The Alga‐Egg Relationship in Ambystoma Maculatum, A Case of Symbiosis

Gilbert, Perry W.

doi:10.2307/1931284

Cited by 49 publications

(60 citation statements)

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“…The mutual benefit of this facultative association has been clearly established through exclusion experiments. Clutches raised in the dark do not accrue detectable algae (6)(7)(8)(9). The presence of algae in these experiments correlates with earlier hatching (6, 9), decreased embryonic mortality (7,8), more synchronous hatching (8,9), and reaching a larger size (8) and later developmental stage (9) at hatching.…”

mentioning

confidence: 54%

“…The presence of algae in these experiments correlates with earlier hatching (6, 9), decreased embryonic mortality (7,8), more synchronous hatching (8,9), and reaching a larger size (8) and later developmental stage (9) at hatching. Additionally, algal growth is minimal in egg capsules after embryos are removed (8), indicating that the embryos, and not the egg capsules, aid algal growth. Algae are thought to benefit from nitrogenous wastes released by the embryos [ref.…”

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confidence: 55%

“…These observations suggest that intracapsular algal cells in our samples comprise a single species. The published literature on this association (6,8,9) refers to the algae as "Oophila amblystomatis" (Lambert ex Printz) (19) on the basis of an informal species designation by Lambert (6), although-to date-no formal taxonomic description exists. Previous studies reported additional bacteria and protists within the egg capsules (6,14).…”

Section: Resultsmentioning

confidence: 99%

“…In the wild, nearly all intratissue algal-animal symbioses are obligatory and consist of photosynthate transfer from symbiont to host (17,27). However, previous research has shown that the Ambystoma-alga association is facultative (6,8,15) and may not result in photosynthate transfer (28). Algalanimal associations are typically limited by the availability of carbon dioxide and photons.…”

Section: Discussionmentioning

confidence: 99%

“…Early attempts to identify or culture the algae from oviducts of gravid female salamanders failed, discouraging further investigations into the anatomical associations between host and symbiont (8,15). All previous research describes the relationship between the algae and embryo as an ectosymbiotic mutualism, with no intratissue or intracellular stages.…”

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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.

110

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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mentioning

confidence: 54%

mentioning

confidence: 55%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

See 3 more Smart Citations

Intracellular invasion of green algae in a salamander host

Kerney

Kim

Hangarter

et al. 2011

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

110

122

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Response of the green alga Oophila sp., a salamander endosymbiont, to a PSII‐inhibitor under laboratory conditions

Baxter

Brain

Rodríguez‐Gil

et al. 2014

Enviro Toxic and Chemistry

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In a rare example of autotroph-vertebrate endosymbiosis, eggs of the yellow-spotted salamander (Ambystoma maculatum) are colonized by a green alga (Oophila sp.) that significantly enhances salamander development. Previous studies have demonstrated the potential for impacts to the salamander embryo when growth of the algae is impaired by exposure to herbicides. To further investigate this relationship, the authors characterized the response of the symbiotic algae (Oophila sp.) alone to the photosystem II (PSII) inhibitor atrazine under controlled laboratory conditions. After extraction of the alga from A. maculatum eggs and optimization of culturing conditions, 4 toxicity assays (96 h each) were conducted. Recovery of the algal population was also assessed after a further 96 h in untreated media. Average median effective concentration (EC50) values of 123 µg L(-1) (PSII yield), 169 µg L(-1) (optical density), and 299 µg L(-1) (growth rate) were obtained after the 96-h exposure. Full recovery of exposed algal populations after 96 h in untreated media was observed for all endpoints, except for optical density at the greatest concentration tested (300 µg L(-1) ). Our results show that, under laboratory conditions, Oophila sp. is generally less sensitive to atrazine than standard test species. Although conditions of growth in standard toxicity tests are not identical to those in the natural environment, these results provide an understanding of the tolerance of this alga to PSII inhibitors as compared with other species.

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Optimization of culturing conditions for toxicity testing with the algaOophilasp. (Chlorophyceae), an amphibian endosymbiont

Rodríguez‐Gil

Brain

Baxter

et al. 2014

Enviro Toxic and Chemistry

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Eggs of the yellow-spotted salamander (Ambystoma maculatum) have a symbiotic relationship with green algae. It has been suggested that contaminants that are preferentially toxic to algae, such as herbicides, may impair the symbiont and, hence, indirectly affect the development of the salamander embryo. To enable testing under near-standard conditions for first-tier toxicity screening, the authors isolated the alga from field-collected eggs and identified conditions providing exponential growth rates in the apparent asexual phase of the alga. This approach provided a uniform, single-species culture, facilitating assessment of common toxicity end points and comparison of sensitivity relative to other species. Sequencing of the 18s ribosomal DNA indicated that the isolated alga is closely related to the recently described Oophila amblystomatis but is more similar to other known Chlamydomonas species, suggesting possible biogeographical variability in the genetic identity of the algal symbiont. After a tiered approach to culturing method refinement, a modified Bristol's media with 1 mM NH4 (+) as nitrogen source was found to provide suitable conditions for toxicity testing at 18 °C and 200 µmol m(-2) s(-1) photosynthetically active radiation (PAR) on a 24-h light cycle. The validity of the approach was demonstrated with Zn(2+) as a reference toxicant. Overall, the present study shows that screening for direct effects of contaminants on the algal symbiont without the presence of the host salamander is possible under certain laboratory conditions.

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The Alga‐Egg Relationship in Ambystoma Maculatum, A Case of Symbiosis

Cited by 49 publications

References 2 publications

Intracellular invasion of green algae in a salamander host

Intracellular invasion of green algae in a salamander host

Response of the green alga Oophila sp., a salamander endosymbiont, to a PSII‐inhibitor under laboratory conditions

Optimization of culturing conditions for toxicity testing with the algaOophilasp. (Chlorophyceae), an amphibian endosymbiont

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