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 seem to 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, we found that depleting the gut
microbiome of Pacific spiny dogfish (Squalus suckleyi) resulted in a
significant reduction in 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.

氮循环与氨基酸合成是肠道微生物组（gut microbiome）助力宿主代谢的两种重要途径，此类过程在氮限制型动物中尤为关键。海洋软骨鱼纲生物（marine elasmobranchs）属于氮限制型动物，因其需要大量氮元素以支撑基于尿素的渗透压调节（urea-based osmoregulation）。然而，经抗生素诱导耗竭肠道微生物组后，这类生物的循环尿素水平会显著下降，并会启动代偿性氮保留策略，例如减少尿素与氨的排泄。我们提出假说：海洋软骨鱼纲的肠道微生物组可将膳食与循环营养物质转化为氨基酸，从而辅助宿主维持碳氮平衡。本研究中，我们发现耗竭太平洋刺角鲨（Squalus suckleyi）的肠道微生物组后，膳食补充的¹⁵N同位素掺入血浆氨基酸的比例显著降低，其中与氮处理及能量代谢相关的氨基酸尤为明显，但该操作对肠道氨基酸转运并无影响。上述结果证实了肠道微生物组对宿主氨基酸池的重要性，以及海洋软骨鱼纲独特的氮处理策略。从更广泛的视角来看，本研究阐明了肠道微生物组如何助力机体稳态（organismal homeostasis），这一现象可能广泛存在于各类动物种群中。