Progress of researches on interactions between sandfly gut microecology and Leishmania infection

doi:10.12140/j.issn.1000-7423.2025.05.017

Abstract

Abstract:

Sandflies, as vectors of multiples pathogens, are of significant epidemiological importance, and has been given attention due to their role in transmitting Leishmania. The growth and development of Leishmania is affected by the diverse microbial communities present in the sandfly gut, which also induces differential gene expression in the sandfly gut. This article summarizes the composition of the sandfly gut microbiota and their interactions with Leishmania, and alterations of functional characteristics in the sandfly gut caused by the parasite. Sandflies, Leishmania, gut microbiota, and gene expression form a complex network, and deciphering their interactions may provide more strategies for leishmaniasis management and sandfly vector control.

Key words: Sandfly, Leishmania, Gut microbiota, Gut function

CLC Number:

R531.6

HE Yaqi, CUI Lei, FANG Yuan, ZHOU Zhengbin, ZHANG Yi. Progress of researches on interactions between sandfly gut microecology and Leishmania infection[J]. CHINESE JOURNAL OF PARASITOLOGY AND PARASITIC DISEASES, 2025, 43(5): 711-717.

Figures/Tables 2

References 61

[1]	李雨晗, 张櫶文, 程功. 虫媒病毒与生物安全[J]. 生物学杂志, 2023, 40(6): 1-6.
	Li YH, Zhang XW, Cheng G. Arboviruses and biosafety[J]. J Biol, 2023, 40(6): 1-6. (in Chinese)
[2]	熊光华. 中国白蛉科白蛉种类[J]. 国际医学寄生虫病杂志, 2008, 35(6): 283-286.
	Xiong GH. Sandfly species of Phlebotomidiae in China[J]. Int J Med Parasit Dis, 2008, 35(6): 283-286. (in Chinese)
[3]	Zhang LM, Leng YJ. Eighty-year research of phlebotomine sandflies (Diptera:Psychodidae) in China (1915-1995). Ⅱ. Phlebotomine vectors of leishmaniasis in China[J]. Parasite, 1997, 4(4): 299-306.
[4]	Telleria EL, Martins-da-Silva A, Tempone AJ, et al. Leishmania, microbiota and sandfly immunity[J]. Parasitology, 2018, 145(10): 1336-1353.
[5]	Tabbabi A, Mizushima D, Yamamoto DS, et al. Sandflies and their microbiota[J]. Parasitologia, 2022, 2(2): 71-87.
[6]	熊光华, 金长发, 管立人. 中国的白蛉[M]. 北京: 科学出版社, 2016: 8-23.
	Xiong GH, Jin CF, Guan LR. Chinese sandflies[M]. Beijing: Science Press, 2016: 8-23. (in Chinese)
[7]	熊光华, 朱显因, 赵佳. 我国首次发现自体生殖中华白蛉[J]. 动物学研究, 1981, (3): 291-293.
	Xiong GH, Zhu XY, Zhao J. Discovery of autogeny in Phlebotomus chinensis (Newstead) in China[J]. Zool Res, 1981(3): 291-293. (in Chinese)
[8]	管立人. 中国白蛉(双翅目:毛蛉科)调查研究工作的展望[J]. 中国寄生虫学与寄生虫病杂志, 2013, 31(4): 310-314.
	Guan LR. Prospect on the investigation of sandflies (Diptera: Psychodidae) in China[J]. Chin J Parasitol Parasit Dis, 2013, 31(4): 310-314. (in Chinese)
[9]	Wilder-Smith A, Gubler DJ, Weaver SC, et al. Epidemic arboviral diseases: Priorities for research and public health[J]. Lancet Infect Dis, 2017, 17(3): e101-e106.
[10]	Maroli M, Feliciangeli MD, Bichaud L, et al. Phlebotomine sandflies and the spreading of leishmaniases and other diseases of public health concern[J]. Med Vet Entomol, 2013, 27(2): 123-147.
[11]	World Health Organization. Leishmaniasis[EB/OL]. (2023-01-12)[2025-03-04]. https://www.who.int/news-room/fact-sheets/detail/leishmaniasis.
[12]	Pavli A, Maltezou HC. Leishmaniasis, an emerging infection in travelers[J]. Int J Infect Dis, 2010, 14(12): e1032-e1039.
[13]	de Vries HJC, Reedijk SH, Schallig HDFH. Cutaneous leishmaniasis: Recent developments in diagnosis and management[J]. Am J Clin Dermatol, 2015, 16(2): 99-109.
[14]	World Health Organization. Control of the leishmaniases[R]. Geneva: World Health Organization, 2010: 5-14.
[15]	Casulli A. New global targets for NTDs in the WHO roadmap 2021-2030[J]. PLoS Negl Trop Dis, 2021, 15(5): e0009373.
[16]	刘国栋. 犬内脏利什曼病时空分布、风险因素及其媒介适生性分析[D]. 哈尔滨: 东北农业大学, 2022: 2-3.
	Liu GD. Analysis of spatial and temporal distribution, risk factors and vector fitness of canine visceral leishmaniasis[D]. Harbin: Northeast Agricultural University, 2022: 2-3. (in Chinese)
[17]	王兆俊, 熊光华, 管立人. 新中国黑热病流行病学与防治成就[J]. 中华流行病学杂志, 2000(1): 51-54.
	Wang ZJ, Xiong GH, Guan LR. Epidemiology and control achievements of kala-azar in new China[J]. Chin J Epidemiol, 2000(1): 51-54. (in Chinese)
[18]	周正斌, 李元元, 李中秋, 等. 2023年我国内脏利什曼病疫情分析[J]. 中国寄生虫学与寄生虫病杂志, 2024, 42(5): 559-565.
	Zhou ZB, Li YY, Li ZQ, et al. Prevalence of visceral leishmaniasis in China in 2023[J]. Chin J Parasitol Parasit Dis, 2024, 42(5): 559-565. (in Chinese)
[19]	陈曦, 师悦, 周升, 等. 全球内脏利什曼病流行风险因素研究进展[J]. 中国血吸虫病防治杂志, 2024, 36(4): 412-421, 427.
	Chen X, Shi Y, Zhou S, et al. Risk factors of visceral leishmaniasis in the world: A review[J]. Chin J Schisto Control, 2024, 36(4): 412-421, 427. (in Chinese)
[20]	王奇, 师悦, 秦瑶, 等. 2017—2022年中国内脏利什曼病流行特征及时空聚集性分析[J]. 热带病与寄生虫学, 2024, 22(2): 68-75.
	Wang Q, Shi Y, Qin Y, et al. Epidemiological characteristics and spatial-temporal cluster of visceral leishmaniosis in China, 2017-2022[J]. J Trop Dis Parasitol, 2024, 22(2): 68-75. (in Chinese)
[21]	Sacks DL. Leishmania-sandfly interactions controlling species-specific vector competence[J]. Cell Microbiol, 2001, 3(4): 189-196.
[22]	Dillon RJ, Lane RP. Influence of Leishmania infection on blood-meal digestion in the sandflies Phlebotomus papatasi and P. langeroni[J]. Parasitol Res, 1993, 79(6): 492-496.
[23]	Sant’anna MR, Diaz-Albiter H, Mubaraki M, et al. Inhibition of trypsin expression in Lutzomyia longipalpis using RNAi enhances the survival of Leishmania[J]. Parasit Vectors, 2009, 2(1): 62.
[24]	Ramalho-Ortigão M, Jochim RC, Anderson JM, et al. Exploring the midgut transcriptome of Phlebotomus papatasi: Comparative analysis of expression profiles of sugar-fed, blood-fed and Leishmania-major-infected sandflies[J]. BMC Genomics, 2007, 8: 300.
[25]	Dostálová A, Votypka J, Favreau AJ, et al. The midgut transcriptome of Phlebotomus (Larroussius) perniciosus, a vector of Leishmania infantum: Comparison of sugar fed and blood fed sandflies[J]. BMC Genomics, 2011, 12: 223.
[26]	Volf P, Hajmova M, Sadlova J, et al. Blocked stomodeal valve of the insect vector: Similar mechanism of transmission in two trypanosomatid models[J]. Int J Parasitol, 2004, 34(11): 1221-1227.
[27]	Dostálová A, Volf P. Leishmania development in sandflies: Parasite-vector interactions overview[J]. Parasit Vectors, 2012, 5: 276.
[28]	Peters W, Killick-Kendrick R. The Leishmaniases in biology and medicine. Vol. 1: Biology and epidemiology[M]. London: Academic Press, 1987: 121-176.
[29]	Ticha L, Kykalova B, Sadlova J, et al. Development of various Leishmania (Sauro leishmania) tarentolae strains in three Phlebotomus species[J]. Microorganisms, 2021, 9(11): 2256.
[30]	Peterkova-Koci K, Robles-Murguia M, Ramalho-Ortigao M, et al. Significance of bacteria in oviposition and larval development of the sandfly Lutzomyia longipalpis[J]. Parasit Vectors, 2012, 5: 145.
[31]	Walters AW, Hughes RC, Call TB, et al. The microbiota influences the Drosophila melanogaster life history strategy[J]. Mol Ecol, 2020, 29(3): 639-653.
[32]	Alencar RB, de Queiroz RG, Barrett TV. Breeding sites of phlebotomine sandflies (Diptera:Psychodidae) and efficiency of extraction techniques for immature stages in Terra-firme forest in Amazonas State, Brazil[J]. Acta Trop, 2011, 118(3): 204-208.
[33]	Gouveia C, Asensi MD, Zahner V, et al. Study on the bacterial midgut microbiota associated to different Brazilian populations of Lutzomyia longipalpis (Lutz & Neiva) (Diptera:Psychodidae)[J]. Neotrop Entomol, 2008, 37(5): 597-601.
[34]	Oliveira SM, Moraes BA, Gonçalves CA, et al. Prevalence of microbiota in the digestive tract of wild females of Lutzomyia longipalpis Lutz & Neiva, 1912) (Diptera:Psychodidae)[J]. Rev Soc Bras Med Trop, 2000, 33(3): 319-322.
[35]	Perira de Oliveira SM, de Morais BA, Gonçalves CA, et al. Digestive tract microbiota in female Lutzomyia longipalpis (Lutz & Neiva, 1912) (Diptera :Psychodidae) from colonies feeding on blood meal and sucrose plus blood meal[J]. Cad Saude Publica, 2001, 17(1): 229-232.
[36]	Li KL, Chen HY, Jiang JJ, et al. Diversity of bacteriome associated with Phlebotomus chinensis (Diptera :Psychodidae) sandflies in two wild populations from China[J]. Sci Rep, 2016, 6: 36406.
[37]	Wang J, Gou QY, Luo GY, et al. Total RNA sequencing of Phlebotomus chinensis sandflies in China revealed viral, bacterial, and eukaryotic microbes potentially pathogenic to humans[J]. Emerg Microbes Infect, 2022, 11(1): 2080-2092.
[38]	Sant’Anna MRV, Diaz-Albiter H, Aguiar-Martins K, et al. Colonisation resistance in the sandfly gut: Leishmania protects Lutzomyia longipalpis from bacterial infection[J]. Parasit Vectors, 2014, 7: 329.
[39]	Hoffmann A. Wolbachia[J]. Curr Biol, 2020, 30(19): R1113-R1114.
[40]	Serbus LR, Casper-Lindley C, Landmann F, et al. The genetics and cell biology of Wolbachia-host interactions[J]. Annu Rev Genet, 2008, 42: 683-707.
[41]	Werren JH, Baldo L, Clark ME. Wolbachia: Master manipulators of invertebrate biology[J]. Nat Rev Microbiol, 2008, 6(10): 741-751.
[42]	Xi ZY, Khoo CCH, Dobson SL. Wolbachia establishment and invasion in an Aedes aegypti laboratory population[J]. Science, 2005, 310(5746): 326-328.
[43]	Latrofa MS, Varotto-Boccazzi I, Louzada-Flores VN, et al. Interaction between Wolbachia pipientis and Leishmania infantum in heart worm infected dogs[J]. Parasit Vectors, 2023, 16: 77.
[44]	McCarthy CB, Diambra LA, Rivera Pomar RV. Metagenomic analysis of taxa associated with Lutzomyia longipalpis, vector of visceral leishmaniasis, using an unbiased high-throughput approach[J]. PLoS Negl Trop Dis, 2011, 5(9): e1304.
[45]	Vivero RJ, Castañeda-Monsalve VA, Romero LR, et al. Gut microbiota dynamics in natural populations of Pintomyia evansi under experimental infection with Leishmania infantum[J]. Microorganisms, 2021, 9(6): 1214.
[46]	Kelly PH, Bahr SM, Serafim TD, et al. The gut microbiome of the vector Lutzomyia longipalpis is essential for survival of Leishmania infantum[J]. mBio, 2017, 8(1): e01121-16.
[47]	Campolina TB, Villegas LEM, Monteiro CC, et al. Tripartite interactions: Leishmania, microbiota and Lutzomyia longipalpis[J]. PLoS Negl Trop Dis, 2020, 14(10): e0008666.
[48]	Karimian F, Koosha M, Choubdar N, et al. Comparative analysis of the gut microbiota of sandfly vectors of zoonotic visceral leishmaniasis (ZVL) in Iran; host-environment interplay shapes diversity[J]. PLoS Negl Trop Dis, 2022, 16(7): e0010609.
[49]	Hurwitz I, Hillesland H, Fieck A, et al. The paratransgenic sandfly: A platform for control of Leishmania transmission[J]. Parasit Vectors, 2011, 4: 82.
[50]	Dey R, Joshi AB, Oliveira F, et al. Gut microbes egested during bites of infected sandflies augment severity of leishmaniasis via inflammasome-derived IL-1β[J]. Cell Host Microbe, 2018, 23(1): 134-143.e6.
[51]	Nimmo DD, Ham PJ, Ward RD, et al. The sandfly Lutzomyia longipalpis shows specific humoral responses to bacterial challenge[J]. Med Vet Entomol, 1997, 11(4): 324-328.
[52]	Tinoco-Nunes B, Telleria EL, da Silva-Neves M, et al. The sandfly Lutzomyia longipalpis LL5 embryonic cell line has active Toll and Imd pathways and shows immune responses to bacteria, yeast and Leishmania[J]. Parasit Vectors, 2016, 9: 222.
[53]	Diaz-Albiter H, Sant’Anna MRV, Genta FA, et al. Reactive oxygen species-mediated immunity against Leishmania mexicana and Serratia marcescens in the sand phlebotomine fly Lutzomyia longipalpis[J]. J Biol Chem, 2012, 287(28): 23995-24003.
[54]	VomáčkováKykalová B, Sassù F, Dutra-Rêgo F, et al. Pathogen-associated molecular patterns (PAMPs) derived from Leishmania and bacteria increase gene expression of antimicrobial peptides and gut surface proteins in sandflies[J]. Int J Parasitol, 2024, 54(10): 485-495.
[55]	Pimenta PF, Modi GB, Pereira ST, et al. A novel role for the peritrophic matrix in protecting Leishmania from the hydrolytic activities of the sandfly midgut[J]. Parasitology, 1997, 115 (Pt 4): 359-369.
[56]	Schlein Y, Jacobson RL. Resistance of Phlebotomus papatasi to infection with Leishmania donovani is modulated by components of the infective bloodmeal[J]. Parasitology, 1998, 117 (Pt 5): 467-473.
[57]	Telleria EL, de Araújo APO, Secundino NF, et al. Trypsin-like serine proteases in Lutzomyia longipalpis: Expression, activity and possible modulation by Leishmania infantum chagasi[J]. PLoS One, 2010, 5(5): e10697.
[58]	da Costa-Latgé SG, Bates P, Dillon R, et al. Characterization of glycoside hydrolase families 13 and 31 reveals expansion and diversification of α-amylase genes in the phlebotomine Lutzomyia longipalpis and modulation of sandfly glycosidase activities by Leishmania infection[J]. Front Physiol, 2021, 12: 635633.
[59]	Jochim RC, Teixeira CR, Laughinghouse A, et al. The midgut transcriptome of Lutzomyia longipalpis: Comparative analysis of cDNA libraries from sugar-fed, blood-fed, post-digested and Leishmania infantum chagasi-infected sandflies[J]. BMC Genomics, 2008, 9: 15.
[60]	Coutinho-Abreu IV, Serafim TD, Meneses C, et al. Leishmania infection induces a limited differential gene expression in the sandfly midgut[J]. BMC Genomics, 2020, 21(1): 608.
[61]	Karimian F, Vatandoost H, Rassi Y, et al. Aerobic midgut microbiota of sandfly vectors of zoonotic visceral leishmaniasis from northern Iran, a step toward finding potential paratransgenic candidates[J]. Parasit Vectors, 2019, 12(1): 10.

发育类型	发育部位	致病特征	典型虫株	媒介白蛉
上幽门型	中肠→前胃	内脏利什曼病或皮肤利什曼病	杜氏利什曼原虫	白蛉属（旧大陆种）
			婴儿利什曼原虫	罗蛉属（新大陆种）
			热带利什曼原虫
围幽门型	后肠→幽门瓣→中肠→前胃	黏膜型内脏利什曼病	巴西利什曼原虫	罗蛉属（新大陆种）
			圭亚那利什曼原虫
			巴拿马利什曼原虫
下幽门型	后肠	非叮咬传播，不感染人类	蜥蜴利什曼原虫亚属	白蛉属（旧大陆种）