Two-step evolution of endosymbiosis between hydra and algae

Ishikawa, Masakazu; Shimizu, Hiroshi; Nozawa, Masahiro; Ikeo, Kazuho; Gojobori, Takashi

doi:10.1016/j.ympev.2016.07.010

Cited by 9 publications

(7 citation statements)

References 31 publications

(34 reference statements)

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“…Similarity of gene expression involved in phagocytosis and nematocytes between the acquired symbiotic strain and the native symbiotic strain. Ishikawa et al 12 postulated that hydras that did not have "endosymbiotic potential" with Chlorococcum evolved into native symbiotic hydras in a step-by-step process by first becoming hydras with endosymbiotic potential. Some Hydra strains with endosymbiotic potential can acquire symbionts by artificial or spontaneous transmission [10][11][12]14 .…”

Section: Resultsmentioning

confidence: 99%

“…is known to be able to establish the symbiotic relationship with brown hydra among algae species in the genus Chlorococcum 10 . Interestingly, many strains of H. vulgaris can incorporate the symbiotic algae by artificial introduction to the gastric cavity 11,12 , despite the rarity of symbiotic H. vulgaris strains in the wild. However, most of the artificially introduced symbionts are not stable in most host strains, and the tolerance to starvation of the host polyp is decreased in the symbiotic strains of H. vulgaris compared with the non-symbiotic strains 11,13 .…”

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confidence: 99%

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Immature symbiotic system between horizontally transmitted green algae and brown hydra

Miyokawa

Kanaya

Itoh

et al. 2021

Sci Rep

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Some strains of brown hydra (Hydra vulgaris) are able to harbor the green algae Chlorococcum in their endodermal epithelial cells as symbionts. However, the relationship between brown hydra and chlorococcum is considered to be incipient symbiosis because most artificially introduced symbionts are not stable and because symbiotic H. vulgaris strains are rare in the wild. In this study, we compared the gene expression levels of the newly established symbiotic hydra (strain 105G), the native symbiotic strain (J7), and their non-symbiotic polyps to determine what changes would occur at the early stage of the evolution of symbiosis. We found that both the 105G and J7 strains showed comparable expression patterns, exhibiting upregulation of lysosomal enzymes and downregulation of genes related to nematocyte development and function. Meanwhile, genes involved in translation and the respiratory chain were upregulated only in strain 105G. Furthermore, treatment with rapamycin, which inhibits translation activity, induced the degeneration of the symbiotic strains (105G and J7). This effect was severe in strain 105G. Our results suggested that evolving the ability to balance the cellular metabolism between the host and the symbiont is a key requirement for adapting to endosymbiosis with chlorococcum.

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Section: Resultsmentioning

confidence: 99%

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confidence: 99%

Immature symbiotic system between horizontally transmitted green algae and brown hydra

Miyokawa

Kanaya

Itoh

et al. 2021

Sci Rep

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“…asymbiotic strains of Hydra vulgaris (Hydrozoa) may establish endosymbiosis with Chlorococcum green algae under laboratory conditions (Ishikawa et al . 2016).…”

Section: Discussionmentioning

confidence: 99%

“…On the other hand, many cnidarians such as the actiniarian Nematostella vectensis ( Hand and Uhlinger 1992), the jellyfishes Clytia hemisphaerica (hydrozoan) (Houliston, Momose and Manuel 2010) and Aurelia aurita (schyphozoan) (Hernroth and Gröndahl 1983), some strains of the freshwater-living polyp Hydra vulgaris (Ishikawa et al . 2016), and even some scleractinian corals (Daly et al . 2007; Barbeitos, Romano and Lasker 2010) are asymbiotic.…”

Section: Introductionmentioning

confidence: 99%

Photosynthetic capacity of the endosymbiotic dinoflagellate Cladocopium sp. is preserved during digestion of its jellyfish host Mastigias papua by the anemone Entacmaea medusivora

Luna

Dang

Cardol

et al. 2019

FEMS Microbiology Ecology

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The sea anemone Entacmaea medusivora (Actiniaria, Anthozoa) commonly feeds on the golden jellyfish Mastigias papua (Rhizostomeae, Scyphozoa) which harbours an endosymbiotic dinoflagellate of the genus Cladocopium (Symbiodiniaceae). In this study, we monitored the photosynthetic activity of the endosymbiotic microalgae while their host jellyfish were ingested and digested by starved medusivorous anemones. By analyzing the photosynthetic yield of photosystem II, we observed that Cladocopium cells remain photosynthetically competent during the whole digestion process, thus confirming the exceptional resistance of Symbiodiniaceae to digestive enzymes. In the gastric cavity of E. medusivora, Cladocopium cells release oxygen, which could broadly stimulate the gastric microbiotic flora of the sea anemone. Ultimately, E. medusivora is not able to retain Cladocopium cells more than few days and physiologically-unaltered cells are therefore expelled in faecal pellets. The potential contribution of E. medusivora to maintain a reservoir of Cladocopium symbionts and its role in the life cycle of M. papua is discussed.

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“…Many interesting endosymbiotic events provide insight into horizontal gene transfer and coevolution. For example, two Hydra species ( H. viridissima and H. vulgaris ) can establish an endosymbiotic relationship with green algae [1, 2]. Gene expression analysis revealed that hosts’ genes associated with oxidative stress can benefit the survival and life cycles of Hydra .…”

Section: Introductionmentioning

confidence: 99%

Genetic basis for the establishment of endosymbiosis in Paramecium

Wang

Fan

et al. 2019

The ISME Journal

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The single-celled ciliate Paramecium bursaria is an indispensable model for investigating endosymbiosis between protists and green-algal symbionts. To elucidate the mechanism of this type of endosymbiosis, we combined PacBio and Illumina sequencing to assemble a high-quality and near-complete macronuclear genome of P. bursaria . The genomic characteristics and phylogenetic analyses indicate that P. bursaria is the basal clade of the Paramecium genus. Through comparative genomic analyses with its close relatives, we found that P. bursaria encodes more genes related to nitrogen metabolism and mineral absorption, but encodes fewer genes involved in oxygen binding and N-glycan biosynthesis. A comparison of the transcriptomic profiles between P. bursaria with and without endosymbiotic Chlorella showed differential expression of a wide range of metabolic genes. We selected 32 most differentially expressed genes to perform RNA interference experiment in P. bursaria , and found that P. bursaria can regulate the abundance of their symbionts through glutamine supply. This study provides novel insights into Paramecium evolution and will extend our knowledge of the molecular mechanism for the induction of endosymbiosis between P. bursaria and green algae.

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Two-step evolution of endosymbiosis between hydra and algae

Cited by 9 publications

References 31 publications

Immature symbiotic system between horizontally transmitted green algae and brown hydra

Immature symbiotic system between horizontally transmitted green algae and brown hydra

Photosynthetic capacity of the endosymbiotic dinoflagellate Cladocopium sp. is preserved during digestion of its jellyfish host Mastigias papua by the anemone Entacmaea medusivora

Genetic basis for the establishment of endosymbiosis in Paramecium

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