Photo-movement in the sea anemone Aiptasia influenced by light quality and symbiotic association

Foo, Shawna A.; Liddell, Lauren; Grossman, Arthur R.; Caldeira, Ken

doi:10.1007/s00338-019-01866-w

Cited by 20 publications

(23 citation statements)

References 47 publications

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“…For example, one opsin from the actinarian-specific subtype 2.2 ASO-II group (ASO-II.12, dark green), and two from the subtype 1 and subtype 2.1 ASO-II group (ASO-II.7 and ASO-II.11, yellow) show significantly higher expression levels in symbiotic anemones when compared with their aposymbiotic (non-symbiotic) counterparts. This is consistent with previous findings that symbiotic association influences photo-movement in Aiptasia ( Foo et al. 2020 ) and suggests that host perception of environmental light by opsin-mediated light sensing may change in response to symbiosis, for example to adjust the levels of sunlight exposure for optimal photosynthesis rates.…”

Section: Resultssupporting

confidence: 92%

Photoreceptor Diversification Accompanies the Evolution of Anthozoa

Gornik

Bergheim

Morel

et al. 2020

Molecular Biology and Evolution

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Anthozoan corals are an ecologically important group of cnidarians, which power the productivity of reef ecosystems. They are sessile, inhabit shallow, tropical oceans and are highly dependent on sun- and moonlight to regulate sexual reproduction, phototaxis and photosymbiosis. However, their exposure to high levels of sunlight also imposes an increased risk of UV-induced DNA damage. How have these challenging photic environments influenced photoreceptor evolution and function in these animals? To address this question, we initially screened the cnidarian photoreceptor repertoire for Anthozoa-specific signatures by a broad scale evolutionary analysis. We compared transcriptomic data of more than 36 cnidarian species and revealed a more diverse photoreceptor repertoire in the anthozoan subphylum than in the subphylum Medusozoa. We classified the three principle opsin classes into distinct subtypes and showed that Anthozoa retained all three classes, which diversified into at least 6 subtypes. In contrast, in Medusozoa only one class with a single subtype persists. Similarly, in Anthozoa we documented three photolyase (PL) classes and two cryptochrome (CRY) classes, while CRYs are entirely absent in Medusozoa. Interestingly, we also identified one anthozoan CRY class (AnthoCRYs), which exhibited unique tandem duplications of the core functional domains. We next explored the functionality of anthozoan photoreceptors in the model species Exaiptasia diaphana (Aiptasia), which recapitulates key photo-behaviors of corals. We show that the diverse opsin genes are differentially expressed in important life-stages common to reef-building corals and Aiptasia and that CRY expression is light-regulated. We thereby provide important clues linking coral evolution with photoreceptor diversification.

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Section: Resultssupporting

confidence: 92%

Photoreceptor Diversification Accompanies the Evolution of Anthozoa

Gornik

Bergheim

Morel

et al. 2020

Molecular Biology and Evolution

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“…For example, one opsin from the actiniarian-specific ASO-II group (ASO-II.12, dark green), and two from the ASO-II group (ASO-II.7 and ASO-II.11, yellow) show significantly higher expression levels in symbiotic anemones when compared to their aposymbiotic (nonsymbiotic) counterparts. This is consistent with previous findings that symbiotic association influences photo-movement in Aiptasia [8] and suggests that host perception of environmental light by opsin-mediated light-sensing may change in response to symbiosis, for example to adjust the levels of sunlight exposure for optimal photosynthesis rates.…”

Section: Life-stage Symbiotic State and Tissue Type-specific Opsin Esupporting

confidence: 92%

“…Other important photo-induced behaviours of cnidarians include phototaxis and diurnal migration [7][8][9][10]. Given the strong dependence of the cnidarian lifestyle upon environmental lighting conditions, a key question is: which mechanisms mediate these broad ranging effects of light?…”

Section: Introductionmentioning

confidence: 99%

Photoreceptor complexity accompanies adaptation to challenging marine environments in Anthozoa

Gornik

Bergheim

Foulkes

et al. 2020

Preprint

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12Light represents a key environmental factor, which shapes the physiology and evolution of 13 most organisms. Notable illustrations of this are reef-building corals (Anthozoa), which 14 adapted to shallow, oligotrophic, tropical oceans by exploiting light from the sun and the 15 moon to regulate various aspects of physiology including sexual reproduction, phototaxis and 16 photosymbiosis. Together with the Medusozoa, (including jellyfish), the Anthozoa constitute 17 the ancestral metazoan phylum cnidaria. While light perception in Medusozoa has received 18 attention, the mechanisms of light sensing in Anthozoa remain largely unknown. Cnidaria 19 express two principle groups of light-sensing proteins: opsins and photolyases/cryptochromes. 20By inspecting the genomic loci encoding these photoreceptors in over 35 cnidarian species, 21 we reveal that Anthozoa have substantially expanded and diversified their photoreceptor 22 repertoire. We confirm that, in contrast to Medusozoa, which retained one opsin class, 23 anthozoans possess all three urmetazoan opsin classes. We show that anthozoans also evolved 24 an extra sub-group (actinarian ASO-IIs). Strikingly, we reveal that cryptochromes including 25 CRY-IIs are absent in Medusozoa, while the Anthozoa retained these and evolved an 26 additional, novel cryptochrome class (AnthoCRYs), which contain unique tandem 27 duplications of up to 6 copies of the PHR region. We explored the functionality of these 28 photoreceptor groups by structure-function and gene expression analysis in the anthozoan 29 model species Exaiptasia pallida (Aiptasia), which recapitulates key photo-behaviors of 30 corals. We identified an array of features that we speculate reflect adaptations to shallow 31 aquatic environments, moonlight-induced spawning synchronization and photosymbiosis. We 32 further propose that photoreceptor complexity and diversity in Anthozoa reflects adaptation to 33 challenging habitats. 34 35 36 37Light from both the sun and moon dominates the life of many organisms and has had a 38 profound impact on their evolution. While the mechanisms underlying light sensing have 39 been studied in a comparatively small group of animal models, little is known about the 40 impact of light on the physiology and evolution of more ancestral metazoan groups such as 41 the cnidarians. These are basal, non-bilaterian, eumetazoan animals divided into two major 42 groups, the Anthozoa and the Medusozoa ( Figure 1A; [1], which both exploit a complexity of 43 sunlight and moonlight-based cues to regulate various aspects of their physiology and 44 behaviour ( Figure 1B). Notable examples of highly light-dependent cnidarians are reef-45 building corals and anemones (both Anthozoa; Figure 1A), many of which live in an 46 evolutionary ancient symbiotic relationship with eukaryotic, photosynthetic dinoflagellates of 47 the Symbiodiniaceae family [2, 3]. The symbionts use sunlight to provide essential 48 photosynthetically-fixed nutrients to their hosts to support host survival in otherwise 49 oligo...

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“…However, none of the experiments we conducted supported this hypothesis. First, M. leonina did not express positive phototaxis that has been observed in many invertebrates that have symbiotic relationships with photosynthetic zooxanthellae, including cnidarians ( Pearse 1974 ; Yamashiro and Nishira 1995 ; Foo et al 2020 , flatworms ( Serȏdio et al 2011 ; Nissen et al 2015 , and sea slugs ( Rahat and Monselise 1979 ; Gallop et al 1980 ; Weaver and Clark 1981 . In some animals, phototaxis is dependent upon the presence of symbiotic zooxanthellae ( Pearse 1974 ; Foo et al 2020 .…”

Section: Discussionmentioning

confidence: 96%

“…First, M. leonina did not express positive phototaxis that has been observed in many invertebrates that have symbiotic relationships with photosynthetic zooxanthellae, including cnidarians ( Pearse 1974 ; Yamashiro and Nishira 1995 ; Foo et al 2020 , flatworms ( Serȏdio et al 2011 ; Nissen et al 2015 , and sea slugs ( Rahat and Monselise 1979 ; Gallop et al 1980 ; Weaver and Clark 1981 . In some animals, phototaxis is dependent upon the presence of symbiotic zooxanthellae ( Pearse 1974 ; Foo et al 2020 . In others, positive phototaxis may occur, but only at lower intensities of light ( Gallop et al 1980 ; Weaver and Clark 1981 ; Serȏdio et al 2011 ), possibly because in photosynthetic organisms, excess light can be damaging ( Haeder et al 1995 ; Cruz et al 2013 .…”

Section: Discussionmentioning

confidence: 96%

The Digestive Diverticula in the Carnivorous Nudibranch, Melibe leonina, Do Not Contain Photosynthetic Symbionts

Watson

Bourque

Sullivan

et al. 2021

Integrative Organismal Biology

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A number of nudibranchs, including Melibe engeli and Melibe pilosa, harbor symbiotic photosynthetic zooxanthellae. Melibe leonina spends most of its adult life on seagrass or kelp, capturing planktonic organisms in the water column with a large, tentacle-lined oral hood that brings food to its mouth. M. leonina also has an extensive network of digestive diverticula, located just beneath its translucent integument, that are typically filled with pigmented material likely derived from ingested food. Therefore, the focus of this project was to test the hypothesis that M. leonina accumulate symbiotic photosynthetic dinoflagellates in these diverticula. First, we conducted experiments to determine if M. leonina exhibits a preference for light, which would allow chloroplasts that it might be harboring to carry out photosynthesis. We found that most M. leonina preferred shaded areas and spent less time in direct sunlight. Second, we examined the small green circular structures in cells lining the digestive diverticula. Like chlorophyll, they exhibited autofluorescence when illuminated at 480 nm, and they were also about the same size as chloroplasts and symbiotic zooxanthellae. However, subsequent electron microscopy found no evidence of chloroplasts in the digestive diverticula of M. leonina; the structures exhibiting autofluorescence at 480 nm were most likely heterolysosomes, consistent with normal molluscan digestion. Third, we did not find evidence of altered oxygen consumption or production in M. leonina housed in different light conditions, suggesting the lack of any significant photosynthetic activity in sunlight. Fourth, we examined the contents of the diverticula, using HPLC, thin layer chromatography, and spectroscopy. The results of these studies indicate that the diverticula did not contain any chlorophyll, but rather harbored other pigments, such as astaxanthin, which likely came from crustaceans in their diet. Together, all of these data suggest that M. leonina does sequester pigments from its diet, but not for the purpose of symbiosis with photosynthetic zooxanthellae. Considering the translucent skin of M. leonina, the pigmented diverticula may instead provide camouflage.

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Photo-movement in the sea anemone Aiptasia influenced by light quality and symbiotic association

Cited by 20 publications

References 47 publications

Photoreceptor Diversification Accompanies the Evolution of Anthozoa

Photoreceptor Diversification Accompanies the Evolution of Anthozoa

Photoreceptor complexity accompanies adaptation to challenging marine environments in Anthozoa

The Digestive Diverticula in the Carnivorous Nudibranch, Melibe leonina, Do Not Contain Photosynthetic Symbionts

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