Malpighamoeba infection compromises fluid secretion and P-glycoprotein detoxification in Malpighian tubules.
ATP Binding Cassette Transporter, Subfamily B
/ metabolism
ATP Binding Cassette Transporter, Subfamily B, Member 1
/ metabolism
Amebiasis
/ parasitology
Amoebida
/ metabolism
Animals
Biological Transport
/ physiology
Bodily Secretions
/ metabolism
Epithelial Cells
/ metabolism
Grasshoppers
/ metabolism
Infections
/ metabolism
Malpighian Tubules
/ microbiology
Water-Electrolyte Balance
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
29 09 2020
29 09 2020
Historique:
received:
06
12
2019
accepted:
29
06
2020
entrez:
30
9
2020
pubmed:
1
10
2020
medline:
5
1
2021
Statut:
epublish
Résumé
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.
Identifiants
pubmed: 32994425
doi: 10.1038/s41598-020-72598-z
pii: 10.1038/s41598-020-72598-z
pmc: PMC7525526
doi:
Substances chimiques
ATP Binding Cassette Transporter, Subfamily B
0
ATP Binding Cassette Transporter, Subfamily B, Member 1
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
15953Subventions
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/L02389X/1
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/R005036/1
Pays : United Kingdom
Références
Maddrell, S. & Gardiner, B. Excretion of alkaloids by Malpighian tubules of insects. J. Exp. Biol. 64, 267–281 (1976).
pubmed: 932618
Després, L., David, J.-P. & Gallet, C. The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol. Evol. 22, 298–307 (2007).
pubmed: 17324485
doi: 10.1016/j.tree.2007.02.010
Goulson, D., Nicholls, E., Botías, C. & Rotheray, E. L. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347, 1255957 (2015).
pubmed: 25721506
doi: 10.1126/science.1255957
Richardson, L. L. et al. Secondary metabolites in floral nectar reduce parasite infections in bumblebees. Proc. R. Soc. B Biol. Sci. 282, 20142471 (2015).
doi: 10.1098/rspb.2014.2471
Manson, J. S., Otterstatter, M. C. & Thomson, J. D. Consumption of a nectar alkaloid reduces pathogen load in bumble bees. Oecologia 162, 81–89 (2010).
pubmed: 19711104
doi: 10.1007/s00442-009-1431-9
Alaux, C. et al. Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environ. Microbiol. 12, 774–782 (2010).
pubmed: 20050872
pmcid: 2847190
doi: 10.1111/j.1462-2920.2009.02123.x
Vidau, C. et al. Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by Nosema ceranae. PLoS ONE 6, e21550 (2011).
pubmed: 21738706
pmcid: 3125288
doi: 10.1371/journal.pone.0021550
McMillan, L. E., Miller, D. W. & Adamo, S. A. Eating when ill is risky: immune defense impairs food detoxification in the caterpillar Manduca sexta. J. Exp. Biol. 221, jeb173336 (2018).
pubmed: 29217626
doi: 10.1242/jeb.173336
King, R. L. & Taylor, A. B. Malpighamœba locustae, n. sp. (Amoebidae), a protozoan parasitic in the Malpighian tubes of grasshoppers. Trans. Am. Microsc. Soc. 55, 6–10 (1936).
doi: 10.2307/3223005
Taylor, A. B. & King, R. L. Further studies on the parasitic amebae found in grasshoppers. Trans. Am. Microsc. Soc. 56, 172–176 (1937).
doi: 10.2307/3222945
Bailey, L. Honey bee pathology. Annu. Rev. Entomol. 13, 191–212 (1968).
doi: 10.1146/annurev.en.13.010168.001203
Harry, O. G. & Finlayson, L. H. Histopathology of secondary infections of Malpighamoeba locustae (Protozoa, Amoebidae) in the desert locust, Schistocerca gregaria (Orthoptera, Acrididae). J. Invertebr. Pathol. 25, 25–33 (1975).
doi: 10.1016/0022-2011(75)90282-7
Harry, O. G. & Finlayson, L. H. The life-cycle, ultrastructure and mode of feeding of the locust amoeba Malpighamoeba locustae. Parasitology 72, 127 (1976).
doi: 10.1017/S0031182000048435
Liu, T. P. Scanning electron microscope observations on the pathological changes of Malpighian tubules in the worker honeybee, Apis mellifera, infected by Malpighamoeba mellificae. J. Invertebr. Pathol. 46, 125–132 (1985).
doi: 10.1016/0022-2011(85)90140-5
Wright, S. H. & Dantzler, W. H. Molecular and cellular physiology of renal organic cation and anion transport. Physiol. Rev. 84, 987–1049 (2004).
pubmed: 15269342
doi: 10.1152/physrev.00040.2003
Gaertner, L. S., Murray, C. L. & Morris, C. E. Transepithelial transport of nicotine and vinblastine in isolated Malpighian tubules of the tobacco hornworm (Manduca sexta) suggests a P-glycoprotein-like mechanism. J. Exp. Biol. 201, 2637–2645 (1998).
pubmed: 9716515
Rheault, M. R., Plaumann, J. S. & O’Donnell, M. J. Tetraethylammonium and nicotine transport by the Malpighian tubules of insects. J. Insect Physiol. 52, 487–498 (2006).
pubmed: 16527303
doi: 10.1016/j.jinsphys.2006.01.008
Leader, J. P. & O’Donnell, M. J. Transepithelial transport of fluorescent p-glycoprotein and MRP2 substrates by insect Malpighian tubules: confocal microscopic analysis of secreted fluid droplets. J. Exp. Biol. 208, 4363–4376 (2005).
pubmed: 16339857
doi: 10.1242/jeb.01911
Rossi, M., De Battisti, D. & Niven, J. E. Transepithelial transport of P-glycoprotein substrate by the Malpighian tubules of the desert locust. PLoS ONE 14, e0223569 (2019).
pubmed: 31593571
pmcid: 6782089
doi: 10.1371/journal.pone.0223569
Dermauw, W. & Van Leeuwen, T. The ABC gene family in arthropods: comparative genomics and role in insecticide transport and resistance. Insect Biochem. Mol. Biol. 45, 89–110 (2014).
pubmed: 24291285
doi: 10.1016/j.ibmb.2013.11.001
Eytan, G. D., Regev, R., Oren, G., Hurwitz, C. D. & Assaraf, Y. G. Efficiency of P-glycoprotein–mediated exclusion of rhodamine dyes from multidrug-resistant cells is determined by their passive transmembrane movement rate. Eur. J. Biochem. 248, 104–112 (1997).
pubmed: 9310367
doi: 10.1111/j.1432-1033.1997.00104.x
Murray, C. L. A P-glycoprotein-like mechanism in the nicotine-resistant insect, Manduca sexta (University of Ottawa, Ottawa, 1996).
O’Donnell, M. Insect excretory mechanisms. Adv. Insect Physiol. 35, 1–122 (2008).
doi: 10.1016/S0065-2806(08)00001-5
Berridge, M. J. The physiology of excretion in the cotton stainer, Dysdercus fasciatus, Signoret. IV. Hormonal control of excretion. J. Exp. Biol. 44, 553–566 (1966).
pubmed: 6006945
Ramsay, J. A. Active transport of water by the Malpighian tubules of the stick insect, Dixippus Morosus (Orthoptera, Phasmidae). J. Exp. Biol. 31, 104–113 (1954).
Maddrell, S. Active transport of water by insect Malpighian tubules. J. Exp. Biol. 207, 894–896 (2004).
pubmed: 14766947
doi: 10.1242/jeb.00846
Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671 (2012).
pubmed: 22930834
pmcid: 5554542
doi: 10.1038/nmeth.2089
R Core Team. R: a language and environment for statistical computing (R Foundation for Statistical Computing, Vienna, Austria, 2019). https://www.R-project.org/ .
Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
doi: 10.18637/jss.v067.i01
Burnham, K. P. & Anderson, D. R. A practical information-theoretic approach. in Model Selection Multimodel Inference 2nd edn (Springer, New York, 2002).
Maddrell, S. H. P. & O’Donnell, M. J. Insect Malpighian tubules: V-ATPase action in ion and fluid transport. J. Exp. Biol. 172, 417–429 (1992).
pubmed: 9874752
Wieczorek, H., Beyenbach, K. W., Huss, M. & Vitavska, O. Vacuolar-type proton pumps in insect epithelia. J. Exp. Biol. 212, 1611–1619 (2009).
pubmed: 19448071
pmcid: 2683008
doi: 10.1242/jeb.030007
Garrett, M. A., Bradley, T. J., Meredith, J. E. & Phillips, J. E. Ultrastructure of the Malpighian tubules of Schistocerca gregaria. J. Morphol. 195, 313–325 (1988).
pubmed: 29898572
doi: 10.1002/jmor.1051950306
Ugwu, M. C., Oli, A., Esimone, C. O. & Agu, R. U. Organic cation rhodamines for screening organic cation transporters in early stages of drug development. J. Pharmacol. Toxicol. Methods 82, 9–19 (2016).
pubmed: 27235784
doi: 10.1016/j.vascn.2016.05.014
Maddrell, S. H. P., Gardiner, B. O. C., Pilcher, D. E. M. & Reynolds, S. E. Active transport by insect Malpighian tubules of acidic dyes and of acylamides. J. Exp. Biol. 61, 357–377 (1974).
pubmed: 4443733
Hinks, C. F. & Ewen, A. B. Pathological effects of the parasite Malameba locustae in males of the migratory grasshopper Melanoplus sanguinipes and its interaction with the insecticide, cypermethrin. Entomol. Exp. Appl. 42, 39–44 (1986).
doi: 10.1111/j.1570-7458.1986.tb02185.x
Sreeramulu, K., Liu, R. & Sharom, F. J. Interaction of insecticides with mammalian P-glycoprotein and their effect on its transport function. Biochim. Biophys. Acta BBA Biomembr. 1768, 1750–1757 (2007).
doi: 10.1016/j.bbamem.2007.04.001
Bernays, E. A. & Chapman, R. F. Plant chemistry and acridoid feeding behaviour. Biochem. Asp. Plant Anim. Coevol. 99, 41 (1978).
Habig, W. H., Pabst, M. J. & Jakoby, W. B. Glutathione S-transferases the first enzymatic step in mercapturic acid formation. J. Biol. Chem. 249, 7130–7139 (1974).
pubmed: 4436300
pmcid: 4436300
Stahlschmidt, Z. R., Acker, M., Kovalko, I. & Adamo, S. A. The double-edged sword of immune defence and damage control: do food availability and immune challenge alter the balance?. Funct. Ecol. 29, 1445–1452 (2015).
doi: 10.1111/1365-2435.12454
Jeschke, V., Gershenzon, J. & Vassão, D. G. A mode of action of glucosinolate-derived isothiocyanates: detoxification depletes glutathione and cysteine levels with ramifications on protein metabolism in Spodoptera littoralis. Insect Biochem. Mol. Biol. 71, 37–48 (2016).
pubmed: 26855197
doi: 10.1016/j.ibmb.2016.02.002
Phillips, J. E. Rectal absorption in the desert locust, Schistocerca gregaria Forskal. I. Water. J. Exp. Biol. 41, 15–38 (1964).
pubmed: 14161606
Phillips, J. Comparative physiology of insect renal function. Am. J. Physiol. Regul. Integr. Comp. Physiol. 241, R241–R257 (1981).
doi: 10.1152/ajpregu.1981.241.5.R241
Proux, J. Lack of responsiveness of Malpighian tubules to the AVP-like insect diuretic hormone on migratory locusts infected with the protozoan Malameba locustae. J. Invertebr. Pathol. 58, 353–361 (1991).
doi: 10.1016/0022-2011(91)90180-X
Phillips, J. E. Rectal absorption in the desert locust, Schistocerca gregaria Forskal. II. Sodium, potassium and chloride. J. Exp. Biol. 41, 39–67 (1964).
pubmed: 14161612
Misof, B. et al. Phylogenomics resolves the timing and pattern of insect evolution. Science 346, 763–767 (2014).
pubmed: 25378627
doi: 10.1126/science.1257570
Venter, I. G. Egg development in the brown locust, Locustana pardalina (Walker), with special reference to the effect of infestation by Malameba locustae. South Afr. J. Agric. Sci. 9, 429–434 (1966).