Malpighian tubules are important determinants of Pseudomonas transstadial transmission and longtime persistence in Anopheles stephensi

Particle and Fibre Toxicology

Olle Terenius¹  Fahimeh Zarenejad⁴  Bagher Yakhchali⁴  Hasan Vatandoost²  Mohammad Ali Oshaghi³  Ali Reza Chavshin⁵ 

[1] Department of Ecology, Swedish University of Agricultural Sciences (SLU), Uppsala, Sweden;Institute for Environmental Research (IER), Tehran, Iran;Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences (TUMS), Tehran, Iran;Department of Environmental Biotechnology, National Institute of Genetic Engineering and Biotechnology (NIGEB), Tehran, Iran;Department of Medical Entomology and Vector Control, School of Public Health, Urmia University of Medical Sciences (UMSU), Urmia, Iran

关键词: Paratransgenesis;    Transstadial transmission;    GFP;    Pseudomonas;    Anopheles stephensi;    Malaria;   

Others  :  1147586
DOI  :  10.1186/s13071-015-0635-6

 received in 2014-09-22, accepted in 2015-01-02,  发布年份 2015

【 摘 要 】

Background

Pseudomonas is a genus of bacteria commonly found in investigations of gut microbes in malaria mosquitoes. Among those mosquitoes is the dominating malaria vector in Asia, Anopheles stephensi, where Pseudomonas is a prevailing bacterium and natural inhabitant of its breeding places. In order to explore the reason for finding Pseudomonas so frequently, an investigation of its localization and transstadial properties was undertaken.

Methods

A Pseudomonas isolate from An. stephensi was transformed successfully with an endogenous plasmid modified to express green fluorescent protein (GFP). Subsequently, the Pseudomonas-GFP was added to the laboratory larval breeding place of An. stephensi and taken up by the larvae. After 24 hours, the larvae were cleaned and moved to a bath with double-distilled water. Also, female adults were fed sugar solution containing Pseudomonas-GFP. The Pseudomonas-GFP was traced in the alimentary canal of larvae, pupae and adults.

Results

Fluorescent microscopy and PCR assays showed that the Pseudomonas bacteria underwent transstadial transmission from larvae to pupae and then to adults. In blood-fed female mosquitoes, the bacteria increased in numbers and remained in the mosquito body for at least three weeks after eclosion. In addition to the midgut, the Malpighian tubules of both larvae and adult mosquitoes were colonized by the bacteria. Also Pseudomonas-GFP that was distributed through sugar solution was able to colonize the Malpighian tubules of adult females.

Conclusions

Colonization of the Malpighian tubules by Pseudomonas bacteria seems to be important for the transstadial passage from larvae to adult and presumably for the longevity of the bacteria in the adult mosquito. The existence of an entry point in the larval stage, and the long duration in the female gut, opens up for a possible use of Pseudomonas in mosquito paratransgenesis.

【 授权许可】

   
2015 Chavsin et al.; licensee BioMed Central.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Abe T, Bignell D, Higashi M. Termites: Evolution, Sociality, Symbiosis, Ecology. Kluwer, Dordrecht; 2000.
• [2]Douglas AE. Nutritional interactions in insect-microbial symbioses: Aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol. 1998; 43:17-37.
• [3]Beard CB, Mason PW, Aksoy S, Tesh RB, Richards FF. Transformation of an insect symbiont and expression of a foreign gene in the Chagas’ disease vector Rhodnius prolixus. Am J Trop Med Hyg. 1992; 46(2):195-200.
• [4]Aksoy S. Wigglesworthia gen. nov. and Wigglesworthia glossinidia sp. nov., taxa consisting of the mycetocyte-associated, primary endosymbionts of tsetse flies. Int J Syst Bacteriol. 1995; 45(4):848-51.
• [5]Baldini F, Segata N, Pompon J, Marcenac P, Robert Shaw W, Dabire RK et al.. Evidence of natural Wolbachia infections in field populations of Anopheles gambiae. Nat Comm. 2014; 5:3985.
• [6]Favia G, Ricci I, Damiani C, Raddadi N, Crotti E, Marzorati M et al.. Bacteria of the genus Asaia stably associate with Anopheles stephensi, an Asian malarial mosquito vector. Proc Natl Acad Sci U S A. 2007; 104(21):9047-51.
• [7]Damiani C, Ricci I, Crotti E, Rossi P, Rizzi A, Scuppa P et al.. Paternal transmission of symbiotic bacteria in malaria vectors. Curr Biol. 2008; 18(23):R1087-8.
• [8]Coutinho-Abreu IV, Zhu KY, Ramalho-Ortigao M. Transgenesis and paratransgenesis to control insect-borne diseases: current status and future challenges. Parasitol Int. 2010; 59(1):1-8.
• [9]Aksoy S, Weiss B, Attardo G. Paratransgenesis applied for control of tsetse transmitted sleeping sickness. Adv Exp Med Biol. 2008; 627:35-48.
• [10]Chavshin AR, Oshaghi MA, Vatandoost H, Pourmand MR, Raeisi A, Terenius O. Isolation and identification of culturable bacteria from wild Anopheles culicifacies, a first step in a paratransgenesis approach. Parasit Vectors. 2014; 7:419. BioMed Central Full Text
• [11]Chavshin AR, Oshaghi MA, Vatandoost H, Pourmand MR, Raeisi A, Enayati AA et al.. Identification of bacterial microflora in the midgut of the larvae and adult of wild caught Anopheles stephensi: a step toward finding suitable paratransgenesis candidates. Acta Trop. 2012; 121(2):129-34.
• [12]Pumpuni CB, Demaio J, Kent M, Davis JR, Beier JC. Bacterial population dynamics in three anopheline species: the impact on Plasmodium sporogonic development. Am J Trop Med Hyg. 1996; 54(2):214-8.
• [13]Terenius O, de Oliveira CD, Pinheiro WD, Tadei WP, James AA, Marinotti O. 16S rRNA gene sequences from bacteria associated with adult Anopheles darlingi (Diptera: Culicidae) mosquitoes. J Med Entomol. 2008; 45(1):172-5.
• [14]Boissiere A, Tchioffo MT, Bachar D, Abate L, Marie A, Nsango SE et al.. Midgut microbiota of the malaria mosquito vector Anopheles gambiae and interactions with Plasmodium falciparum infection. PLoS pathogens. 2012; 8(5):e1002742.
• [15]Wang Y, Gilbreath TM, Kukutla P, Yan G, Xu J. Dynamic gut microbiome across life history of the malaria mosquito Anopheles gambiae in Kenya. PLoS ONE. 2011; 6(9):e24767.
• [16]Djadid ND, Jazayeri H, Raz A, Favia G, Ricci I, Zakeri S. Identification of the midgut microbiota of An. stephensi and An. maculipennis for their application as a paratransgenic tool against malaria. PLoS ONE. 2011;6(12):e28484.
• [17]Rani A, Sharma A, Rajagopal R, Adak T, Bhatnagar RK. Bacterial diversity analysis of larvae and adult midgut microflora using culture-dependent and culture-independent methods in lab-reared and field-collected Anopheles stephensi-an Asian malarial vector. BMC Microbiol. 2009; 9:96. BioMed Central Full Text
• [18]Sambrook J, Russell DW. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York; 2001.
• [19]Pidiyar VJ, Jangid K, Patole MS, Shouche YS. Studies on cultured and uncultured microbiota of wild Culex quinquefasciatus mosquito midgut based on 16 s ribosomal RNA gene analysis. Am J Trop Med Hyg. 2004; 70(6):597-603.
• [20]Li J, McLellan S, Ogawa S. Accumulation and fate of green fluorescent labeled Escherichia coli in laboratory-scale drinking water biofilters. Water Res. 2006; 40(16):3023-8.
• [21]Sarrazin S, Mossadegh-Keller N, Fukao T, Aziz A, Mourcin F, Vanhille L et al.. MafB Restricts M-CSF-Dependent Myeloid Commitment Divisions of Hematopoietic Stem Cells. Cell. 2009; 138(2):300-13.
• [22]Briones AM, Shililu J, Githure J, Novak R, Raskin L. Thorsellia anophelis is the dominant bacterium in a Kenyan population of adult Anopheles gambiae mosquitoes. ISME J. 2008; 2(1):74-82.
• [23]Jadin J, Vincke IH, Dunjic A, Delville JP, Wery M, Bafort J et al.. Role of Pseudomonas in the sporogenesis of the hematozoon of malaria in the mosquito. Bull Soc Pathol Exot Filiales. 1966; 59(4):514-25.
• [24]Coon KL, Vogel KJ, Brown MR, Strand MR. Mosquitoes rely on their gut microbiota for development. Mol Ecol. 2014; 23(11):2727-39.
• [25]Moll RM, Romoser WS, Modrzakowski MC, Moncayo AC, Lerdthusnee K. Meconial peritrophic membranes and the fate of midgut bacteria during mosquito (Diptera: Culicidae) metamorphosis. J Med Entomol. 2001; 38(1):29-32.
• [26]Lindh JM, Borg-Karlson AK, Faye I. Transstadial and horizontal transfer of bacteria within a colony of Anopheles gambiae (Diptera: Culicidae) and oviposition response to bacteria-containing water. Acta Trop. 2008; 107(3):242-50.
• [27]Chavshin AR, Oshaghi MA, Vatandoost H, Yakhchali B, Raeisi A, Zarenejad F. Escherichia coli expressing a green fluorescent protein (GFP) in Anopheles stephensi: a preliminary model for paratransgenesis. Symbiosis. 2013; 60:17-24.
• [28]Singh SR, Hou SX. Multipotent stem cells in the Malpighian tubules of adult Drosophila melanogaster. J Exp Biol. 2009; 212(Pt 3):413-23.
• [29]Gautam NK, Tapadia MG. Ecdysone signaling is required for proper organization and fluid secretion of stellate cells in the Malpighian tubules of Drosophila melanogaster. Int J Dev Biol. 2010; 54(4):635-42.
• [30]Riehle MA, Jacobs-Lorena M. Using bacteria to express and display anti-parasite molecules in mosquitoes: current and future strategies. Insect Biochem Mol Biol. 2005; 35(7):699-707.
• [31]Gaio Ade O, Gusmão DS, Santos AV, Berbert-Molina MA, Pimenta PF, Lemos FJ. Contribution of midgut bacteria to blood digestion and egg production in Aedes aegypti (Diptera: Culicidae) (L.). Parasit Vectors. 2011; 4:105. BioMed Central Full Text
• [32]Pumpuni CB, Beier MS, Nataro JP, Guers LD, Davis JR. Plasmodium falciparum: inhibition of sporogonic development in Anopheles stephensi by gram-negative bacteria. Exp Parasitol. 1993; 77(2):195-9.
• [33]Riehle MA, Moreira CK, Lampe D, Lauzon C, Jacobs-Lorena M. Using bacteria to express and display anti-Plasmodium molecules in the mosquito midgut. Int J Parasitol. 2007; 37(6):595-603.
• [34]Muro A, Genchi C, Cordero M, Simón F. Human Dirofilariasis in the European Union. Parasitology Today. 1999; 15(9):386-9.
• [35]Theis JH. Public health aspects of dirofilariasis in the United States. Vet Parasitol. 2005; 133:157-80.
• [36]Kan SP, Rajah KV, Dissanaike AS. Survey of dirofilariasis among dogs in seremban, Malaysia. Vet Parasitol. 1977; 3(2):177-81.
• [37]Azari-Hamidian S, Yaghoobi-Ershadi MR, Javadian E, Abai MR, Mobedi I, Linton YM et al.. Distribution and ecology of mosquitoes in a focus of dirofilariasis in northwestern Iran, with the first finding of filarial larvae in naturally infected local mosquitoes. Med Vet Entomol. 2009; 23(2):111-21.
• [38]Gellatly SL, Hancock REW. Pseudomonas aeruginosa: new insights into pathogenesis and host defenses. Pathog Dis. 2013; 67(3):159-73.