Most relationships between animals and microbes interface in one of two locations: on the outside of animal cells (mostly to the benefit of both parties, think gut microbiota) or on the inside of animal cells (mostly to the benefit of the microbe, think malaria). Currently, the only exception to the latter among vertebrates is the unique relationship between spotted salamanders (Ambystoma maculatum) and the green algae that can be found in the tissues of developing salamander embryos, Oophila amblystomatis.
I’ve written previously on how easy it may be to make tidy conclusions about this vertebrate-algae relationship, and how new work was beginning to build a more detailed case for symbiotic co-evolution between these taxa. I missed an important update in this line of research this May that shows this putative mutualism is not so, uhh, mutual.
John Burns and colleagues built on the discovery of O. amblystomatis entering and persisting in salamander cells by investigating the potential for gene expression changes that may happen during this invasion. Previous work established that when O. amblystomatis grows outside of salamander cells, but within membranes that protect the developing salamanders, the algae appear to benefit from the availability of embryo-generated waste while, in turn, the embryo absorbs the extra oxygen produced by the algae. How similar were circumstances inside the invaded salamander cells for both parties? To get at this question, the authors collected RNAseq data to compare gene expression between 1) algae that was inside or outside of salamander cells and 2) salamander cells that were with or without algae.
Modified final panels from Figure 1 (Burns et al. 2017). Deferentially expressed algal transcripts on left and differentially expressed salamander transcripts on right. “Intracapsular” in this case refers to outside of salamander cell, but still within the developing egg mass.
When it comes to changes in gene expression, the story of salamander-algae mutualism seems awfully one-sided. Less that 1% of salamander genes displayed any differential expression when their cells were with or without algae. In contrast, the algae showed six times the number of changes in expression when they were found inside salamander cells, and these changes don’t sound like “kumbaya” to me. Many of these changes were typically stress-associated, including the over-expression of heat shock proteins, shifts from oxidative to fermentative metabolism, and increases in autophagy proteins. The stress response shown by O. amblystomatis is hypothesized to be a general symptom from reduced efficiency of photosynthesis. Salamander cells, in contrast, take a much more relaxed stance on algal intrusion, showing a lukewarm immune responses and even suggestions of metabolic changes that could indicate the use of energy created by the captured algae.
In the conclusions, the authors put this new discovery into the context of other microbe-host interactions that have been canonized only to get upended by new data. Just because the story makes sense doesn’t mean that it isn’t worth going a level deeper – good advice for all of us.
Burns, J. A., Zhang, H., Hill, E., Kim, E., & Kerney, R. (2017). Transcriptome analysis illuminates the nature of the intracellular interaction in a vertebrate-algal symbiosis. eLife, 6.