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Comparative Study
. 2011;6(9):e25144.
doi: 10.1371/journal.pone.0025144. Epub 2011 Sep 16.

In situ enzyme activity in the dissolved and particulate fraction of the fluid from four pitcher plant species of the genus Nepenthes

Yayoi Takeuchi  1 , Michaela M Salcher, Masayuki Ushio, Rie Shimizu-Inatsugi, Masaki J Kobayashi, Bibian Diway, Christian von Mering, Jakob Pernthaler, Kentaro K Shimizu
Affiliations
Comparative Study

In situ enzyme activity in the dissolved and particulate fraction of the fluid from four pitcher plant species of the genus Nepenthes

Yayoi Takeuchi et al. PLoS One. 2011.

Abstract

The genus Nepenthes, a carnivorous plant, has a pitcher to trap insects and digest them in the contained fluid to gain nutrient. A distinctive character of the pitcher fluid is the digestive enzyme activity that may be derived from plants and dwelling microbes. However, little is known about in situ digestive enzymes in the fluid. Here we examined the pitcher fluid from four species of Nepenthes. High bacterial density was observed within the fluids, ranging from 7×10(6) to 2.2×10(8) cells ml(-1). We measured the activity of three common enzymes in the fluid: acid phosphatases, β-D-glucosidases, and β-D-glucosaminidases. All the tested enzymes detected in the liquid of all the pitcher species showed activity that considerably exceeded that observed in aquatic environments such as freshwater, seawater, and sediment. Our results indicate that high enzyme activity within a pitcher could assist in the rapid decomposition of prey to maximize efficient nutrient use. In addition, we filtered the fluid to distinguish between dissolved enzyme activity and particle-bound activity. As a result, filtration treatment significantly decreased the activity in all enzymes, while pH value and Nepenthes species did not affect the enzyme activity. It suggested that enzymes bound to bacteria and other organic particles also would significantly contribute to the total enzyme activity of the fluid. Since organic particles are themselves usually colonized by attached and highly active bacteria, it is possible that microbe-derived enzymes also play an important role in nutrient recycling within the fluid and affect the metabolism of the Nepenthes pitcher plant.

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Conflict of interest statement

Competing Interests: BD is an employee of Sarawak Forestry Corporation, which permitted and supported the authors' field research in Lambir Hills National Park in Sarawak, Malaysia. This does not alter the authors' adherence to all the PLoS ONE policies on sharing data and materials.

Figures

Figure 1
Figure 1. Total enzyme activity (before filtration) and dissolved enzyme activity (after filtration) in Borneo.
(a) Acid phosphatases (AP), (b) β-d-glucosidases (BG), and (c) β-d-glucosaminidases (NAG) in each species. A closed symbol represents that dissolved enzyme activity was not detectable and was treated as zero. The differences in mean values between untreated and filtered fluid were examined by Wilcoxon signed-rank test, and p-values were adjusted by the BH method for multiple comparison and were shown in the upper box for each species (unadjusted p-values are shown in brackets). ns: not significant.
Figure 2
Figure 2. Total enzyme activity (before filtration) and dissolved enzyme activity (after filtration) in Zurich.
(a) Acid phosphatases (AP), (b) β-d-glucosidases (BG), and (c) β-d-glucosaminidases (NAG) in each species. A closed symbol represents that dissolved enzyme activity was not detectable and was treated as zero. The differences in mean values between untreated and filtered fluid were examined by the Wilcoxon signed rank test, and p-values were adjusted by the BH method for multiple comparison and were shown in the upper box for each species (unadjusted p-values are shown in brackets). ns: not significant.
Figure 3
Figure 3. Average (SD) of pH values in each species per date/site.
The differences in mean value of the pH between the dates/sites within a species were examined by the Kruskal–Wallis test (p-values adjusted by the BH method, shown above each species). Differences of a species/site between dates were also examined by the Kruskal–Wallis test (X-axis legend; Feb. and Aug.; not significant, Jun. and Nov.; p = 0.005). Results that share the same letters are not significantly different (lower case for species examined at the same date, upper case for dates between species, Scheffé-type test, p<0.05).
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