Coprophagous features in carnivorous Nepenthes plants: a task for ureases

Abstract

Most terrestrial carnivorous plants are specialized on insect prey digestion to obtain additional nutrients. Few species of the genus Nepenthes developed mutualistic relationships with mammals for nitrogen supplementation. Whether dietary changes require certain enzymatic composition to utilize new sources of nutrients has rarely been tested. Here, we investigated the role of urease for Nepenthes hemsleyana that gains nitrogen from the bat Kerivoula hardwickii while it roosts inside the pitchers. We hypothesized that N. hemsleyana is able to use urea from the bats’ excrements. In fact, we demonstrate that 15N-enriched urea provided to Nepenthes pitchers is metabolized and its nitrogen is distributed within the plant. As ureases are necessary to degrade urea, these hydrolytic enzymes should be involved. We proved the presence and enzymatic activity of a urease for Nepenthes plant tissues. The corresponding urease cDNA from N. hemsleyana was isolated and functionally expressed. A comprehensive phylogenetic analysis for eukaryotic ureases, including Nepenthes and five other carnivorous plants’ taxa, identified them as canonical ureases and reflects the plant phylogeny. Hence, this study reveals ureases as an emblematic example for an efficient, low-cost but high adaptive plasticity in plants while developing a further specialized lifestyle from carnivory to coprophagy.

Metabolomics Analysis Reveals Tissue-Specific Metabolite Compositions in Leaf Blade and Traps of Carnivorous Nepenthes Plants

“…Interestingly, the final enzymatic step to release ammonia from ureides is catalyzed by a urease. Its presence and activity were recently demonstrated for Nepenthes and other carnivorous plants [41]. Whether or not this scenario mirrors the nitrogen translocation and distribution that occurs in Nepenthes remains to be elucidated.…”

“…Following this thread, it may also explain why no effect of feeding was found in the leaf blades. Experiments with N. hemsleyana , a coprophagous Nepenthes species that does not catch prey any more but feeds on bat feces [ 44 ], showed that upon 15 N-enriched urea application into pitchers, after only four days, 15 N was significantly detectable in protein fractions of leaf blades [ 41 ].…”

Discovery of digestive enzymes in carnivorous plants with focus on proteases

“…This suggests significant role of common hydrolytic enzymes, especially phosphatases, proteases, and chitinases, in prey digestion of various carnivorous plants regardless of different families or trapping mechanisms. Recently, Yilamujiang et al (2017) reported the presence of a novel digestive enzyme urease in N. hemsleyana which has developed a symbiosis relationship with bat.…”

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Discovery of digestive enzymes in carnivorous plants with focus on proteases

“…Recently, Yilamujiang et al, (2017) reported the presence of a novel digestive enzyme urease in N. hemsleyana which has developed a symbiosis relationship with bat.…”