Symbiosis of Algae and Invertebrates: Aspects of the Symbiont Surface and the Host-Symbiont Interface

Muscatine, Leonard; Pool, R.R.; Trench, Robert K.

doi:10.2307/3225518

Cited by 77 publications

(49 citation statements)

References 40 publications

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“…However, these vacuoles also resemble the accumulation bodies of encysting dinoflagellates, which are a form of autophagic vesicle (22). Therefore, the increase of vacuole size may be associated with alimentary canal and cellular invasion, programmed cell death (33), or even algal cell encystment (22,26).…”

Section: Discussionmentioning

confidence: 99%

“…This resembles endosymbioses between cyanobacterial Prochloron sp. and didemnid ascidian hosts (24), dinoflagellates of the genus Symbiodinium and cnidarian, poriferan, mollusk, platyhelminth, and foraminiferan hosts (1,25), and between the green alga Chlorella and ciliate, poriferan, and cnidarian hosts (26). However, the Ambystoma-alga symbiosis is unique in several features.…”

Section: Discussionmentioning

confidence: 99%

“…This is similar to the association between Platymonas convolutae (a prasinophycean green alga) and acoel flatworms of the genus Convoluta sp., but unlike the association of Chlorella sp. (a trebouxiophycean green alga) with cnidarian hydras (26), which are contained in a symbiosomal membrane.…”

Section: Discussionmentioning

confidence: 99%

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Intracellular invasion of green algae in a salamander host

Kerney

Kim

Hangarter

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

112

122

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The association between embryos of the spotted salamander (Ambystoma maculatum) and green algae ("Oophila amblystomatis" Lamber ex Printz) has been considered an ectosymbiotic mutualism. We show here, however, that this symbiosis is more intimate than previously reported. A combination of imaging and algal 18S rDNA amplification reveals algal invasion of embryonic salamander tissues and cells during development. Algal cells are detectable from embryonic and larval Stages 26-44 through chlorophyll autofluorescence and algal 18S rDNA amplification. Algal cell ultrastructure indicates both degradation and putative encystment during the process of tissue and cellular invasion. Fewer algal cells were detected in later-stage larvae through FISH, suggesting that the decline in autofluorescent cells is primarily due to algal cell death within the host. However, early embryonic egg capsules also contained encysted algal cells on the inner capsule wall, and algal 18S rDNA was amplified from adult reproductive tracts, consistent with oviductal transmission of algae from one salamander generation to the next. The invasion of algae into salamander host tissues and cells represents a unique association between a vertebrate and a eukaryotic alga, with implications for research into cell-cell recognition, possible exchange of metabolites or DNA, and potential congruence between host and symbiont population structures.photosymbiont | endosymbiosis | amphibian | chlorophyte

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Intracellular invasion of green algae in a salamander host

Kerney

Kim

Hangarter

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

112

122

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“…The discovery that the green 'bodies' were plastids was made in 1965 after microscopic observations of Elysia atroviridis (Kawaguti and Yamasu, 1965). Research publications over the next 10-20years, principally by Trench (Trench, 1969;Trench et al, 1969;Trench et al, 1972;Trench et al, 1973a;Trench et al, 1973b;Muscatine et al, 1975;Trench, 1975), but also by Clark (Clark and Busacca, 1978;Clark et al, 1990), Jensen (Jensen, 1986), Hinde (Hinde, 1980;Hinde and Smith, 1972;Hinde and Smith, 1974) and others (Green and Muscatine, 1972;Graves et al, 1979), greatly advanced our understanding of functional kleptoplasty in sea slugs, in particular at the ecological and physiological levels.…”

Section: Introductionmentioning

confidence: 99%

The making of a photosynthetic animal

Rumpho

Pelletreau

Moustafa

et al. 2011

Journal of Experimental Biology

147

124

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SummarySymbiotic animals containing green photobionts challenge the common perception that only plants are capable of capturing the sun's rays and converting them into biological energy through photoautotrophic CO 2 fixation (photosynthesis). 'Solar-powered' sacoglossan molluscs, or sea slugs, have taken this type of symbiotic association one step further by solely harboring the photosynthetic organelle, the plastid (chloroplast). One such sea slug, Elysia chlorotica, lives as a 'plant' when provided with only light and air as a result of acquiring plastids during feeding on its algal prey Vaucheria litorea. The captured plastids (kleptoplasts) are retained intracellularly in cells lining the digestive diverticula of the sea slug, a phenomenon sometimes referred to as kleptoplasty. Photosynthesis by the plastids provides E. chlorotica with energy and fixed carbon for its entire lifespan of 10months. The plastids are not transmitted vertically (i.e. are absent in eggs) and do not undergo division in the sea slug. However, de novo protein synthesis continues, including plastid-and nuclear-encoded plastid-targeted proteins, despite the apparent absence of algal nuclei. Here we discuss current data and provide hypotheses to explain how long-term photosynthetic activity is maintained by the kleptoplasts. This fascinating 'green animal' provides a unique model to study the evolution of photosynthesis in a multicellular heterotrophic organism. Supplementary material available online at

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“…Stony corals (Scleractinia) can form mutualistic symbioses with photosynthetic dinoflagellates of the genus Symbiodinium that are based on nutritional exchange and allow coral reef growth in oligotrophic marine environments (Muscatine et al, 1975;Trench, 1979). These reef-building corals provide the foundation for the coral reef ecosystem and a habitat for millions of marine species.…”

Section: Introductionmentioning

confidence: 99%

Unfolding the secrets of coral–algal symbiosis

et al. 2014

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Dinoflagellates from the genus Symbiodinium form a mutualistic symbiotic relationship with reefbuilding corals. Here we applied massively parallel Illumina sequencing to assess genetic similarity and diversity among four phylogenetically diverse dinoflagellate clades (A, B, C and D) that are commonly associated with corals. We obtained more than 30 000 predicted genes for each Symbiodinium clade, with a majority of the aligned transcripts corresponding to sequence data sets of symbiotic dinoflagellates and o2% of sequences having bacterial or other foreign origin. We report 1053 genes, orthologous among four Symbiodinium clades, that share a high level of sequence identity to known proteins from the SwissProt (SP) database. Approximately 80% of the transcripts aligning to the 1053 SP genes were unique to Symbiodinium species and did not align to other dinoflagellates and unrelated eukaryotic transcriptomes/genomes. Six pathways were common to all four Symbiodinium clades including the phosphatidylinositol signaling system and inositol phosphate metabolism pathways. The list of Symbiodinium transcripts common to all four clades included conserved genes such as heat shock proteins (Hsp70 and Hsp90), calmodulin, actin and tubulin, several ribosomal, photosynthetic and cytochrome genes and chloroplast-based hemecontaining cytochrome P450, involved in the biosynthesis of xanthophylls. Antioxidant genes, which are important in stress responses, were also preserved, as were a number of calcium-dependent and calcium/calmodulin-dependent protein kinases that may play a role in the establishment of symbiosis. Our findings disclose new knowledge about the genetic uniqueness of symbiotic dinoflagellates and provide a list of homologous genes important for the foundation of coral-algal symbiosis.

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Symbiosis of Algae and Invertebrates: Aspects of the Symbiont Surface and the Host-Symbiont Interface

Cited by 77 publications

References 40 publications

Intracellular invasion of green algae in a salamander host

Intracellular invasion of green algae in a salamander host

The making of a photosynthetic animal

Unfolding the secrets of coral–algal symbiosis

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