Abstract
During embryonic development, cells of the green alga Oophila amblystomatis enter cells of the salamander Ambystoma maculatum forming an endosymbiosis. Here, using de novo dual-RNA seq, we compared the host salamander cells that harbored intracellular algae to those without algae and the algae inside the animal cells to those in the egg capsule. This two-by-two-way analysis revealed that intracellular algae exhibit hallmarks of cellular stress and undergo a striking metabolic shift from oxidative metabolism to fermentation. Culturing experiments with the alga showed that host glutamine may be utilized by the algal endosymbiont as a primary nitrogen source. Transcriptional changes in salamander cells suggest an innate immune response to the alga, with potential attenuation of NF-κB, and metabolic alterations indicative of modulation of insulin sensitivity. In stark contrast to its algal endosymbiont, the salamander cells did not exhibit major stress responses, suggesting that the host cell experience is neutral or beneficial.
Highlights
All vertebrates have a ‘microbiome’ that includes mutualist ecto-symbionts living in close association with, but not within, their cells (Douglas, 2010)
A test for contaminating mRNA from A. maculatum lysed during dissociation was shown to be negative (Figure 1—figure supplement 1) A total evidence assembly contained all reads from all samples (n = 3 intra-capsular algal samples from three different eggs; salamander cells with and without algae from n = 4 individual salamander embryos)
This was followed by homology and abundance filtering (Figure 1—figure supplements 2, 3 and 4), producing 46,549 A. maculatum and 6,726 O. amblystomatis genes that were used in differential expression analysis
Summary
All vertebrates have a ‘microbiome’ that includes mutualist ecto-symbionts living in close association with, but not within, their cells (Douglas, 2010). The green alga Oophila amblystomatis enters the cells of the salamander Ambystoma maculatum during early development (Kerney et al, 2011), and co-culture experiments show that the algae consistently benefit the salamander embryo hosts (Small et al, 2014; Graham et al, 2013; Pinder and Friet, 1994). There is a long history of experimentation on the ectosymbiotic association between O. amblystomatis and A. maculatum: where the alga populates salamander egg capsules that contain developing embryos (Small et al, 2014; Gilbert, 1944). The intracellular association between these two organisms was only recently recognized (Kerney et al, 2011), 122 years after the first published description of green salamander egg masses (Orr, 1888)
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