The roles of oxygen and ammonia in the symbiotic relationship between the spotted salamander Ambystoma maculatum and the green alga Oophila amblystomatis during embryonic development

Abstract

Some of the positive benefits of the symbiotic relationship between the yellow spotted salamander Ambystoma maculatum and the green alga Oophila amblystomatis on salamander embryonic development have been well documented. However, the fundamental basis of the relationship, in terms of the exchange of metabolic and photosynthetic products, is under debate, especially as it relates to newly discovered endosymbiotic aspects of the relationship. We developed a novel experimental approach in which we liberated egg capsules from egg masses and compared de-capsulated embryos to capsulated embryos. We were able to discern the contribution of salamander embryo respiration and ammonia excretion and algal photosynthesis to oxygen and ammonia dynamics within the egg capsules under light and dark conditions. Algal photosynthesis drove oxygen production under light conditions, while salamander respiration caused hypoxia during dark conditions. Ammonia was consumed to such an extent that it may be the limiting factor for algal growth. Algal cells actively penetrated the developing gut of embryos through the blastopore from an early developmental stage, and some algae came to reside in the vicinity of liver primordia towards later embryonic development, perhaps explaining the lack of detectable ammonia production by de-capsulated embryos. We suggest that oxygen and ammonia may influence A. maculatum growth and O. amblystomatis population dynamics. We have also demonstrated the extent to which algal cells penetrate internal spaces of embryos, which may be the precursor to endosymbiosis between these two species.

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Acknowledgments

Anthony Miller is thanked for the use of his O2 microelectrode and valuable review of the manuscript. Bill Marshall is thanked for use of his vibratome and Stephen Jewkes is thanked for permission to collect egg masses from the Upper Fairmont pond. A NSERC Discovery Grant and an infrastructure grant from the Canada Foundation for Innovation to CDB supported this research. RSB was partially supported by a Jack McLachlan fellowship for undergraduate student research. Two anonymous reviewers provided useful comment.

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Correspondence to Daniel P. Small.

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Small, D.P., Bennett, R.S. & Bishop, C.D. The roles of oxygen and ammonia in the symbiotic relationship between the spotted salamander Ambystoma maculatum and the green alga Oophila amblystomatis during embryonic development. Symbiosis 64, 1–10 (2014). https://doi.org/10.1007/s13199-014-0297-8

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Keywords

  • Ambystoma maculatum
  • Symbiosis
  • Embryonic development
  • Ammonia exchange
  • Oxygen exchange