Assessing Survival of Transgenic Bacteria, Serratia AS1 and Enterobacter cloacae, in Sugar Bait, White Saxaul Plant (Haloxylon persicum) and Rodent Barrow’s Soil, A Contained-Field Study for Paratransgenesis Approach
-
Marzieh Ghassemi
,
Amir Ahmad Akhavan
,
Alireza Zahraei-Ramezani
,
Bagher Yakhchali
,
Mohammad Reza Zarean
,
Reza Jafari
,
Mohammad Ali Oshaghi
Abstract
Background: The viability and persistence of engineered bacterium candidates in field conditions is one of the considerable challenges in the paratransgenesis approach to fighting vector-borne diseases.
Methods: In this study two engineered bacterium candidates to produce paratransgenic sand flies, Serratia AS1 and Enterobacter cloacae expressing m-Cherry fluorescent were applied on the leaves of the white saxaul plant (Haloxylon persicum), sugar bait, and rodent burrow soil and their persistent time was tested in desert condition, Matin Abad County, Isfahan, August 2022. A PBS suspension of 109 cells/ml was used for sugar bait, spraying on plant leaves (~10 cm2) and 10 cm2 of rodent burrow soil. Sand fly samples were taken daily and were plated on LB Agar and the fluorescent cells were counted after 24 hours.
Results: Time course in general caused a decrease in the number of bacteria for both strains. The two strains were persistent in sugar bait and on plant leaves for four days and on soil for two days. Although there were slight differences between the number of the bacteria in sugar baits, which was not significant (P< 0.05). The number of E. cloacae surviving on plant and in soil were significantly (P< 0.0001 and P= 0.046) higher than Serratia AS1.
Conclusion: This study shows that plants or sugar bait are useful routes for delivery of the transformed bacteria for the paratransgenesis approach, although, the bacteria ought to be sprayed on plants or sugar baits should be replaced with new ones in four days intervals.
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2. Fofana A, Yerbanga RS, Bilgo E, Ouedraogo GA, Gendrin M, Ouedraogo JB (2022) The Strategy of Paratransgenesis for the Control of Malaria Transmission. Front Trop Dis. 3: 867104.
3. Wilke ABB, Marrelli MT (2015) Para-transgen¬esis: a promising new strategy for mosquito vector control. Parasit Vec-tors. 8: 342.
4. Ratcliffe NA, Furtado Pacheco JP, Dyson P, Castro HC, Gonzalez MS, Azambuja P, Mello CB (2022) Overview of para-transgenesis as a strategy to control path¬ogen transmission by insect vectors. Par¬asit Vectors. 15(1): 112.
5. Oshaghi MA, Rassi Y, Tajedin L, Abai MR, Akhavan AA, Enayati A, Moh¬tarami F (2011) Mitochondrial DNA di¬versity in the populations of great gerbils, Rhom-bomys opimus, the main reservoir of cu-taneous leishmaniasis. Acta Trop. 119 (2–3): 165–171.
6. Rassi Y, Oshaghi MA, Azani SM, Abaie MR, Rafizadeh S, Mohebai M, Moh-tarami F, Zeinali Mk (2011) Molecular detection of Leishmania infection due to Leishmania major and Leishmania tu-ran¬ica in the vectors and reservoir host in Iran. Vector Borne Zoonotic Dis. 11 (2): 145–150.
7. Hajjaran H, Mohebali M, Abai MR, Oshaghi MA, Zarei Z, Charehdar S, Mirjalali H, Sharifdini M, Teimouri A (2013) Natu¬ral infection and phylogenetic classifica¬tion of Leishmania spp. infecting Rhom¬bomys opimus, a primary reservoir host of zoonotic cutaneous leishmaniasis in Northeast Iran. Trans R Soc Trop Med Hyg. 107(9): 550–557.
8. Bakhshi H, Oshaghi MA, Abai MR, Rassi Y, Akhavan AA, Mohebali M, Hajaran H, Mohtarami F, Mirzajani H, Maleki-Ravasan N (2013) MtDNA CytB Struc-ture of Rhombomys opimus (Rodentia: Gerbellidae), the Main Reservoir of Cu-taneous Leishmania¬sis in the Borderline of Iran-Turkmenistan. J Arthropod Borne Dis. 7(2): 173–184.
9. Hajjaran H, Mohebali M, Teimouri A, Oshaghi MA, Mirjalali H, Kazemi-Rad E, Shiee MR, Naddaf SR (2014) Identi-fi¬cation and phylogenetic relationship of Iranian strains of various Leishmania spe¬cies isolated from cutaneous and vis-cer¬al cases of leish¬maniasis based on N-acetyl¬glucosamine-1-phosphate transfer-ase gene. Infect Genet Evol. 26: 203–212.
10. Yurchenko V, Chistyakov DS, Akhmad-ishina LV, Lukashev AN, Sádlová J, Strelko¬va MV (2023) Revisiting epide-mi¬ology of leishmaniasis in central Asia: les¬sons learnt. Parasitology. 150(2): 129–136.
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16. Da Costa SG, Moraes CDS, Bates P, Dil-lon R, Genta FA (2019) Development of Leishmania mexicana in Lutzomyia long¬ipalpis in the absence of sugar feeding. Mem Inst Oswaldo Cruz. 114: e180482.
17. Killick-Kendrick R, Killick-Kendrick M (1987) Honeydew of aphids as a source of sugar for Phlebotomus ariasi. Med Vet Entomol. 1(3): 297–302.
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21. Gálvez R, Montoya A, Fontal F, Martínez De Murguía L, Miró G (2018) Control-ling phlebotomine sand flies to prevent canine Leishmania infantum infection: A case of knowing your enemy. Res Vet Sci. 121: 94–103.
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23. Koosha M, Vatandoost H, Karimian F, Choubdar N, Oshaghi MA (2019) Deliv-ery of a genetically marked Serratia AS1 to medically important arthropods for use in RNAi and paratransgenic control strat¬egies. Microb Ecol. 78(1): 185–194.
24. Abbasi R (2017) Determining the dynam-ics of the Entrobacter cloacae-RFP- De-fensin population in the gut of Phleboto-mus papatasi, vector for zoonotic cuta-ne¬ous leishmaniasis, and its effect on Leishmania major burden in the vector under laboratory condition. [MSc the-sis]. School of Public Health, Teh¬ran Univer¬sity of Medical Sciences, Iran.
25. Dehghan H, Oshaghi MA, Moosa-Kazemi SH, Yakhchali B, Vatandoost H, Ma-leki-Ravasan N, Rassi Y, Moham¬madza-deh H, Abai MR, Mohtarami F (2017) Dynamics of Transgenic Enterobacter clo¬acae Expressing Green Fluorescent Pro¬tein Defensin (GFP-D) in Anopheles ste¬phensi Under Laboratory Condition. J Art¬hropod Borne Dis. 11(4): 515–532.
26. Dehghan H (2017) Utility of para¬trans-gen¬ic Anopheles stephensi using recombi¬nant bacteria Enterobacter cloacae express¬ing defensin and scorpine to decrease ma¬lar¬ia vector capacity: [PhD dissertation]. School of Public Health, Tehran Univer¬sity of Medical Sciences, Iran.
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28. Pires ACAM, Villegas LEM, Campolina TB, Orfanó AS, Pimenta PFP, Secun-dino NFC (2017) Bacterial diversity of wild-caught Lutzomyia longipalpis (a vec¬tor of zoonotic visceral leishmaniasis in Brazil) under distinct physiological con¬di¬tions by metagenomics analysis. Para¬sit Vectors. 10(1): 627.
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30. Karimian F, Koosha M, Choubdar N, Oshaghi MA (2022) Comparative anal-ysis of the gut microbiota of sand fly vectors of zoonotic visceral leish¬mani-asis (ZVL) in Iran; host-environment in-ter¬play shapes diversity. PLoS Negl Trop Dis. 16(7): e0010609.
31. Hurwitz I, Hillesland H, Fieck A, Das P, Durvasula R (2011) The paratransgenic sand fly: a platform for control of Leish-mania transmission. Parasit Vec¬tors. 4: 82.
32. Huang W, Vega-Rodriguez J, Kizito C, Cha SJ, Jacobs-Lorena M (2022) Combin¬ing transgenesis with paratransgenesis to fight malaria. Elife. 11: e77584.
33. Dehghan H, Mosa-Kazemi SH, Yakhchali B, Maleki-Ravasan N, Vatandoost H, Oshaghi MA (2022) Evaluation of anti-malaria potency of wild and genetically modified Enterobacter cloacae express-ing effector proteins in Anopheles ste-phensi. Parasit Vectors. 15(1): 63.
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2. Fofana A, Yerbanga RS, Bilgo E, Ouedraogo GA, Gendrin M, Ouedraogo JB (2022) The Strategy of Paratransgenesis for the Control of Malaria Transmission. Front Trop Dis. 3: 867104.
3. Wilke ABB, Marrelli MT (2015) Para-transgen¬esis: a promising new strategy for mosquito vector control. Parasit Vec-tors. 8: 342.
4. Ratcliffe NA, Furtado Pacheco JP, Dyson P, Castro HC, Gonzalez MS, Azambuja P, Mello CB (2022) Overview of para-transgenesis as a strategy to control path¬ogen transmission by insect vectors. Par¬asit Vectors. 15(1): 112.
5. Oshaghi MA, Rassi Y, Tajedin L, Abai MR, Akhavan AA, Enayati A, Moh¬tarami F (2011) Mitochondrial DNA di¬versity in the populations of great gerbils, Rhom-bomys opimus, the main reservoir of cu-taneous leishmaniasis. Acta Trop. 119 (2–3): 165–171.
6. Rassi Y, Oshaghi MA, Azani SM, Abaie MR, Rafizadeh S, Mohebai M, Moh-tarami F, Zeinali Mk (2011) Molecular detection of Leishmania infection due to Leishmania major and Leishmania tu-ran¬ica in the vectors and reservoir host in Iran. Vector Borne Zoonotic Dis. 11 (2): 145–150.
7. Hajjaran H, Mohebali M, Abai MR, Oshaghi MA, Zarei Z, Charehdar S, Mirjalali H, Sharifdini M, Teimouri A (2013) Natu¬ral infection and phylogenetic classifica¬tion of Leishmania spp. infecting Rhom¬bomys opimus, a primary reservoir host of zoonotic cutaneous leishmaniasis in Northeast Iran. Trans R Soc Trop Med Hyg. 107(9): 550–557.
8. Bakhshi H, Oshaghi MA, Abai MR, Rassi Y, Akhavan AA, Mohebali M, Hajaran H, Mohtarami F, Mirzajani H, Maleki-Ravasan N (2013) MtDNA CytB Struc-ture of Rhombomys opimus (Rodentia: Gerbellidae), the Main Reservoir of Cu-taneous Leishmania¬sis in the Borderline of Iran-Turkmenistan. J Arthropod Borne Dis. 7(2): 173–184.
9. Hajjaran H, Mohebali M, Teimouri A, Oshaghi MA, Mirjalali H, Kazemi-Rad E, Shiee MR, Naddaf SR (2014) Identi-fi¬cation and phylogenetic relationship of Iranian strains of various Leishmania spe¬cies isolated from cutaneous and vis-cer¬al cases of leish¬maniasis based on N-acetyl¬glucosamine-1-phosphate transfer-ase gene. Infect Genet Evol. 26: 203–212.
10. Yurchenko V, Chistyakov DS, Akhmad-ishina LV, Lukashev AN, Sádlová J, Strelko¬va MV (2023) Revisiting epide-mi¬ology of leishmaniasis in central Asia: les¬sons learnt. Parasitology. 150(2): 129–136.
11. Maleki-Ravasan N, Oshaghi MA, Afshar D, Arandian MH, Hajikhani S, Akhavan AA, Yakhchali B, Shirazi MH, Rassi Y, Jafa¬ri R, Aminian K, Fazeli-Varzaneh RA, Dur¬vasula R (2015) Aerobic bacterial flo¬ra of biotic and abiotic compartments of a hyperendemic Zoonotic Cutaneous Leish¬maniasis (ZCL) focus. Parasit Vec¬tors. 8: 63.
12. Ghassemi M, Akhavan AA, Zahraei-Ram-azani A, Yakhchali B, Arandian MH, Jafa¬ri R, Akhlaghi M, Shirani-Bidabadi L, Azam K, Koosha M, Oshaghi MA (2023) Rodents as vehicle for delivery of trans¬genic bacteria to make paratransgenic sand fly vectors of cutaneous leish¬man¬iasis in field condition. Sci Rep. 13(1): 14912.
13. Akhlaghi M (2017) Study on dynamics of modified bacteria (Enterobacter cloacae and Serratia AS1) in Phlebotomus pa¬pa-tasi, the main vector of zoonotic cu¬ta-neous leishmaniasis in Iran [MSc the¬sis]. School of Public Health, Teh¬ran Uni¬ver-sity of Medical Sciences, Iran.
14. Wang S, Dos-Santos ALA, Huang W, Liu KC, Oshaghi MA, Wei G, Agre P, Ja-cobs-Lorena M (2017) Driving mos¬qui¬to refractoriness to Plasmodium falci¬pa-rum with engineered symbiotic bacteria. Science. 357(6358): 1399–1402.
15. Müller GC, Revay EE, Schlein Y (2011) Relative attraction of the sand fly Phleboto¬mus papatasi to local flowering plants in the Dead Sea region. J Vector Ecol. 36 Suppl 1: S187–194.
16. Da Costa SG, Moraes CDS, Bates P, Dil-lon R, Genta FA (2019) Development of Leishmania mexicana in Lutzomyia long¬ipalpis in the absence of sugar feeding. Mem Inst Oswaldo Cruz. 114: e180482.
17. Killick-Kendrick R, Killick-Kendrick M (1987) Honeydew of aphids as a source of sugar for Phlebotomus ariasi. Med Vet Entomol. 1(3): 297–302.
18. Qualls WA, Müller GC, Khallaayoune K, Revay EE, Zhioua E, Kravchenko VD, Arheart KL, Xue RD, Schlein Y, Haus-mann A, Kline DL, Beier JC (2015) Con¬trol of sand flies with attractive toxic sugar baits (ATSB) and potential impact on non-target organisms in Morocco. Par¬asit Vectors. 8: 87.
19. Saghafipour A, Vatandoost H, Zahraei-Ram¬azani AR, Yaghoobi-Ershadi MR, Rassi Y, Shirzadi MR, Akhavan AA (2016) Bi¬oassay evaluation of residual activity of attractive toxic sugar-treated barrier fence in the control of Phlebotomus papatasi (Diptera: Psy-chodidae). J Vector Borne Dis. 53(4): 335–340.
20. Saghafipour A, Vatandoost H, Zahraei-Ramazani AR, Yaghoobi-Ershadi MR, Rassi Y, Karami Jooshin M, Shirzadi MR, Akhavan AA (2017) Control of zo-onotic cutaneous leishmaniasis vector, Phleboto¬mus papatasi, using attractive toxic sugar baits (ATSB). PLoS One. 12(4): e0173558.
21. Gálvez R, Montoya A, Fontal F, Martínez De Murguía L, Miró G (2018) Control-ling phlebotomine sand flies to prevent canine Leishmania infantum infection: A case of knowing your enemy. Res Vet Sci. 121: 94–103.
22. Yousefi S, Zahraei-Ramazani AR, Rassi Y, Vatandoost H, Yaghoobi-Ershadi MR, Af¬latoonian MR, Akhavan AA, Aghaei-Af¬shar A, Amin M, Paksa A (2020) Evalu¬a¬tion of Different Attractive Traps for Cap¬tur¬ing Sand Flies (Diptera: Psy¬chodidae) in an Endemic Area of Leish¬maniasis, Southeast of Iran. J Arthropod Borne Dis. 14(2): 202–213.
23. Koosha M, Vatandoost H, Karimian F, Choubdar N, Oshaghi MA (2019) Deliv-ery of a genetically marked Serratia AS1 to medically important arthropods for use in RNAi and paratransgenic control strat¬egies. Microb Ecol. 78(1): 185–194.
24. Abbasi R (2017) Determining the dynam-ics of the Entrobacter cloacae-RFP- De-fensin population in the gut of Phleboto-mus papatasi, vector for zoonotic cuta-ne¬ous leishmaniasis, and its effect on Leishmania major burden in the vector under laboratory condition. [MSc the-sis]. School of Public Health, Teh¬ran Univer¬sity of Medical Sciences, Iran.
25. Dehghan H, Oshaghi MA, Moosa-Kazemi SH, Yakhchali B, Vatandoost H, Ma-leki-Ravasan N, Rassi Y, Moham¬madza-deh H, Abai MR, Mohtarami F (2017) Dynamics of Transgenic Enterobacter clo¬acae Expressing Green Fluorescent Pro¬tein Defensin (GFP-D) in Anopheles ste¬phensi Under Laboratory Condition. J Art¬hropod Borne Dis. 11(4): 515–532.
26. Dehghan H (2017) Utility of para¬trans-gen¬ic Anopheles stephensi using recombi¬nant bacteria Enterobacter cloacae express¬ing defensin and scorpine to decrease ma¬lar¬ia vector capacity: [PhD dissertation]. School of Public Health, Tehran Univer¬sity of Medical Sciences, Iran.
27. Akhoundi M, Bakhtiari R, Guillard T, Baghaei A, Tolouei R, Sereno D, Tou¬bas D, Depaquit J, Abyaneh MR (2012) Di-versity of the bacterial and fungal mi¬cro-flora from the midgut and cuticle of phlebotomine sand flies collected in North-Western Iran. PLoS One. 7(11): e50259.
28. Pires ACAM, Villegas LEM, Campolina TB, Orfanó AS, Pimenta PFP, Secun-dino NFC (2017) Bacterial diversity of wild-caught Lutzomyia longipalpis (a vec¬tor of zoonotic visceral leishmaniasis in Brazil) under distinct physiological con¬di¬tions by metagenomics analysis. Para¬sit Vectors. 10(1): 627.
29. Gunathilaka N, Perera H, Wijerathna T, Rodrigo W, Wijegunawardana NDAD (2020) The Diversity of Midgut Bacteria among Wild-Caught Phlebotomus ar-gen¬tipes (Psychodidae: Phlebotominae), the Vector of Leishmaniasis in Sri Lanka. Biomed Res Int. 2020: 5458063.
30. Karimian F, Koosha M, Choubdar N, Oshaghi MA (2022) Comparative anal-ysis of the gut microbiota of sand fly vectors of zoonotic visceral leish¬mani-asis (ZVL) in Iran; host-environment in-ter¬play shapes diversity. PLoS Negl Trop Dis. 16(7): e0010609.
31. Hurwitz I, Hillesland H, Fieck A, Das P, Durvasula R (2011) The paratransgenic sand fly: a platform for control of Leish-mania transmission. Parasit Vec¬tors. 4: 82.
32. Huang W, Vega-Rodriguez J, Kizito C, Cha SJ, Jacobs-Lorena M (2022) Combin¬ing transgenesis with paratransgenesis to fight malaria. Elife. 11: e77584.
33. Dehghan H, Mosa-Kazemi SH, Yakhchali B, Maleki-Ravasan N, Vatandoost H, Oshaghi MA (2022) Evaluation of anti-malaria potency of wild and genetically modified Enterobacter cloacae express-ing effector proteins in Anopheles ste-phensi. Parasit Vectors. 15(1): 63.
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| Files | ||
| Issue | Vol 18 No 1 (2024) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/jad.v18i1.15668 | |
| Keywords | ||
| Paratransgenesis Symbionts Sand fly Leishmaniasis Vector-borne diseases | ||
| Rights and permissions | |
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Ghassemi M, Akhavan AA, Zahraei-Ramezani A, Yakhchali B, Zarean MR, Jafari R, Oshaghi M. Assessing Survival of Transgenic Bacteria, Serratia AS1 and Enterobacter cloacae, in Sugar Bait, White Saxaul Plant (Haloxylon persicum) and Rodent Barrow’s Soil, A Contained-Field Study for Paratransgenesis Approach. J Arthropod Borne Dis. 2024;18(1):12–27.
