Algas que vivem dentro de células de salamandras: primeiro caso conhecido de endosimbiontes vertebrados

Algae That Live Inside the Cells of Salamanders Are the First Known Vertebrate Endosymbionts

ScienceDaily (Apr. 4, 2011) — A species of algae long known to associate with spotted salamanders has been discovered to live inside the cells of developing embryos, say scientists from the U.S. and Canada, who report their findings in this week'sProceedings of the National Academy of Sciences.

Salamander embryos grow inside egg capsules that are covered with and usually infiltrated by a type of green algae. (Credit: Courtesy of Roger Hangarter)

This is the first known example of a eukaryotic algae living stably inside the cells of any vertebrate.

"It raises the possibility that more animal/algae symbioses exist that we are not aware of," said Indiana University Bloomington biologist Roger Hangarter, the PNAS report's sole American coauthor. "Since other salamanders and some frog species have similar algae/egg symbioses, it is possible that some of those will also have the type of endosymbioses we have seen in the spotted salamander."

Biologists Ryan Kerney, Eunsoo Kim, Aaron Heiss, and Brian Hall of Dalhousie University in Halifax, Nova Scotia, and Cory Bishop of St. Frances Xavier University in Antigonish, Nova Scotia, are the other members of the research team. Kerney was the report's lead author.

"We were particularly excited to discover this association in spotted salamander embryos, because this species was a model organism for early experimental embryology research and is a locally common salamander in eastern North America," Kerney said. "We hope that this study will highlight biodiversity research on common North American species, which can easily be overlooked or even considered over-studied."

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Intracellular invasion of green algae in a salamander host

1. Ryan Kerney^a,¹, 
2. Eunsoo Kim^b, 
3. Roger P. Hangarter^c, 
4. Aaron A. Heiss^a,
5. Cory D. Bishop^d, and 
6. Brian K. Hall^a

+Author Affiliations

1. ^aDepartment of Biology, Dalhousie University, Halifax, NS, Canada B3H 4J1;
2. ^bDepartment of Biochemistry and Molecular Biology, Dalhousie University, Halifax, NS, Canada B3H 1X5;
3. ^cDepartment of Biology, Indiana University, Bloomington, IN 47405; and
4. ^dDepartment of Biology, St. Francis Xavier University, Antigonish, NS, Canada B2G 2W5

1. Edited by David B. Wake, University of California, Berkeley, CA, and approved February 18, 2011 (received for review December 6, 2010)

Abstract

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

Footnotes

• ↵¹To whom correspondence should be addressed. E-mail:ryankerney@gmail.com.

• Author contributions: R.K. designed research; R.K., E.K., R.P.H., A.A.H., and C.D.B. performed research; E.K., R.P.H., A.A.H., and C.D.B. contributed new reagents/analytic tools; R.K. and B.K.H. analyzed data; and R.K., E.K., R.P.H., A.A.H., C.D.B., and B.K.H. wrote the paper.
• The authors declare no conflict of interest.
• This article is a PNAS Direct Submission.
• Data deposition: The sequences reported in this paper have been deposited in the GenBank database [accession nos. HM590633 (Oophila sp. 16S) andHM590634 (Oophila sp. 18S)].
• This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1018259108/-/DCSupplemental.

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