Absence of a functional gut microbiome impairs host amino acid metabolism in the Pacific spiny dogfish (Squalus suckleyi).

Nitrogen recycling and amino acid synthesis are two notable ways in which the gut microbiome can contribute to host metabolism, and these processes are especially important in nitrogen-limited animals. Marine elasmobranchs are nitrogen limited as they require substantial amounts of this element to support urea-based osmoregulation. However, following antibiotic-induced depletion of the gut microbiome, elasmobranchs are known to experience a significant decline in circulating urea and employ compensatory nitrogen conservation strategies such as reduced urea and ammonia excretion. We hypothesized that the elasmobranch gut microbiome transforms dietary and recycled nutrients into amino acids, supporting host carbon and nitrogen balance. Here, using stable isotope analyses, we found that depleting the gut microbiome of Pacific spiny dogfish (Squalus suckleyi) resulted in a significant reduction to the incorporation of supplemented dietary 15N into plasma amino acids, notably those linked to nitrogen handling and energy metabolism, but had no effect on gut amino acid transport. These results demonstrate the importance of gut microbes to host amino acid pools and the unique nitrogen handling strategy of marine elasmobranchs. More broadly, these results elucidate how the gut microbiome contributes to organismal homeostasis, which is likely a ubiquitous phenomenon across animal populations.

The gut microbiome may influence post-prandial nitrogen handling in an elasmobranch, the Pacific spiny dogfish (Squalus suckleyi).

Nitrogen recycling through the gut microbiome is an important mechanism used throughout vertebrates to reclaim valuable nitrogen trapped in urea. Evidence suggests it may be especially important in nitrogen limited animals, yet little is known about its role in marine elasmobranchs, which are said to be severely nitrogen limited. In the present study we used antibiotics to deplete the gut microbiome of Pacific spiny dogfish and assessed the role of the microbiome in nitrogen handling in both fed and fasted states. In fed animals, antibiotic treatment eliminated the activity of the microbial enzyme urease and reduced cellulase activity by 78%. This reduction in microbial enzyme activity resulted in significantly lower plasma urea levels which then trended upward as urea excretion rates decreased. Ammonia excretion rates were also significantly lower in antibiotic treated fish compared to the control fed. Finally, antibiotic treated fed individuals lost an average of 7.4% of their body mass while the fed controls lost only 1.8% of their body mass. Nitrogen handling in fasted animals was not significantly impacted by a reduction in microbial activity. These results suggest that compromising the gut microbiome significantly influences post-prandial nitrogen handling in spiny dogfish, and that the recycling of urea­nitrogen may be vital to maintaining nitrogen balance in these fish.