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Functional Chloroplasts in Metazoan Cells - A Unique Evolutionary Strategy in Animal Life

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Functional Chloroplasts in Metazoan Cells - A Unique Evolutionary Strategy in Animal Life

Katharina Händeler et al. Front Zool.

Abstract

Background: Among metazoans, retention of functional diet-derived chloroplasts (kleptoplasty) is known only from the sea slug taxon Sacoglossa (Gastropoda: Opisthobranchia). Intracellular maintenance of plastids in the slug's digestive epithelium has long attracted interest given its implications for understanding the evolution of endosymbiosis. However, photosynthetic ability varies widely among sacoglossans; some species have no plastid retention while others survive for months solely on photosynthesis. We present a molecular phylogenetic hypothesis for the Sacoglossa and a survey of kleptoplasty from representatives of all major clades. We sought to quantify variation in photosynthetic ability among lineages, identify phylogenetic origins of plastid retention, and assess whether kleptoplasty was a key character in the radiation of the Sacoglossa.

Results: Three levels of photosynthetic activity were detected: (1) no functional retention; (2) short-term retention lasting about one week; and (3) long-term retention for over a month. Phylogenetic analysis of one nuclear and two mitochondrial loci revealed reciprocal monophyly of the shelled Oxynoacea and shell-less Plakobranchacea, the latter comprising a monophyletic Plakobranchoidea and paraphyletic Limapontioidea. Only species in the Plakobranchoidea expressed short- or long-term kleptoplasty, most belonging to a speciose clade of slugs bearing parapodia (lateral flaps covering the dorsum). Bayesian ancestral character state reconstructions indicated that functional short-term retention arose once in the last common ancestor of Plakobranchoidea, and independently evolved into long-term retention in four derived species.

Conclusion: We propose a sequential progression from short- to long-term kleptoplasty, with different adaptations involved in each step. Short-term kleptoplasty likely arose as a deficiency in plastid digestion, yielding additional energy via the release of fixed carbon. Functional short-term retention was an apomorphy of the Plakobranchoidea, but the subsequent evolution of parapodia enabled slugs to protect kleptoplasts against high irradiance and further prolong plastid survival. We conclude that functional short-term retention was necessary but not sufficient for an adaptive radiation in the Plakobranchoidea, especially in the genus Elysia which comprises a third of all sacoglossan species. The adaptations necessary for long-term chloroplast survival arose independently in species feeding on different algal hosts, providing a valuable study system for examining the parallel evolution of this unique trophic strategy.

Figures

Figure 1
Figure 1
Representative sacoglossans showing habitus typical of major plakobranchacean clades. Approximation of length is given. (A) Cyerce nigricans on Chlorodesmis fastigiata (Lizard Island, Great Barrier Reef; 4 cm), (B) Polybranchia orientalis (Lizard Island, Great Barrier Reef; 2 cm), (C) Elysia ornata (Lizard Island, Great Barrier Reef; 2 cm), (D) Elysia crispata on sediment (Dominican Republic; 4 cm), (E) Plakobranchus ocellatus (Lizard Island, Great Barrier Reef; 4 cm), (F) Elysia pusilla (Maldives; 1 cm), (G) Elysia tomentosa (Lizard Island, Great Barrier Reef; 1.5 cm) (H) Thuridilla carlsoni (Lizard Island, Great Barrier Reef; 2 cm). (I) Elysia viridis (Mediterranean Sea, animal placed on brown algae; 1,5 cm). (J) Thuridilla hopei (Mediterranean Sea, 2 cm).
Figure 2
Figure 2
Representative sacoglossans on their host algae. Approximation of length is given. (A) Costasiella cf. kuroshimae on Avrainvillea erecta (Lizard Island, Great Barrier Reef; 1 cm), (B) Elysia spec. 5 found affiliated with Chlorodesmis fastigiata (Lizard Island, Great Barrier Reef; 1 cm), (C) Ercolania kencolesi inside of Boergesenia cf. forbesii (Lizard Island, Great Barrier Reef; 0.5 cm), (D) Lobiger viridis on Caulerpa spec. (Lizard Island, Great Barrier Reef; 0.5 cm), (E) Bosellia mimetica on Halimeda tuna (Mediterranean Sea; 1 cm).
Figure 3
Figure 3
Phylogeny of Sacoglossa. A Bayesian analysis was performed on concatenated partial gene sequences of the nuclear 28S, the mitochondrial 16S, and the mitochondrial coxI (1st and 2nd positions only) loci. Shown is a 50% majority-rule consensus tree generated from the post-burn-in tree sample. Numbers above branches are posterior probability support, black dot: posterior probability = 100, black triangle: posterior probability = 95 - 99.
Figure 4
Figure 4
Yield values (PAM measurements) of Costasiella cf. kuroshimae compared to Plakobranchus ocellatus. Y is the yield value of chloroplasts' photosynthesis that has been measured every day after capture of animal. Y is plotted against the days of starvation. Trendlines are calculated in Excel. In every figure the species with the longest measured ability of chloroplasts' function, Plakobranchus ocellatus, is shown as reference. Black trendline indicates no functional retention. Trendlines of species with long-term retention are green. Standard deviation and mean values are given.
Figure 5
Figure 5
Yield values (PAM measurements) of the genera Bosellia and Thuridilla compared to Plakobranchus ocellatus. Y is the yield value of chloroplasts' photosynthesis that has been measured every day after capture of animal. Y is plotted against the days of starvation. Trendlines are calculated in Excel. In every figure the species with the longest measured ability of chloroplasts' function, Plakobranchus ocellatus, is shown as reference. Trendlines of species that had short-term retention are blue. Trendlines of species with long-term retention are green. For better clarity standard deviation and mean values are not included.
Figure 6
Figure 6
Yield values (PAM measurements) of the genus Elysia compared to Plakobranchus ocellatus. Y is the yield value of chloroplasts' photosynthesis that has been measured every day after capture of animal. Y is plotted against the days of starvation. Trendlines are calculated in Excel. In every figure the species with the longest measured ability of chloroplasts' function, Plakobranchus ocellatus, is shown as reference. Black trendlines indicate no functional retention. Trendlines of species that had short-term retention are blue. Trendlines of species with long-term retention are green. For better clarity standard deviation and mean values are not included.
Figure 7
Figure 7
Evolutionary patterns in photosynthetic activity and host use in the Sacoglossa. Information on host algae was taken from Händeler & Wägele [26], Händeler et al. (unpublished data), Teugels et al. [98], Trowbridge [99]; Krug et al. [100] and authors' data. Empty square: no-functional chloroplast retention, blue square: functional short-term chloroplast retention, green star: functional long-term chloroplast retention.

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