigma. The Trancão MPB community had higher photosynthetic capacity (higher ETR max), was photoacclimated to higher irradiances (higher E k) and had lower efficiency at limiting irradiances (lower α). The different taxonomic composition and size-class distribution could explain the observed results, as small cells are usually more active due to larger surface to volume ratios. Photosynthetic capacities of the two studied MPB communities increased with temperature until 35 °C. Photosynthetic efficiencies were not affected by temperature in the 15–35 °C range and both ETR max and α decreased at the extreme temperature of 42 °C. MPB communities were able to increase photosynthetic capacity and productivity under transient exposure to high sediment temperatures, similar to that observed during summer midday low tides. [Copyright &y& Elsevier]