Malpighamoeba infection compromises fluid secretion and P-glycoprotein detoxification in Malpighian tubules

Marta Rossi,Swidbert R Ott,Jeremy E Niven

doi:10.1038/s41598-020-72598-z

Marta Rossi, Swidbert R Ott + Show 1 more

Open Access

https://doi.org/10.1038/s41598-020-72598-z

Copy DOI

Journal: Scientific Reports	Publication Date: Sep 29, 2020
Citations: 4	License type: open-access

Affiliation: University of Sussex, University of Leicester

Abstract

Malpighian tubules, analogous to vertebrate nephrons, play a key role in insect osmoregulation and detoxification. Tubules can become infected with a protozoan, Malpighamoeba, which damages their epithelial cells, potentially compromising their function. Here we used a modified Ramsay assay to quantify the impact of Malpighamoeba infection on fluid secretion and P-glycoprotein-dependent detoxification by desert locust Malpighian tubules. Infected tubules have a greater surface area and a higher fluid secretion rate than uninfected tubules. Infection also impairs P-glycoprotein-dependent detoxification by reducing the net rhodamine extrusion per surface area. However, due to the increased surface area and fluid secretion rate, infected tubules have similar total net extrusion per tubule to uninfected tubules. Increased fluid secretion rate of infected tubules likely exposes locusts to greater water stress and increased energy costs. Coupled with reduced efficiency of P-glycoprotein detoxification per surface area, Malpighamoeba infection is likely to reduce insect survival in natural environments.

Highlights

Malpighian tubules, analogous to vertebrate nephrons, play a key role in insect osmoregulation and detoxification
Uninfected Malpighian tubules were transparent with a distinct lumen (Fig. 2A,B), whereas the lumina of infected tubules were filled with M. locustae cysts throughout their length and had a thinner and less clearly defined wall than those of uninfected tubules (Fig. 2C,D)
We found that surface area positively influences the fluid secretion rate independently of the health status of tubules (Table 2B, Fig. 4)

Summary

Introduction

Malpighian tubules, analogous to vertebrate nephrons, play a key role in insect osmoregulation and detoxification. We used a modified Ramsay assay to quantify the impact of Malpighamoeba infection on fluid secretion and P-glycoprotein-dependent detoxification by desert locust Malpighian tubules. Compromised tubule function may disrupt osmoregulation and impair detoxification, preventing insects from maintaining their internal osmotic environment, and exposing their cells to the waste products of metabolism and to environmental toxins. The impact of such impairment may be severe in those insects that are exposed to environmental toxins as a consequence of feeding directly on plant tissues or their products (such as nectar or pollen) because of the presence of secondary m etabolites[2]. In the case of Malpighian tubules, P-glycoproteins contribute to the excretion of ingested toxic substances[16]

Methods

Results

Conclusion