Molecular Detection and Differentiation of Arthropod, Fungal, Protozoan, Bacterial and Viral Pathogens of Honeybees.

Lucas Lannutti, Fernanda Noemi Gonzales, Maria José Dus Santos, Mónica Florin-Christensen, Leonhard Schnittger
Author Information
  1. Lucas Lannutti: Instituto de Patobiología Veterinaria (IPVET), Instituto Nacional de Tecnología Agropecuaria-Consejo Nacional de Investigaciones Científicas y Tecnológicas (INTA-CONICET), Hurlingham 1686, Argentina.
  2. Fernanda Noemi Gonzales: Instituto de Virología e Innovaciones Tecnológicas (IVIT), Instituto Nacional de Tecnología Agropecuaria-Consejo Nacional de Investigaciones Científicas y Tecnológicas (INTA-CONICET), Hurlingham 1686, Argentina.
  3. Maria José Dus Santos: Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET), Buenos Aires 1917, Argentina. ORCID
  4. Mónica Florin-Christensen: Instituto de Patobiología Veterinaria (IPVET), Instituto Nacional de Tecnología Agropecuaria-Consejo Nacional de Investigaciones Científicas y Tecnológicas (INTA-CONICET), Hurlingham 1686, Argentina. ORCID
  5. Leonhard Schnittger: Instituto de Patobiología Veterinaria (IPVET), Instituto Nacional de Tecnología Agropecuaria-Consejo Nacional de Investigaciones Científicas y Tecnológicas (INTA-CONICET), Hurlingham 1686, Argentina. ORCID

Abstract

The honeybee is highly appreciated worldwide because of its products, but also as it is a pollinator of crops and wild plants. The beehive is vulnerable to infections due to arthropods, fungi, protozoa, bacteria and/or viruses that manage to by-pass the individual and social immune mechanisms of bees. Due to the close proximity of bees in the beehive and their foraging habits, infections easily spread within and between beehives. Moreover, international trade of bees has caused the global spread of infections, several of which result in significant losses for apiculture. Only in a few cases can infections be diagnosed with the naked eye, by direct observation of the pathogen in the case of some arthropods, or by pathogen-associated distinctive traits. Development of molecular methods based on the amplification and analysis of one or more genes or genomic segments has brought significant progress to the study of bee pathogens, allowing for: (i) the precise and sensitive identification of the infectious agent; (ii) the analysis of co-infections; (iii) the description of novel species; (iv) associations between geno- and pheno-types and (v) population structure studies. Sequencing of bee pathogen genomes has allowed for the identification of new molecular targets and the development of specific genotypification strategies.

Keywords

References

  1. Viruses. 2021 Jul 11;13(7): [PMID: 34372546]
  2. Appl Environ Microbiol. 1999 May;65(5):2243-5 [PMID: 10224028]
  3. Rev Argent Microbiol. 2017 Apr - Jun;49(2):166-173 [PMID: 28449942]
  4. Gigascience. 2018 Dec 1;7(12): [PMID: 30535280]
  5. J Appl Microbiol. 2015 Sep;119(3):640-54 [PMID: 26176631]
  6. Appl Environ Microbiol. 2012 Jan;78(1):227-35 [PMID: 22020517]
  7. Arch Razi Inst. 2018 Dec;73(4):311-318 [PMID: 31077121]
  8. Curr Protoc Microbiol. 2018 Feb 22;48:9E.1.1-9E.1.6 [PMID: 29512117]
  9. J Virol. 2008 Jul;82(13):6209-17 [PMID: 18434396]
  10. J Econ Entomol. 2010 Aug;103(4):1039-50 [PMID: 20857710]
  11. PLoS Pathog. 2009 Jun;5(6):e1000466 [PMID: 19503607]
  12. Appl Environ Microbiol. 2001 May;67(5):2384-7 [PMID: 11319129]
  13. Mycol Res. 2007 May;111(Pt 5):509-47 [PMID: 17572334]
  14. J Eukaryot Microbiol. 2014 Jan-Feb;61(1):42-50 [PMID: 24102764]
  15. J Invertebr Pathol. 2019 Feb;161:47-53 [PMID: 30707918]
  16. J Invertebr Pathol. 2019 Jan;160:95-97 [PMID: 30448510]
  17. J Invertebr Pathol. 2015 Jul;129:36-9 [PMID: 26031564]
  18. J Invertebr Pathol. 2015 Feb;125:9-15 [PMID: 25527406]
  19. J Invertebr Pathol. 2006 Jan;91(1):69-73 [PMID: 16376930]
  20. Viruses. 2017 Oct 27;9(11): [PMID: 29077069]
  21. Vet Sci. 2020 Sep 08;7(3): [PMID: 32911814]
  22. Neotrop Entomol. 2021 Apr;50(2):312-316 [PMID: 32845459]
  23. Curr Opin Insect Sci. 2018 Apr;26:120-129 [PMID: 29764651]
  24. Vet Microbiol. 2011 Apr 21;149(1-2):200-5 [PMID: 21050682]
  25. Annu Rev Microbiol. 1978;32:221-48 [PMID: 360966]
  26. Parasit Vectors. 2017 Jun 8;10(1):287 [PMID: 28595622]
  27. Environ Microbiol. 2011 Feb;13(2):404-13 [PMID: 20880328]
  28. Environ Microbiol Rep. 2013 Feb;5(1):74-7 [PMID: 23757133]
  29. J Invertebr Pathol. 2015 Sep;130:21-7 [PMID: 26146231]
  30. Int J Syst Evol Microbiol. 2006 Mar;56(Pt 3):501-511 [PMID: 16514018]
  31. Microbiol Spectr. 2017 Apr;5(2): [PMID: 28944750]
  32. Sci Rep. 2018 Jun 11;8(1):8879 [PMID: 29891995]
  33. Microbiology (Reading). 2004 Jul;150(Pt 7):2381-2390 [PMID: 15256579]
  34. J Invertebr Pathol. 2013 Nov;114(3):250-4 [PMID: 24025844]
  35. Microorganisms. 2021 May 18;9(5): [PMID: 34070128]
  36. Genet Mol Res. 2009 Aug 18;8(3):990-7 [PMID: 19731219]
  37. Sci Rep. 2019 Mar 7;9(1):3820 [PMID: 30846803]
  38. J Invertebr Pathol. 2020 Jan;169:107279 [PMID: 31738888]
  39. Vet Sci. 2020 Aug 15;7(3): [PMID: 32824137]
  40. Parasitol Res. 2020 Feb;119(2):411-421 [PMID: 31915912]
  41. Sci Rep. 2016 Sep 14;6:33329 [PMID: 27625313]
  42. Environ Microbiol. 2018 Apr;20(4):1302-1329 [PMID: 29575513]
  43. PLoS One. 2016 Dec 21;11(12):e0167752 [PMID: 28002470]
  44. J Invertebr Pathol. 2016 Feb;134:1-5 [PMID: 26721451]
  45. New Microbiol. 2008 Oct;31(4):439-44 [PMID: 19123297]
  46. Exp Appl Acarol. 2019 Jul;78(3):315-326 [PMID: 31197529]
  47. Parasitol Res. 2012 Apr;110(4):1403-10 [PMID: 21927870]
  48. J Insect Sci. 2016 Jun 01;16(1): [PMID: 27252482]
  49. Environ Microbiol Rep. 2011 Oct;3(5):565-8 [PMID: 23761336]
  50. Microorganisms. 2022 Jan 02;10(1): [PMID: 35056545]
  51. Vet Sci. 2022 Mar 21;9(3): [PMID: 35324875]
  52. Microb Ecol. 2017 May;73(4):978-987 [PMID: 27837253]
  53. J Invertebr Pathol. 2011 Jul;107(3):216-9 [PMID: 21419132]
  54. PLoS One. 2012;7(4):e35954 [PMID: 22563427]
  55. PLoS One. 2017 May 3;12(5):e0176831 [PMID: 28467471]
  56. J Gen Virol. 2005 Aug;86(Pt 8):2281-2289 [PMID: 16033976]
  57. PLoS One. 2012;7(3):e33708 [PMID: 22442715]
  58. Vet Rec. 2012 Oct 20;171(16):400 [PMID: 22940789]
  59. PLoS One. 2017 Aug 17;12(8):e0182814 [PMID: 28817641]
  60. PLoS One. 2017 Nov 15;12(11):e0187924 [PMID: 29140998]
  61. Front Vet Sci. 2021 Feb 26;8:582677 [PMID: 33718463]
  62. Bull Entomol Res. 2021 Feb;111(1):100-110 [PMID: 32594919]
  63. BMC Res Notes. 2014 Dec 05;7:878 [PMID: 25475654]
  64. Sci Rep. 2020 Sep 29;10(1):15953 [PMID: 32994425]
  65. Environ Microbiol Rep. 2013 Aug;5(4):525-9 [PMID: 23864566]
  66. Viruses. 2015 Jul 06;7(7):3586-602 [PMID: 26154017]
  67. J Invertebr Pathol. 2009 Jul;101(3):204-9 [PMID: 19467238]
  68. PLoS One. 2021 May 20;16(5):e0244906 [PMID: 34014937]
  69. PLoS One. 2015 Dec 31;10(12):e0145609 [PMID: 26720131]
  70. J Virol Methods. 2013 Dec;194(1-2):102-6 [PMID: 23948157]
  71. Insects. 2017 Mar 07;8(1): [PMID: 28272333]
  72. Infect Genet Evol. 2015 Apr;31:87-94 [PMID: 25583446]
  73. Vet Clin North Am Food Anim Pract. 2021 Nov;37(3):521-533 [PMID: 34689918]
  74. Annu Rev Entomol. 2000;45:519-48 [PMID: 10761588]
  75. J Gen Virol. 2011 Jan;92(Pt 1):156-61 [PMID: 20926636]
  76. Mol Ecol Resour. 2009 May;9(3):855-8 [PMID: 21564768]
  77. Microb Ecol. 1982 Dec;8(4):387-99 [PMID: 24226055]
  78. BMC Genomics. 2010 Oct 25;11:602 [PMID: 20973996]
  79. Genes (Basel). 2018 Aug 20;9(8): [PMID: 30127293]
  80. Vet Clin North Am Food Anim Pract. 2021 Nov;37(3):401-412 [PMID: 34689910]
  81. PLoS One. 2013;8(3):e57540 [PMID: 23526946]
  82. J Invertebr Pathol. 2012 Jan;109(1):172-4 [PMID: 22138255]
  83. Mol Biol Evol. 2002 Dec;19(12):2313-7 [PMID: 12446822]
  84. Appl Environ Microbiol. 2004 Dec;70(12):7185-91 [PMID: 15574916]
  85. J Appl Microbiol. 2010 Jul;109(1):107-15 [PMID: 20015206]
  86. Environ Microbiol. 2015 Apr;17(4):1414-24 [PMID: 25244044]
  87. Microbiologyopen. 2014 Jun;3(3):341-55 [PMID: 24771723]
  88. Prikl Biokhim Mikrobiol. 2013 Jan-Feb;49(1):88-93 [PMID: 23662456]
  89. FEMS Microbiol Lett. 2014 Aug;357(1):40-8 [PMID: 24975021]
  90. PeerJ. 2020 Jul 17;8:e9424 [PMID: 32742773]
  91. Insects. 2021 Feb 09;12(2): [PMID: 33572468]
  92. Front Microbiol. 2021 Jun 02;12:645353 [PMID: 34149635]
  93. Sci Rep. 2019 Aug 27;9(1):12445 [PMID: 31455863]
  94. Eur J Protistol. 2017 Oct;61(Pt A):13-19 [PMID: 28826077]
  95. Naturwissenschaften. 2013 Mar;100(3):229-34 [PMID: 23340580]
  96. J Invertebr Pathol. 2016 Nov;141:38-40 [PMID: 27816748]
  97. Vet Sci. 2020 Oct 21;7(4): [PMID: 33096775]
  98. J Invertebr Pathol. 2010 Jan;103 Suppl 1:S20-9 [PMID: 19909969]
  99. J Anim Ecol. 2015 May;84(3):615-624 [PMID: 25646973]
  100. Science. 2012 Jun 8;336(6086):1304-6 [PMID: 22679096]
  101. Open Vet J. 2020 Apr;10(1):53-58 [PMID: 32426257]
  102. Appl Environ Microbiol. 2002 Dec;68(12):6446-50 [PMID: 12450876]
  103. Pest Manag Sci. 2018 Dec;74(12):2667-2670 [PMID: 29998601]
  104. PLoS One. 2018 Dec 6;13(12):e0206938 [PMID: 30521535]
  105. J Invertebr Pathol. 2010 Oct;105(2):151-5 [PMID: 20570679]
  106. Parasitol Int. 2021 Aug;83:102361 [PMID: 33894389]
  107. J Invertebr Pathol. 2008 Sep;99(1):8-13 [PMID: 18571197]
  108. J Vet Sci. 2021 May;22(3):e40 [PMID: 34056881]
  109. J Invertebr Pathol. 2010 Jan;103 Suppl 1:S10-9 [PMID: 19909971]
  110. J Invertebr Pathol. 2006 Jun;92(2):105-8 [PMID: 16630626]
  111. PLoS One. 2011;6(6):e20656 [PMID: 21687739]
  112. J Invertebr Pathol. 2013 May;113(1):1-6 [PMID: 23352902]
  113. Viruses. 2020 May 23;12(5): [PMID: 32456246]
  114. PLoS One. 2014 Apr 17;9(4):e95057 [PMID: 24743507]
  115. J Invertebr Pathol. 2010 Jan;103 Suppl 1:S48-61 [PMID: 19909976]
  116. Eur J Protistol. 2020 Apr;73:125688 [PMID: 32143143]
  117. PLoS Pathog. 2014 Jun 26;10(6):e1004230 [PMID: 24968198]
  118. PLoS One. 2014 Mar 05;9(3):e90914 [PMID: 24599066]
  119. Parasitol Int. 2020 Apr;75:102052 [PMID: 31927138]
  120. Rev Argent Microbiol. 2011 Apr-May;43(2):84-6 [PMID: 21731968]
  121. J Invertebr Pathol. 2006 Jun;92(2):93-5 [PMID: 16574143]
  122. Insects. 2018 Nov 16;9(4): [PMID: 30453484]
  123. J Invertebr Pathol. 2011 Nov;108(3):224-5 [PMID: 21939664]
  124. J Invertebr Pathol. 2005 Oct;90(2):118-21 [PMID: 16214161]
  125. J Protozool. 1967 Aug;14(3):485-7 [PMID: 6050656]
  126. Exp Appl Acarol. 2002;27(1-2):69-78 [PMID: 12593513]
  127. PLoS One. 2008;3(12):e4071 [PMID: 19115015]
  128. Front Microbiol. 2019 Jan 24;9:3205 [PMID: 30733713]
  129. Saudi J Biol Sci. 2020 Jan;27(1):518-523 [PMID: 31889877]
  130. Appl Environ Microbiol. 2006 Apr;72(4):2414-20 [PMID: 16597939]
  131. Microb Biotechnol. 2013 Nov;6(6):731-9 [PMID: 23919248]
  132. PLoS One. 2012;7(8):e43562 [PMID: 22927991]
  133. Int J Med Microbiol. 2020 Feb;310(2):151394 [PMID: 31959580]
  134. J Invertebr Pathol. 2006 Feb;91(2):98-104 [PMID: 16376373]
  135. J Invertebr Pathol. 2010 Jan;103 Suppl 1:S30-47 [PMID: 19909972]
  136. Virology. 2011 Aug 15;417(1):106-12 [PMID: 21652054]
  137. Exp Appl Acarol. 2000 Mar;24(3):165-89 [PMID: 11108385]
  138. J Zoo Wildl Med. 2014 Jun;45(2):219-27 [PMID: 25000681]
  139. J Virol. 2009 Nov;83(22):11560-8 [PMID: 19726502]
  140. Microb Ecol. 2015 Aug;70(2):522-33 [PMID: 25794593]
  141. J Invertebr Pathol. 2005 Oct;90(2):98-103 [PMID: 16214164]
  142. Viruses. 2015 Jun 23;7(6):3285-309 [PMID: 26110586]
  143. Parasitol Res. 2018 Feb;117(2):623-628 [PMID: 29282526]
  144. PLoS Biol. 2019 Oct 10;17(10):e3000502 [PMID: 31600204]
  145. Sci Rep. 2017 Jul 11;7(1):5084 [PMID: 28698604]
  146. Microb Pathog. 2021 Oct;159:105122 [PMID: 34352375]
  147. J Invertebr Pathol. 2010 Jan;103 Suppl 1:S96-119 [PMID: 19909970]
  148. Appl Environ Microbiol. 1995 Apr;61(4):1323-30 [PMID: 7747954]
  149. Curr Opin Insect Sci. 2018 Apr;26:142-148 [PMID: 29764654]
  150. Mol Ecol. 2015 May;24(10):2379-91 [PMID: 25846956]
  151. Sci Rep. 2017 Jan 25;7:41045 [PMID: 28120868]
  152. Ann Microbiol (Paris). 1983 May-Jun;134A(3):383-97 [PMID: 6195951]
  153. Acta Vet Hung. 2009 Sep;57(3):383-8 [PMID: 19635710]
  154. Viruses. 2020 Jun 02;12(6): [PMID: 32498304]
  155. Viruses. 2019 Jan 24;11(2): [PMID: 30678330]
  156. Appl Environ Microbiol. 2003 Mar;69(3):1504-10 [PMID: 12620836]
  157. Curr Opin Virol. 2016 Aug;19:16-22 [PMID: 27351468]
  158. Exp Appl Acarol. 2007;43(1):1-24 [PMID: 17828576]
  159. J Invertebr Pathol. 2004 Oct-Nov;87(2-3):84-93 [PMID: 15579317]
  160. J Invertebr Pathol. 2008 Feb;97(2):186-8 [PMID: 17880997]
  161. Proc Natl Acad Sci U S A. 2019 Jan 29;116(5):1792-1801 [PMID: 30647116]
  162. Curr Opin Insect Sci. 2018 Apr;26:89-96 [PMID: 29764667]
  163. Insects. 2020 Apr 16;11(4): [PMID: 32316296]
  164. Ecol Evol. 2019 Aug 14;9(18):10241-10252 [PMID: 31624548]
  165. Viruses. 2014 May 05;6(5):2012-27 [PMID: 24800677]
  166. Insect Mol Biol. 2006 Oct;15(5):715-8 [PMID: 17069642]
  167. Biotechnol Adv. 2018 Jul - Aug;36(4):1167-1184 [PMID: 29608951]
  168. Parasitol Res. 2015 Feb;114(2):651-8 [PMID: 25399817]
  169. Apidologie. 2016;47:251-266 [PMID: 27053820]
  170. PLoS One. 2009 Aug 03;4(8):e6481 [PMID: 19649264]
  171. Mol Ecol. 2000 Sep;9(9):1436-8 [PMID: 10972785]
  172. Genome Biol Evol. 2013;5(6):1151-64 [PMID: 23711669]
  173. Appl Environ Microbiol. 2007 Oct;73(20):6331-8 [PMID: 17675417]
  174. Appl Environ Microbiol. 1998 May;64(5):1983-5 [PMID: 9572987]
  175. Vet Microbiol. 2014 Jun 25;171(1-2):221-6 [PMID: 24768448]
  176. J Invertebr Pathol. 2012 May;110(1):108-13 [PMID: 22425522]
  177. Exp Appl Acarol. 2016 Nov;70(3):287-297 [PMID: 27631761]
  178. Korean J Parasitol. 2015 Jun;53(3):315-20 [PMID: 26174825]
  179. Curr Opin Insect Sci. 2015 Aug;10:65-70 [PMID: 29588016]
  180. Appl Environ Microbiol. 2013 Jun;79(12):3882-6 [PMID: 23584776]
  181. J Invertebr Pathol. 2008 Sep;99(1):117-9 [PMID: 18471826]
  182. Insects. 2021 Apr 19;12(4): [PMID: 33921572]
  183. J Invertebr Pathol. 2011 Oct;108(2):135-7 [PMID: 21839741]
  184. J Econ Entomol. 2021 Apr 13;114(2):520-529 [PMID: 33503242]
  185. ISME J. 2016 May;10(5):1264-73 [PMID: 26574686]
  186. Environ Microbiol Rep. 2016 Jun;8(3):407-12 [PMID: 27083139]
  187. Proc Biol Sci. 2005 Feb 22;272(1561):411-9 [PMID: 15734696]
  188. J Pest Sci (2004). 2021;94(4):1487-1504 [PMID: 34720788]
  189. Insects. 2019 Nov 12;10(11): [PMID: 31726746]
  190. Appl Environ Microbiol. 2009 May;75(10):3344-7 [PMID: 19304833]
  191. Rev Sci Tech. 1997 Apr;16(1):172-6 [PMID: 9329115]
  192. Saudi J Biol Sci. 2017 Jul;24(5):979-982 [PMID: 28663691]
  193. J Invertebr Pathol. 2010 Oct;105(2):164-70 [PMID: 20600088]
  194. Microb Biotechnol. 2017 Mar;10(2):296-322 [PMID: 27273822]
  195. J Gen Virol. 2004 Aug;85(Pt 8):2263-2270 [PMID: 15269367]
  196. Microb Biotechnol. 2016 Nov;9(6):772-781 [PMID: 27365124]
  197. Int J Mol Sci. 2021 Sep 17;22(18): [PMID: 34576241]
  198. J Virol. 2006 Dec;80(23):11528-38 [PMID: 16971448]
  199. J Invertebr Pathol. 2010 Jan;103(1):53-8 [PMID: 19850047]
  200. PLoS Pathog. 2016 Aug 18;12(8):e1005757 [PMID: 27537076]
  201. J Microbiol Methods. 2018 Mar;146:61-63 [PMID: 29391178]
  202. J Invertebr Pathol. 2014 Jun;119:47-9 [PMID: 24746850]
  203. J Invertebr Pathol. 2007 Mar;94(3):222-5 [PMID: 17207498]
  204. Commun Biol. 2019 Oct 1;2:357 [PMID: 31583288]
  205. J Fungi (Basel). 2021 Aug 30;7(9): [PMID: 34575752]
  206. Pathogens. 2021 Aug 17;10(8): [PMID: 34451508]
  207. J Virol Methods. 2012 Mar;180(1-2):26-31 [PMID: 22207079]
  208. Trends Parasitol. 2020 Jul;36(7):592-606 [PMID: 32456963]
  209. Lett Appl Microbiol. 2010 Jun 1;50(6):603-10 [PMID: 20406378]
  210. Appl Environ Microbiol. 2009 Nov;75(22):7212-20 [PMID: 19783750]
  211. Viruses. 2019 May 09;11(5): [PMID: 31075870]
  212. Vet Microbiol. 2014 Mar 14;169(3-4):203-10 [PMID: 24485932]
  213. Parasitology. 2013 Sep;140(11):1346-56 [PMID: 23880415]
  214. Nature. 2016 Dec 8;540(7632):220-229 [PMID: 27894123]
  215. Eur J Protistol. 2018 Apr;63:44-50 [PMID: 29459253]
  216. Annu Rev Virol. 2019 Sep 29;6(1):49-69 [PMID: 31185188]
  217. J Invertebr Pathol. 2010 Oct;105(2):200-3 [PMID: 20600092]
  218. Virulence. 2020 Dec;11(1):554-567 [PMID: 32456539]
  219. J Eukaryot Microbiol. 2015 Sep-Oct;62(5):567-83 [PMID: 25712037]
  220. Lab Chip. 2019 Feb 26;19(5):789-797 [PMID: 30719512]
  221. Ecol Evol. 2013 Feb;3(2):298-311 [PMID: 23467539]
  222. Vet Sci. 2020 Aug 13;7(3): [PMID: 32823756]
  223. Saudi J Biol Sci. 2019 Nov;26(7):1553-1556 [PMID: 31762625]
  224. Parasitol Res. 2012 Aug;111(2):601-7 [PMID: 22453498]
  225. Sci Rep. 2020 May 5;10(1):7532 [PMID: 32372055]
  226. PLoS Pathog. 2014 Jul 31;10(7):e1004261 [PMID: 25079600]
  227. ISME J. 2014 Aug;8(8):1588-97 [PMID: 24599072]
  228. Curr Protoc Hum Genet. 2001 May;Chapter 9:Unit 9.8 [PMID: 18428319]
  229. PLoS One. 2020 Sep 8;15(9):e0237544 [PMID: 32898160]
  230. J Virol Methods. 2014 Mar;197:7-13 [PMID: 24121133]
  231. J Vet Med Sci. 2014 Apr;76(4):491-8 [PMID: 24334815]
  232. J Invertebr Pathol. 2018 Jan;151:76-81 [PMID: 29113738]
  233. Saudi J Biol Sci. 2021 Apr;28(4):2067-2075 [PMID: 33911922]
  234. Insects. 2021 Nov 17;12(11): [PMID: 34821836]
  235. J Eukaryot Microbiol. 2013 May-Jun;60(3):309-12 [PMID: 23445243]
  236. Front Vet Sci. 2021 Apr 12;8:659683 [PMID: 33912610]
  237. Viruses. 2015 May 22;7(5):2654-67 [PMID: 26008705]
  238. J Gen Virol. 2017 Nov;98(11):2864-2875 [PMID: 29058655]
  239. Naturwissenschaften. 2001 Apr;88(4):147-58 [PMID: 11480702]
  240. Insects. 2021 Aug 14;12(8): [PMID: 34442293]
  241. Viruses. 2019 Jan 29;11(2): [PMID: 30699904]
  242. Ital J Food Saf. 2015 Sep 25;4(3):5364 [PMID: 27800411]
  243. J Virol. 2017 Jul 27;91(16): [PMID: 28515299]
  244. Science. 2007 Oct 12;318(5848):283-7 [PMID: 17823314]
  245. Int J Parasitol. 2020 Nov;50(13):1117-1124 [PMID: 32822679]
  246. mBio. 2018 Oct 9;9(5): [PMID: 30301854]
  247. Front Cell Infect Microbiol. 2017 Jul 06;7:301 [PMID: 28730143]
  248. Virus Res. 2008 May;133(2):280-4 [PMID: 18243390]
  249. PLoS One. 2015 Oct 09;10(10):e0140337 [PMID: 26451849]
  250. Microb Ecol. 2020 Nov;80(4):908-919 [PMID: 32666305]
  251. J Virol Methods. 2007 Apr;141(1):7-13 [PMID: 17166598]
  252. Sci Rep. 2020 Jun 26;10(1):10454 [PMID: 32591554]
  253. Mol Ecol Resour. 2008 May;8(3):698-700 [PMID: 21585875]
  254. J Apic Res. 2013 Jan;52(1): [PMID: 24198438]
  255. J Invertebr Pathol. 2007 Sep;96(1):1-10 [PMID: 17428493]
  256. Genome Biol Evol. 2015 Aug 08;7(9):2458-72 [PMID: 26254485]
  257. Exp Appl Acarol. 2017 May;72(1):61-67 [PMID: 28540471]
  258. Nature. 2016 Dec 22;540(7634):539-543 [PMID: 27880757]
  259. Vet Res. 2010 Nov-Dec;41(6):54 [PMID: 20423694]
  260. Vet Parasitol. 2010 Jun 24;170(3-4):212-7 [PMID: 20299152]
  261. PLoS One. 2010 Dec 22;5(12):e14357 [PMID: 21203504]
  262. Braz J Microbiol. 2019 Apr;50(2):471-480 [PMID: 30666531]
  263. Parasitol Res. 2015 Nov;114(11):3999-4004 [PMID: 26210302]
  264. Iran J Parasitol. 2016 Apr-Jun;11(2):259-264 [PMID: 28096862]
  265. Int J Food Microbiol. 2003 Mar 25;81(3):195-201 [PMID: 12485745]
  266. Arch Virol. 2000;145(10):2015-26 [PMID: 11087089]
  267. Curr Opin Insect Sci. 2018 Apr;26:69-75 [PMID: 29764663]
  268. J Vet Sci. 2020 Jan;21(1):e4 [PMID: 31940683]
  269. Clin Microbiol Infect. 2018 Apr;24(4):350-354 [PMID: 29309930]
  270. Clin Diagn Lab Immunol. 2001 Jan;8(1):93-104 [PMID: 11139201]
  271. Exp Parasitol. 2012 Dec;132(4):530-6 [PMID: 22974586]
  272. Sci Rep. 2015 Jun 30;5:10982 [PMID: 26123939]
  273. PLoS One. 2020 Aug 28;15(8):e0238252 [PMID: 32857797]
  274. J Invertebr Pathol. 2011 May;107(1):43-9 [PMID: 21345338]
  275. Genet Mol Res. 2012 Sep 13;11(3):3310-4 [PMID: 23079825]
  276. Vet Med Int. 2021 Aug 11;2021:6346703 [PMID: 34422255]
  277. Exp Appl Acarol. 2019 Feb;77(2):161-171 [PMID: 30810851]
  278. Wellcome Open Res. 2018 Sep 24;3:124 [PMID: 30345391]
  279. Annu Rev Entomol. 2019 Jan 7;64:205-226 [PMID: 30629896]
  280. J Invertebr Pathol. 2013 May;113(1):52-5 [PMID: 23352901]
  281. J Invertebr Pathol. 2016 Sep;139:6-11 [PMID: 27392956]
  282. Rev Sci Tech. 2016 Dec;35(3):825-833 [PMID: 28332647]
  283. J Invertebr Pathol. 2006 Oct;93(2):135-9 [PMID: 16737710]
  284. Adv Virus Res. 2007;70:33-80 [PMID: 17765703]
  285. J Virol Methods. 2021 Jul;293:114163 [PMID: 33864854]
  286. Lett Appl Microbiol. 2004;39(1):25-33 [PMID: 15189284]
  287. J Invertebr Pathol. 2018 May;154:37-41 [PMID: 29608918]
  288. J Bacteriol. 2012 Jun;194(11):3014 [PMID: 22582373]
  289. Vet Microbiol. 2009 Oct 20;139(1-2):193-6 [PMID: 19559547]
  290. Sci Rep. 2017 Dec 12;7(1):17447 [PMID: 29234127]
  291. Environ Microbiol. 2015 Nov;17(11):4443-58 [PMID: 25914091]
  292. Appl Microbiol Biotechnol. 2016 Sep;100(17):7387-95 [PMID: 27394713]
  293. Pest Manag Sci. 2021 Mar;77(3):1476-1481 [PMID: 33135316]
  294. J Invertebr Pathol. 2021 Sep;184:107628 [PMID: 34090931]
  295. Int J Parasitol. 2019 Jul;49(8):657-667 [PMID: 31170411]
  296. Pathogens. 2021 Mar 19;10(3): [PMID: 33808848]
  297. J Econ Entomol. 2017 Apr 1;110(2):319-332 [PMID: 28334185]
  298. J Virol Methods. 2012 Sep;184(1-2):63-8 [PMID: 22609890]
  299. Parasitol Res. 2020 Dec;119(12):3947-3956 [PMID: 33043420]
  300. J Invertebr Pathol. 2016 Jun;137:38-42 [PMID: 27126517]
  301. J Gen Virol. 2007 Dec;88(Pt 12):3428-3438 [PMID: 18024913]
  302. J Virol Methods. 2019 Aug;270:70-78 [PMID: 31026560]
  303. PLoS One. 2017 Dec 19;12(12):e0190017 [PMID: 29261772]

Grants

  1. PICT-2014-1585/Ministry of Science, Technology and Productive Innovation (MinCyT), Argentina
  2. 2019-PE-E1-I017-001/National Agricultural Technology Institute, Argentina

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