Research progress on pathogens carried by sand flies and their gut microbiota

doi:10.12140/j.issn.1000-7423.2025.01.020

Abstract

Abstract:

As a vector of multiple pathogens, sand flies have important epidemiological significance. A large number of microbial communities are colonized in the gut of sand flies, which pose a significant impact on the reproduction, growth and development of sand flies and sand flies-borne pathogens. The review summarizes the species of pathogens carried by sand flies and the composition of gut microbiota, and unravel the interactions among sand flies, pathogens, and gut microbiota. Gut microbiota not only directly inhibits the infection and transmission of pathogens, but also indirectly alters the ability of pathogen infections and transmission by sand flies through participation in the immune responses and defense mechanisms of sand flies.

Key words: Sand fly, Pathogen, Gut microbiota

CLC Number:

R384.1

CUI Lei, FANG Yuan, ZHOU Zhengbin, HE Yaqi, ZHANG Yi. Research progress on pathogens carried by sand flies and their gut microbiota[J]. CHINESE JOURNAL OF PARASITOLOGY AND PARASITIC DISEASES, 2025, 43(1): 129-134.

References 62

[1]	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)
[2]	管立人, 顾灯安, 王捷. 白蛉的生物学和防制对策[J]. 国际医学寄生虫病杂志, 2007, 34(6): 283-290.
	Guan LR, Gu DA, Wang J. Biology and control strategy of Phlebotomine sandfly[J]. Int J Med Parasit Dis, 2007, 34(6): 283-290. (in Chinese)
[3]	Galati EAB, Rodrigues BL. A review of historical Phlebotominae taxonomy (Diptera ∶ Psychodidae)[J]. Neotrop Entomol, 2023, 52(4): 539-559.
[4]	Lozano-Sardaneta YN, Díaz-Cruz JA, Viveros-Santos V, et al. Phylogenetic relations among Mexican phlebotomine sand flies (Diptera ∶ Psychodidae) and their divergence time estimation[J]. PLoS One, 2023, 18(6): e0287853.
[5]	Lozano-Sardaneta YN, Viveros-Santos V, Colunga-Salas P, et al. Is Psathyromyia shannoni (Diptera ∶ Psychodidae ∶ Phlebotominae) a species complex? Retrospective study of genetic diversity of COI gene, pathogens and geographic distribution[J]. Acta Trop, 2023, 238: 106807.
[6]	Karimian F, Koosha M, Choubdar N, et al. Comparative analysis of the gut microbiota of sand fly vectors of zoonotic visceral leishmaniasis (ZVL) in Iran; host-environment interplay shapes diversity[J]. PLoS Negl Trop Dis, 2022, 16(7): e0010609.
[7]	Omondi ZN, Arserim SK, T?z S, et al. Host-parasite interactions: Regulation of Leishmania infection in sand fly[J]. Acta Parasitol, 2022, 67(2): 606-618.
[8]	Labbé F, Abdeladhim M, Abrudan J, et al. Genomic analysis of two phlebotomine sand fly vectors of Leishmania from the New and Old World[J]. PLoS Negl Trop Dis, 2023, 17(4): e0010862.
[9]	Lopez Y, Arana B, Rizzo N, et al. A neglected among the neglected: A review of cutaneous leishmaniasis in Guatemala[J]. Trans R Soc Trop Med Hyg, 2023, 117(9): 609-616.
[10]	Shita EY, Nibret E, Munshea A, et al. Burden and risk factors of cutaneous leishmaniasis in Ethiopia: A systematic review and meta-analysis[J]. Int J Dermatol, 2022, 61(11): 1336-1345.
[11]	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)
[12]	张丽, 马雅军. 基于线粒体DNA的我国中华白蛉群体遗传分化研究[J]. 中国热带医学, 2016, 16(10): 947-952.
	Zhang L, Ma YJ. Molecular population genetic structure of Phlebotomus chinensis (Diptera ∶ Psychodidae) in China inferred by mitochondrial DNA[J]. China Trop Med, 2016, 16(10): 947-952. (in Chinese)
[13]	张红卫, 刘颖, 杨成运, 等. 以全健康理念推进我国内脏利什曼病从控制走向消除[J]. 热带病与寄生虫学, 2022, 20(4): 181-184.
	Zhang HW, Liu Y, Yang CY, et al. Promoting visceral leishmaniasis from control to elimination in China based on One Health approach[J]. J Trop Dis Parasitol, 2022, 20(4): 181-184. (in Chinese)
[14]	罗卓韦, 周正斌, 公衍峰, 等. 我国内脏利什曼病的流行现状和防控挑战[J]. 中国寄生虫学与寄生虫病杂志, 2022, 40(2): 146-152.
	Luo ZW, Zhou ZB, Gong YF, et al. Current status and challenges of visceral leishmaniasis in China[J]. Chin J ParasitolParasit Dis, 2022, 40(2): 146-152. (in Chinese)
[15]	Chen HM, Chen HY, Tao F, et al. Leishmania infection and blood sources analysis in Phlebotomus chinensis (Diptera ∶ Psychodidae) along extension region of the Loess Plateau, China[J]. Infect Dis Poverty, 2020, 9: 125.
[16]	Jancarova M, Polanska N, Volf P, et al. The role of sand flies as vectors of viruses other than phleboviruses[J]. J Gen Virol, 2023, 104(4).
[17]	Ferreira FV, Aguiar ERGR, Olmo RP, et al. The small non-coding RNA response to virus infection in the Leishmania vector Lutzomyia longipalpis[J]. PLoS Negl Trop Dis, 2018, 12(6): e0006569.
[18]	Wang QY, Yin QK, Fu SH, et al. Isolation and identification of sandfly-borne viruses from sandflies collected from June to August, 2019, in Yangquan County, China[J]. Viruses, 2022, 14(12): 2692.
[19]	Paquette SJ, Simon AY, Xiii A, et al. Medically significant vector-borne viral diseases in Iran[J]. Microorganisms, 2023, 11(12): 3006.
[20]	Sellali S, Lafri I, Ayhan N, et al. Neutralizing based sero-prevalence study of Toscana virus in livestock from Algeria[J]. Comp Immunol Microbiol Infect Dis, 2023, 103: 102075.
[21]	Amaro F, Zé-Zé L, Alves MJ. Sandfly-borne phleboviruses in Portugal: Four and still counting[J]. Viruses, 2022, 14(8): 1768.
[22]	程睿, 范娜, 鲁晓睛, 等. 白蛉传播的病毒及其与疾病关系的研究进展[J]. 中国热带医学, 2018, 18(10): 1070-1075.
	Cheng R, Fan N, Lu XJ, et al. Sandflies transmitted virus and its associated infection[J]. China Trop Med, 2018, 18(10): 1070-1075. (in Chinese)
[23]	Li Y, Wang YN, Tian F, et al. First report of Karimabad virus in Rhombomys opimus in China[J]. One Health, 2022,15:100437.
[24]	梁国栋. 我国自然界白蛉携带病毒的研究进展[J]. 中华实验和临床病毒学杂志, 2022, 36(4): 469-474.
	Liang GD. Research progress of natural sandfly-borne viruses in China[J]. Chin J Exp Clin Virol, 2022, 36(4): 469-474. (in Chinese)
[25]	王晶. 山西省虫媒病毒的分离与鉴定: 中国首次从白蛉中分离到白蛉病毒属病毒[D]. 青岛: 青岛大学, 2020: 2-4.
	Wang J. Isolation and identification of insect-borne viruses in Shanxi Province: Sandfly virus was isolated from China for the first time[D]. Qingdao: Qingdao University, 2020: 2-4. (in Chinese)
[26]	Lafri I, Bitam I. Phlebotomine sandflies and associated pathogens in Algeria: Update and comprehensive overview[J]. Vet Ital, 2021, 57(3)
[27]	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.
[28]	Hustedt J, Prasetyo DB, Fiorenzano JM, et al. Correction: Phlebotomine sand flies (Diptera ∶ Psychodidae) and sand fly-borne pathogens in the greater Mekong subregion: A systematic review[J]. Parasit Vectors, 2022, 15(1): 432.
[29]	Mohd Jaafar F, Belhouchet M, Belaganahalli M, et al. Full-genome characterisation of Orungo, Lebombo and Changuinola viruses provides evidence for co-evolution of orbiviruses with their arthropod vectors[J]. PLoS One, 2014, 9(1): e86392.
[30]	Silva SP, Dilcher M, Weber F, et al. Genetic and biological characterization of selected Changuinola viruses (Reoviridae ∶ Orbivirus) from Brazil[J]. J Gen Virol, 2014, 95(Pt 10): 2251-2259.
[31]	Marklewitz M, Handrick S, Grasse W, et al. Gouleako virus isolated from West African mosquitoes constitutes a proposed novel genus in the family Bunyaviridae[J]. J Virol, 2011, 85(17): 9227-9234.
[32]	Zorrilla VO, Lozano ME, Espada LJ, et al. Comparison of sand fly trapping approaches for vector surveillance of Leishmania and Bartonella species in ecologically distinct, endemic regions of Peru[J]. PLoS Negl Trop Dis, 2021, 15(7): e0009517.
[33]	栗冬梅, 张建中, 刘起勇. 中国巴尔通体与相关疾病的研究进展[J]. 中国人兽共患病学报, 2008, 24(8): 762-765, 770.
	Li DM, Zhang JZ, Liu QY. Research progress of Bartonella and related diseases in China[J]. Chin J Zoonoses, 2008, 24(8): 762-765, 770. (in Chinese)
[34]	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.
[35]	Espa?a PP, Uranga A, Cillóniz C, et al. Q fever (Coxiella burnetii)[J]. Semin Respir Crit Care Med, 2020, 41(4): 509-521.
[36]	陆秋成, 何恒果, 蒲德强. 昆虫肠道微生物种类及其功能研究进展[J]. 四川农业科技, 2023(2): 48-52.
	Lu QC, He HG, Pu DQ. Research progress on species and functions of intestinal microorganisms in insects[J]. Sichuan Agric Sci Technol, 2023(2): 48-52. (in Chinese)
[37]	Monteiro CC, Villegas LEM, Campolina TB, et al. Bacterial diversity of the American sand fly Lutzomyia intermedia using high-throughput metagenomic sequencing[J]. Parasit Vectors, 2016, 9(1): 480.
[38]	Akhoundi M, Bakhtiari R, Guillard T, et al. Diversity of the bacterial and fungal microflora from the midgut and cuticle of phlebotomine sand flies collected in North-Western Iran[J]. PLoS One, 2012, 7(11): e50259.
[39]	Abbasi I, Nasereddin A, Warburg A. Development of a next generation DNA sequencing-based multi detection assay for detecting and identifying Leishmania parasites, blood sources, plant meals and intestinal microbiome in phlebotomine sand flies[J]. Acta Trop, 2019, 199: 105101.
[40]	Karimian F, Vatandoost H, Rassi Y, et al. Aerobic midgut microbiota of sand fly vectors of zoonotic visceral leishmaniasis from northern Iran, a step toward finding potential paratransgenic candidates[J]. Parasit Vectors, 2019, 12(1): 10.
[41]	Vivero RJ, Villegas-Plazas M, Cadavid-Restrepo GE, et al. Wild specimens of sand fly phlebotomine Lutzomyia evansi, vector of leishmaniasis, show high abundance of Methylobacterium and natural carriage of Wolbachia and Cardinium types in the midgut microbiome[J]. Sci Rep, 2019, 9(1): 17746.
[42]	Pires ACAM, Villegas LEM, Campolina TB, et al. Bacterial diversity of wild-caught Lutzomyia longipalpis (a vector of zoonotic visceral leishmaniasis in Brazil) under distinct physiological conditions by metagenomics analysis[J]. Parasit Vectors, 2017, 10(1): 627.
[43]	Fraihi W, Fares W, Perrin P, et al. An integrated overview of the midgut bacterial flora composition of Phlebotomus perniciosus, a vector of zoonotic visceral leishmaniasis in the Western Mediterranean Basin[J]. PLoS Negl Trop Dis, 2017, 11(3): e0005484.
[44]	Papadopoulos C, Karas PA, Vasileiadis S, et al. Host species determines the composition of the prokaryotic microbiota in Phlebotomus sandflies[J]. Pathogens, 2020, 9(6): 428.
[45]	Parvizi P, Bordbar A, Najafzadeh N. Detection of Wolbachia pipientis, including a new strain containing the wsp gene, in two sister species of Paraphlebotomus sandflies, potential vectors of zoonotic cutaneous leishmaniasis[J]. Mem Inst Oswaldo Cruz, 2013, 108(4): 414-420.
[46]	Karatepe B, Aksoy S, Karatepe M. Investigation of Wolbachia spp. and Spiroplasma spp. in Phlebotomus species by molecular methods[J]. Sci Rep, 2018, 8(1): 10616.
[47]	Lozano-Sardaneta YN, Marina CF, Torres-Monzón JA, et al. Molecular detection of Wolbachia and Bartonella as part of the microbiome of phlebotomine sand flies from Chiapas, Mexico[J]. Parasitol Res, 2023, 122(6): 1293-1301.
[48]	Pimentel AC, Cesar CS, Martins M, et al. The antiviral effects of the symbiont bacteria Wolbachia in insects[J]. Front Immunol, 2021, 11: 626329.
[49]	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.
[50]	Campolina TB, Villegas LEM, Monteiro CC, et al. Tripartite interactions: Leishmania, microbiota and Lutzomyia longipalpis[J]. PLoS Negl Trop Dis, 2020, 14(10): e0008666.
[51]	Amni F, Maleki-Ravasan N, Nateghi-Rostami M, et al. Co-infection of Phlebotomus papatasi (Diptera ∶ Psychodidae) gut bacteria with Leishmania major exacerbates the pathological responses of BALB/c mice[J]. Front Cell Infect Microbiol, 2023, 13: 1115542.
[52]	Sant’Anna MRV, Diaz-Albiter H, Aguiar-Martins K, et al. Colonisation resistance in the sand fly gut: Leishmania protects Lutzomyia longipalpis from bacterial infection[J]. Parasit Vectors, 2014, 7: 329.
[53]	Moraes CS, Seabra SH, Castro DP, et al. Leishmania (Leishmania) chagasi interactions with Serratia marcescens: Ultrastructural studies, lysis and carbohydrate effects[J]. Exp Parasitol, 2008, 118(4): 561-568.
[54]	Tom A, Pradeep Kumar N, Kumar A, et al. Interactions between Leishmania parasite and sandfly: A review[J]. Parasitol Res, 2023, 123(1): 6.
[55]	Serafim TD, Coutinho-Abreu IV, Dey R, et al. Leishmaniasis: The act of transmission[J]. Trends Parasitol, 2021, 37(11): 976-987.
[56]	Telleria EL, Martins-da-Silva A, Tempone AJ, et al. Leishmania, microbiota and sand fly immunity[J]. Parasitology, 2018, 145(10): 1336-1353.
[57]	刘彪, 康迅, 王悦鑫, 等. 蚊虫肠道菌群的多样性与应用研究进展[J]. 海南医学院学报, 2022, 28(7): 550-554, 560.
	Liu B, Kang X, Wang YX, et al. Research progress on the diversity and application of mosquito intestinal flora[J]. J Hainan Med Univ, 2022, 28(7): 550-554, 560. (in Chinese)
[58]	Blackwell M. Made for each other: Ascomycete yeasts and insects[J]. Microbiol Spectr, 2017, 5(3): 5.3.13.
[59]	Gatesoupe FJ. Live yeasts in the gut: Natural occurrence, dietary introduction, and their effects on fish health and development[J]. Aquaculture, 2007, 267(1/2/3/4): 20-30.
[60]	Martin E, VarottoBoccazzi I, De Marco L, et al. The mycobiota of the sand fly Phlebotomus perniciosus: Involvement of yeast symbionts in uric acid metabolism[J]. Environ Microbiol, 2018, 20(3): 1064-1077.
[61]	Tabbabi A, Mizushima D, Yamamoto DS, et al. Effects of host species on microbiota composition in Phlebotomus and Lutzomyia sand flies[J]. Parasit Vectors, 2023, 16(1): 310.
[62]	Karaku? M, Karabey B, Or?un Kalkan ?, et al. Midgut bacterial diversity of wild populations of Phlebotomus (P.) papatasi, the vector of zoonotic cutaneous leishmaniasis (ZCL) in Turkey[J]. Sci Rep, 2017, 7(1): 14812.