Identification of Intestinal Fungal Microflora and Bacterial Pathogens in the Collected Adult Ixodes ricinus from the Northern Provinces of Iran
-
Manijeh Yousefi Behzadi
,
Neda Moazzezy
,
Mehdi Rohani
,
Saied Reza Naddaf
,
Ehsan Mostafavi
,
Ali Mohamadi
,
Masoomeh Shams-Ghahfarokhi
,
Nasrin Pashootan
,
Mehdi Razzaghi-Abyaneh
Abstract
Background: Ticks are vectors of many pathogens that involve various important diseases in humans and animals, they have several diverse hosts consequently can retain a diverse group of indigenous microbes, from bacteria to fungi. Little is known about the prevalence and diversity of tick microflora colonizing the midgut and their effects on ticks and their interaction. This information is important for development of vector control strategies.
Methods: This study was carried out in northern Iran during autumn 2019. Ticks, Ixodes ricinus caught alive on the bodies of domestic animals in the fall. The tick homogenate was prepared. The identification of fungal isolates was carried out according to a combination of macro and microscopic morphology and molecular sequencing. Pathogenic bacteria of the family Borreliaceae, Francisella tularensis, Borrelia burgdorferi and Coxiella burnetii were tested by real-time PCR.
Results: A total of 133 mature I. ricinus ticks were collected from domestic animals, including 71.5% cattle and 28.5% sheep. The tick frequency rates were 87.21% for Mazandaran, 8.28% for Golestan and 4.51% for Gilan Provinces. Total prevalence of fungal tick contamination was 53.4% (75/133) of which Trichoderma harzianum (57%) was the most prevalent species followed by Aspergillus spp. (42%), Mortierella alpine (19%) and Penicillium polonicum (14%). All tick samples were negative for three pathogenic bacteria including Francisella tularensis, Coxiella burnetii, and Borrelia burgdorferi by real-time PCR analysis.
Conclusion: These results show a first picture of the microbial diversity of ticks and highlight the importance of microbiota and their role in host-pathogen interaction.
1. Irwin PJ, Jefferies R (2004) Arthropod-trans¬mitted diseases of companion animals in Southeast Asia. Trend Parasitol. 20(1): 27–34.
2. Krenn HW, Aspöck H (2012) Form, func-tion and evolution of the mouthparts of blood-feeding Arthropoda. Arthropod Struct Develop. 41(2): 101–118.
3. Abraham NM, Liu L, Jutras BL, Yadav AK, Narasimhan S, Gopalakrishnan V, An¬sari JM, Jefferson KK, Cava F, Ja-cobs-Wagner C, Fikrig E (2017) Patho-gen-mediated manipulation of arthropod mi¬crobiota to promote infection. Proc Natl Acad Sci. 114(5): E781–E90.
4. Bonnet SI, Binetruy F, Hernández-Jarguín AM, Duron O (2017) The tick microbi-ome: why non-pathogenic microorgan-isms matter in tick biology and pathogen transmission. Front Cell Infect Microbi-ol. 7: 236.
5. Sonenshine DE (2018) Range expansion of tick disease vectors in North America: im¬plications for spread of tick-borne dis-ease. Int J Environ Res Publ Health. 15 (3): 478.
6. Choubdar N, Karimian F, Koosha M, Oshaghi MA (2021) An integrated overview of the bacterial flora composition of Hyalom¬ma anatolicum, the main vector of CCHF. PLoS Negl Trop Dis. 15(6): e0009480.
7. Eisen RJ, Kugeler KJ, Eisen L, Beard CB, Paddock CD (2017) Tick-borne zoono-ses in the United States: persistent and emerging threats to human health. ILAR J. 58(3): 319–335.
8. Shah SZ, Jabbar B, Ahmed N, Rehman A, Nasir H, Nadeem S, Jabbar I, Rahman ZU, Azam S (2018) Epidemiology, path-o¬gen¬esis, and control of a tick-borne disease-Kyasanur forest disease: current status and future directions. Front Cell Infect Mi¬crobiol. 8: 149.
9. Kilpatrick AM, Dobson AD, Levi T, Salkeld DJ, Swei A, Ginsberg HS, Kjemtrup A, Padgett KA, Jensen PM, Fish D, Ogden NH, Diuk-Wasser MA (2017) Lyme dis¬ease ecology in a changing world: con¬sensus, uncertainty and critical gaps for im¬proving control. Philosoph Transact Roy¬al Soc B: Biol Sci. 372(1722): 20160117.
10. Shams-Davatchi C (1997) The first en-dem¬ic case of lyme brocellosis in Iran. Med J Islamic Republ Iran. 11(3): 237.
11. Naddaf SR, Mahmoudi A, Ghasemi A, Ro¬hani M, Mohammadi A, Ziapour SP, Nemati AH, Mostafavi E (2020) Infec-tion of hard ticks in the Caspian Sea lit-toral of Iran with Lyme borreliosis and relapsing fever borreliae. Ticks Tick-borne Dis. 11(6): 101500.
12. Zellner B, Huntley JF (2019) Ticks and Tularemia: Do We Know What We Don't Know? Front Cell Infect Microbiol. 9: 146.
13. Rahravani M, Moravedji M, Mostafavi E, Baseri N, Seyfi H, Mohammadi M, Ziaei AH, Mozoun MM, Latifian M, Esmaeili S (2022) Molecular detection of Fran-cisella tularensis in small ruminants and their ticks in western Iran, Comp Immu-nol Microbiol Infect Dis. 83: 101779.
14. Kirkan Ş, Erbaş G, Parin U (2017) Bacte-rial Tick-Borne Diseases of Livestock Animals. Chapter 7, In: Livestock Sci-enc¬es (Sekin S. Eds.), InTech Open, Ri-jeka, Croatia, pp. 109–128.
15. Moradnejad P, Esmaeili S, Maleki M, Sadeghpour A, Kamali M, Rohani M, Ghasemi A, Bagheri Amiri F, Pasha HR, Boudagh S, Bakhshandeh H, Naderi N, Ghadrdoost B, Lotfian S, Dehghan Manshadi SA, Mostafavi E (2019) Q fe-ver endocarditis in Iran. Sci Rep. 9(1): 1–7.
16. Nokhodian Z, Feizi A, Ataei B, Hoseini SG, Mostafavi E (2017) Epidemiology of Q fever in Iran: A systematic review and meta-analysis for estimating sero¬log-ical and molecular prevalence. J Res Med Sci. 22: 121.
17. Khatat SEH, Sahibi H (2015) Anaplasma phagocytophilum: An emerging but un-recognized tick-borne pathogen. Rev Mar Sci Agron Vét. 3(2): 43–52.
18. Hosseini-Vasoukolaei N, Oshaghi MA, Sha¬yan P, Vatandoost H, Ba-bamahmoudi F, Yaghoobi-Ershadi MR, Telmadarraiy Z, Mohtarami F (2014) Anaplasma Infec¬tion in Ticks, Livestock and Human in Ghaemshahr, Mazandaran Province, Iran. J Arthropod Borne Dis. 8(2): 204–211.
19. Martino C, Dilmore AH, Burcham ZM, Metcalf JL, Jeste D, Knight R (2022) Mi¬crobiota succession throughout life from the cradle to the grave. Nat Rev Micro¬biol. 20: 707–720.
20. Clube J (2018) Altering microbial popula-tions and modifying microbiota. Google Patents.
21. Mathison BA, Pritt BS (2014) Laboratory identification of arthropod ectoparasites. Clin Microbiol Rev. 27(1): 48–67.
22. Švec P, Hönig V, Zubriková D, Wittmann M, Pfister K, Grubhoffer L (2019) The use of multi-criteria evaluation for the selec¬tion of study plots for monitoring of I. rici¬nus ticks–Example from Central Eu¬rope. Ticks Tick-borne Dis. 10(4): 905–910.
23. Rehman A, Nijhof AM, Sauter-Louis C, Schauer B, Staubach C, Conraths FJ (2017) Distribution of ticks infesting ru-minants and risk factors associated with high tick prevalence in livestock farms in the semi-arid and arid agro-ecological zones of Pakistan. Parasit Vectors. 10(1): 190.
24. Mansfield KL, Jizhou L, Phipps LP, John-son N (2017) Emerging tick-borne vi-ruses in the twenty-first century. Front Cell In¬fect Microbiol. 7: 298.
25. Rahbari S, Nabian S, Shayan P (2007) Pri-mary report on distribution of tick fauna in Iran. Parasitol Res. 101(2): 175–177.
26. Yakhchali M, Hosseine A (2006) Preva-lence and ectoparasites fauna of sheep and goats flocks in Urmia suburb, Iran. Vet¬erinarski Arhiv. 76(5): 431–442.
27. Sofizadeh A, Telmadarraiy Z, Rahnama A, Gorganli-Davaji A, Hosseini-Chegeni A (2014) Hard tick species of livestock and their bioecology in Golestan Province, north of Iran. J Arthropod Borne Dis. 8 (1): 108–116.
28. Hosseini-Chegani A, Tavakoli M, Telma-darraiy Z (2019) The updated list of ticks (Acari: Ixodidae and Argasidae) occur¬ring in Iran with a key to the identifica¬tion of species. Syst Appl Acarol. 24(11): 2133–2166.
29. Yakhchali M, Rostami A, Esmaelzadeh M (2011) Diversity and seasonal distribu-tion of ixodid ticks in the natural habitat of domestic ruminants in north and south of Iran. Revue Méd Vét. 162(5): 229–235.
30. Anderson JF, Magnarelli LA (2008) Biol-ogy of ticks. Infectious disease clinics of North America. 22(2): 195–215.
31. Akhoundi M, Bakhtiari R, Guillard T, Baghaei A, Tolouei R, Sereno D, Toubas D, Depaquit J, Abyaneh MR (2012) Di-versity of the bacterial and fungal mi¬cro-flora from the midgut and cuticle of phlebotom¬ine sand flies collected in North-Western Iran. PloS One. 7(11): e50259.
32. Mygind PH, Fischer RL, Schnorr KM, Han¬sen MT, Sönksen CP, Ludvigsen S, Raventós D, Buskov S, Christensen B, De Maria L, Taboureau O, Yaver D, Elvig-Jørgensen SG, Sørensen MV, Chris¬tensen BE, Kjaerulff S, Frimodt-Moller N, Leh¬rer RI, Zasloff M, Kristensen HH (2005) Plectasin is a peptide antibiotic with ther¬apeutic potential from a saprophytic fun¬gus. Nature. 437(7061): 975–980.
33. Yeo H, Pell JK, Alderson PG, Clark SJ, Pye BJ (2003) Laboratory evaluation of temperature effects on the germination and growth of entomopathogenic fungi and on their pathogenicity to two aphid species. Pest Manag Sci: formerly Pest Sci. 59(2): 156–165.
34. Yoder JA, Dobrotka CJ, Fisher KA, LeB-arge AP, Pekins PJ, McLellan S (2018) Entomopathogenic fungi of the winter tick in moose wallows: a possible bio-con¬trol for adult moose? ALCES. 54: 55–70.
35. Kalsbeek V, Frandsen F, Steenberg T (1995) Entomopathogenic fungi associated with Ixodes ricinus ticks. Exp Appl Acarol. 19 (1): 45–51.
36. Rao GUB, Narladkar BW (2018) Role of entomopathogenic fungi in tick control: A review. J Entomol Zoolog Stud. 6(1): 1265–1269.
37. Szczepańska A, Kiewra D, Plewa-Tutaj K, Dyczko D, Guz-Regner K (2020) Sen-sitivity of Ixodes ricinus (L.,1758) and Dermacentor reticulatus (Fabr.,1794) ticks to entomopathogenic fungi isolates: pre¬liminary study. Parasitol Res. 119(11): 3857–3861.
38. Institute of Medicine (2011) Critical Needs and Gaps in Understanding Prevention, Ame¬lioration, and Resolution of Lyme and Other Tick-Borne Diseases: The Short-Term and Long-Term Outcomes: Work¬shop Report. Washington, DC: The Na¬tional Academies Press. Available at: https://doi.org/10.17226/13134.
39. Guizzo MG, Dolezelikova K, Neupane S, Frantova H, Hrbatova A, Pafco B, Fiorot¬ti J, Kopacek P, Zurek L (2022) Char¬ac¬terization and manipulation of the bacte¬rial community in the midgut of Ixodes ricinus. Parasit Vectors. 15: 248.
40. Carpi G, Cagnacci F, Wittekindt NE, Zhao F, Qi J, Tomsho LP, Drautz DI, Rizzoli A, Schuster SC (2011) Meta-genomic pro¬file of the bacterial communities associ¬at¬ed with Ixodes ricinus ticks. Plos One. 6(10): e25604.
41. Goodrich JK, Di Rienzi SC, Poole AC, Koren O, Walters WA, Caporaso JG, Knight R, Ley RE (2014) Conducting a microbiome study. Cell. 158(2): 250–262.
42. Hartelt K, Wurst E, Collatz J, Zimmer-mann G, Kleespies RG, Oehme RM, Kim¬mig P, Steidle JLM, Mackenstedt U (2008) Biological control of the tick Ixodes rici¬nus with entomopathogenic fungi and nem¬atodes: Preliminary results from la¬bor¬atory experiments. Int J Med Micro¬biol. 298: 314–320.
43. Wassermann M, Selzer P, Steidle JL, Macken¬stedt U (2016) Biological con-trol of Ixodes ricinus larvae and nymphs with Metarhizium anisopliae blasto-spores. Ticks tick-borne Dis. 7(5): 768–771.
44. Zhioua E, Ginsberg HS, Humber RA, LeBrun RA (1999) Preliminary survey for entomopathogenic fungi associated with Ixodes scapularis (Acari: Ixodidae) in south¬ern New York and New England, USA. J Med Entomol. 36(5): 635–637.
45. Saravanakumar K, Li Y, Yu C, Wang Q, Wang M, Sun J, Gao JX, Chen J (2017) Effect of Trichoderma harzianum on maize rhizosphere microbiome and biocontrol of Fusarium Stalk rot. Sci Rep. 7(1): 1–13.
2. Krenn HW, Aspöck H (2012) Form, func-tion and evolution of the mouthparts of blood-feeding Arthropoda. Arthropod Struct Develop. 41(2): 101–118.
3. Abraham NM, Liu L, Jutras BL, Yadav AK, Narasimhan S, Gopalakrishnan V, An¬sari JM, Jefferson KK, Cava F, Ja-cobs-Wagner C, Fikrig E (2017) Patho-gen-mediated manipulation of arthropod mi¬crobiota to promote infection. Proc Natl Acad Sci. 114(5): E781–E90.
4. Bonnet SI, Binetruy F, Hernández-Jarguín AM, Duron O (2017) The tick microbi-ome: why non-pathogenic microorgan-isms matter in tick biology and pathogen transmission. Front Cell Infect Microbi-ol. 7: 236.
5. Sonenshine DE (2018) Range expansion of tick disease vectors in North America: im¬plications for spread of tick-borne dis-ease. Int J Environ Res Publ Health. 15 (3): 478.
6. Choubdar N, Karimian F, Koosha M, Oshaghi MA (2021) An integrated overview of the bacterial flora composition of Hyalom¬ma anatolicum, the main vector of CCHF. PLoS Negl Trop Dis. 15(6): e0009480.
7. Eisen RJ, Kugeler KJ, Eisen L, Beard CB, Paddock CD (2017) Tick-borne zoono-ses in the United States: persistent and emerging threats to human health. ILAR J. 58(3): 319–335.
8. Shah SZ, Jabbar B, Ahmed N, Rehman A, Nasir H, Nadeem S, Jabbar I, Rahman ZU, Azam S (2018) Epidemiology, path-o¬gen¬esis, and control of a tick-borne disease-Kyasanur forest disease: current status and future directions. Front Cell Infect Mi¬crobiol. 8: 149.
9. Kilpatrick AM, Dobson AD, Levi T, Salkeld DJ, Swei A, Ginsberg HS, Kjemtrup A, Padgett KA, Jensen PM, Fish D, Ogden NH, Diuk-Wasser MA (2017) Lyme dis¬ease ecology in a changing world: con¬sensus, uncertainty and critical gaps for im¬proving control. Philosoph Transact Roy¬al Soc B: Biol Sci. 372(1722): 20160117.
10. Shams-Davatchi C (1997) The first en-dem¬ic case of lyme brocellosis in Iran. Med J Islamic Republ Iran. 11(3): 237.
11. Naddaf SR, Mahmoudi A, Ghasemi A, Ro¬hani M, Mohammadi A, Ziapour SP, Nemati AH, Mostafavi E (2020) Infec-tion of hard ticks in the Caspian Sea lit-toral of Iran with Lyme borreliosis and relapsing fever borreliae. Ticks Tick-borne Dis. 11(6): 101500.
12. Zellner B, Huntley JF (2019) Ticks and Tularemia: Do We Know What We Don't Know? Front Cell Infect Microbiol. 9: 146.
13. Rahravani M, Moravedji M, Mostafavi E, Baseri N, Seyfi H, Mohammadi M, Ziaei AH, Mozoun MM, Latifian M, Esmaeili S (2022) Molecular detection of Fran-cisella tularensis in small ruminants and their ticks in western Iran, Comp Immu-nol Microbiol Infect Dis. 83: 101779.
14. Kirkan Ş, Erbaş G, Parin U (2017) Bacte-rial Tick-Borne Diseases of Livestock Animals. Chapter 7, In: Livestock Sci-enc¬es (Sekin S. Eds.), InTech Open, Ri-jeka, Croatia, pp. 109–128.
15. Moradnejad P, Esmaeili S, Maleki M, Sadeghpour A, Kamali M, Rohani M, Ghasemi A, Bagheri Amiri F, Pasha HR, Boudagh S, Bakhshandeh H, Naderi N, Ghadrdoost B, Lotfian S, Dehghan Manshadi SA, Mostafavi E (2019) Q fe-ver endocarditis in Iran. Sci Rep. 9(1): 1–7.
16. Nokhodian Z, Feizi A, Ataei B, Hoseini SG, Mostafavi E (2017) Epidemiology of Q fever in Iran: A systematic review and meta-analysis for estimating sero¬log-ical and molecular prevalence. J Res Med Sci. 22: 121.
17. Khatat SEH, Sahibi H (2015) Anaplasma phagocytophilum: An emerging but un-recognized tick-borne pathogen. Rev Mar Sci Agron Vét. 3(2): 43–52.
18. Hosseini-Vasoukolaei N, Oshaghi MA, Sha¬yan P, Vatandoost H, Ba-bamahmoudi F, Yaghoobi-Ershadi MR, Telmadarraiy Z, Mohtarami F (2014) Anaplasma Infec¬tion in Ticks, Livestock and Human in Ghaemshahr, Mazandaran Province, Iran. J Arthropod Borne Dis. 8(2): 204–211.
19. Martino C, Dilmore AH, Burcham ZM, Metcalf JL, Jeste D, Knight R (2022) Mi¬crobiota succession throughout life from the cradle to the grave. Nat Rev Micro¬biol. 20: 707–720.
20. Clube J (2018) Altering microbial popula-tions and modifying microbiota. Google Patents.
21. Mathison BA, Pritt BS (2014) Laboratory identification of arthropod ectoparasites. Clin Microbiol Rev. 27(1): 48–67.
22. Švec P, Hönig V, Zubriková D, Wittmann M, Pfister K, Grubhoffer L (2019) The use of multi-criteria evaluation for the selec¬tion of study plots for monitoring of I. rici¬nus ticks–Example from Central Eu¬rope. Ticks Tick-borne Dis. 10(4): 905–910.
23. Rehman A, Nijhof AM, Sauter-Louis C, Schauer B, Staubach C, Conraths FJ (2017) Distribution of ticks infesting ru-minants and risk factors associated with high tick prevalence in livestock farms in the semi-arid and arid agro-ecological zones of Pakistan. Parasit Vectors. 10(1): 190.
24. Mansfield KL, Jizhou L, Phipps LP, John-son N (2017) Emerging tick-borne vi-ruses in the twenty-first century. Front Cell In¬fect Microbiol. 7: 298.
25. Rahbari S, Nabian S, Shayan P (2007) Pri-mary report on distribution of tick fauna in Iran. Parasitol Res. 101(2): 175–177.
26. Yakhchali M, Hosseine A (2006) Preva-lence and ectoparasites fauna of sheep and goats flocks in Urmia suburb, Iran. Vet¬erinarski Arhiv. 76(5): 431–442.
27. Sofizadeh A, Telmadarraiy Z, Rahnama A, Gorganli-Davaji A, Hosseini-Chegeni A (2014) Hard tick species of livestock and their bioecology in Golestan Province, north of Iran. J Arthropod Borne Dis. 8 (1): 108–116.
28. Hosseini-Chegani A, Tavakoli M, Telma-darraiy Z (2019) The updated list of ticks (Acari: Ixodidae and Argasidae) occur¬ring in Iran with a key to the identifica¬tion of species. Syst Appl Acarol. 24(11): 2133–2166.
29. Yakhchali M, Rostami A, Esmaelzadeh M (2011) Diversity and seasonal distribu-tion of ixodid ticks in the natural habitat of domestic ruminants in north and south of Iran. Revue Méd Vét. 162(5): 229–235.
30. Anderson JF, Magnarelli LA (2008) Biol-ogy of ticks. Infectious disease clinics of North America. 22(2): 195–215.
31. Akhoundi M, Bakhtiari R, Guillard T, Baghaei A, Tolouei R, Sereno D, Toubas D, Depaquit J, Abyaneh MR (2012) Di-versity of the bacterial and fungal mi¬cro-flora from the midgut and cuticle of phlebotom¬ine sand flies collected in North-Western Iran. PloS One. 7(11): e50259.
32. Mygind PH, Fischer RL, Schnorr KM, Han¬sen MT, Sönksen CP, Ludvigsen S, Raventós D, Buskov S, Christensen B, De Maria L, Taboureau O, Yaver D, Elvig-Jørgensen SG, Sørensen MV, Chris¬tensen BE, Kjaerulff S, Frimodt-Moller N, Leh¬rer RI, Zasloff M, Kristensen HH (2005) Plectasin is a peptide antibiotic with ther¬apeutic potential from a saprophytic fun¬gus. Nature. 437(7061): 975–980.
33. Yeo H, Pell JK, Alderson PG, Clark SJ, Pye BJ (2003) Laboratory evaluation of temperature effects on the germination and growth of entomopathogenic fungi and on their pathogenicity to two aphid species. Pest Manag Sci: formerly Pest Sci. 59(2): 156–165.
34. Yoder JA, Dobrotka CJ, Fisher KA, LeB-arge AP, Pekins PJ, McLellan S (2018) Entomopathogenic fungi of the winter tick in moose wallows: a possible bio-con¬trol for adult moose? ALCES. 54: 55–70.
35. Kalsbeek V, Frandsen F, Steenberg T (1995) Entomopathogenic fungi associated with Ixodes ricinus ticks. Exp Appl Acarol. 19 (1): 45–51.
36. Rao GUB, Narladkar BW (2018) Role of entomopathogenic fungi in tick control: A review. J Entomol Zoolog Stud. 6(1): 1265–1269.
37. Szczepańska A, Kiewra D, Plewa-Tutaj K, Dyczko D, Guz-Regner K (2020) Sen-sitivity of Ixodes ricinus (L.,1758) and Dermacentor reticulatus (Fabr.,1794) ticks to entomopathogenic fungi isolates: pre¬liminary study. Parasitol Res. 119(11): 3857–3861.
38. Institute of Medicine (2011) Critical Needs and Gaps in Understanding Prevention, Ame¬lioration, and Resolution of Lyme and Other Tick-Borne Diseases: The Short-Term and Long-Term Outcomes: Work¬shop Report. Washington, DC: The Na¬tional Academies Press. Available at: https://doi.org/10.17226/13134.
39. Guizzo MG, Dolezelikova K, Neupane S, Frantova H, Hrbatova A, Pafco B, Fiorot¬ti J, Kopacek P, Zurek L (2022) Char¬ac¬terization and manipulation of the bacte¬rial community in the midgut of Ixodes ricinus. Parasit Vectors. 15: 248.
40. Carpi G, Cagnacci F, Wittekindt NE, Zhao F, Qi J, Tomsho LP, Drautz DI, Rizzoli A, Schuster SC (2011) Meta-genomic pro¬file of the bacterial communities associ¬at¬ed with Ixodes ricinus ticks. Plos One. 6(10): e25604.
41. Goodrich JK, Di Rienzi SC, Poole AC, Koren O, Walters WA, Caporaso JG, Knight R, Ley RE (2014) Conducting a microbiome study. Cell. 158(2): 250–262.
42. Hartelt K, Wurst E, Collatz J, Zimmer-mann G, Kleespies RG, Oehme RM, Kim¬mig P, Steidle JLM, Mackenstedt U (2008) Biological control of the tick Ixodes rici¬nus with entomopathogenic fungi and nem¬atodes: Preliminary results from la¬bor¬atory experiments. Int J Med Micro¬biol. 298: 314–320.
43. Wassermann M, Selzer P, Steidle JL, Macken¬stedt U (2016) Biological con-trol of Ixodes ricinus larvae and nymphs with Metarhizium anisopliae blasto-spores. Ticks tick-borne Dis. 7(5): 768–771.
44. Zhioua E, Ginsberg HS, Humber RA, LeBrun RA (1999) Preliminary survey for entomopathogenic fungi associated with Ixodes scapularis (Acari: Ixodidae) in south¬ern New York and New England, USA. J Med Entomol. 36(5): 635–637.
45. Saravanakumar K, Li Y, Yu C, Wang Q, Wang M, Sun J, Gao JX, Chen J (2017) Effect of Trichoderma harzianum on maize rhizosphere microbiome and biocontrol of Fusarium Stalk rot. Sci Rep. 7(1): 1–13.
| Files | ||
| Issue | Vol 16 No 2 (2022) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/jad.v16i2.11801 | |
| Keywords | ||
| Microflora Ixodes ricinus Fungal species Mycoflora Microbiome | ||
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How to Cite
1.
Yousefi Behzadi M, Moazzezy N, Rohani M, Naddaf SR, Mostafavi E, Mohamadi A, Shams-Ghahfarokhi M, Pashootan N, Razzaghi-Abyaneh M. Identification of Intestinal Fungal Microflora and Bacterial Pathogens in the Collected Adult Ixodes ricinus from the Northern Provinces of Iran. J Arthropod Borne Dis. 2023;16(2):97–107.
