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Erschienen in: Archives of Virology 12/2022

13.09.2022 | Original Article

Characterization of Solenopsis invicta virus 4, a polycipivirus infecting the red imported fire ant Solenopsis invicta

verfasst von: Steven M. Valles, David H. Oi, Jason B. Oliver, James J. Becnel

Erschienen in: Archives of Virology | Ausgabe 12/2022

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Abstract

Solenopsis invicta virus 4 (SINV-4), a new polycipivirus, was characterized in the host in which it was discovered, Solenopsis invicta. SINV-4 was detected in the worker and larval stages of S. invicta, but not in pupae, male or female alates, or queens. The SINV-4 titer was highest in worker ants, with a mean of 1.14 × 107 ± 5.84 ×107 SINV-4 genome equivalents/ng RNA. Electron microscopic examination of negatively stained samples from particles purified from SINV-4-infected fire ant workers revealed isometric particles with a mean diameter of 47.3 ± 1.4 nm. The mean inter-colony SINV-4 infection rate among S. invicta worker ants was 45.8 ± 38.6 in Alachua County, Florida. In S. invicta collected in Argentina, SINV-4 was detected in 22% of 54 colonies surveyed from across the Formosa region. There did not appear to be any seasonality associated with the SINV-4 infection rate among S. invicta nests. SINV-4 was successfully transmitted to uninfected S. invicta colonies by feeding. Among three colonies of S. invicta inoculated with SINV-4, two retained the infection for up to 72 days. The replicative genome strand of SINV-4 was detected in 18% (n = 11) of SINV-4-infected S. invicta colonies. Among 33 ant species examined, the plus genome strand of SINV-4 was detected in undetermined species of Dorymyrmex and Pheidole, Cyphomyrmex rimosus, Monomorium pharaonis, Pheidole obscurithorax, Solenopsis geminata, Solenopsis richteri, Solenopsis xyloni, and Solenopsis invicta. However, the replicative (minus) genome strand was only detected in S. invicta. SINV-4 infection did not impact brood production or queen fecundity in S. invicta. The mean brood rating (63.3% ± 8.8) after 31 days for SINV-4-infected colonies was not statistically different from that of uninfected colonies (48.3 ± 25.5). At the end of the 31-day test period, mean egg production was not significantly different between SINV-4-infected S. invicta colonies (287.7 ± 45.2 eggs laid/24 hours) and uninfected control colonies (193.0 ± 43.6 eggs laid/24 hours).
Literatur
1.
Zurück zum Zitat APHIS (2021) Imported Fire Ants. USDA-APHIS APHIS (2021) Imported Fire Ants. USDA-APHIS
2.
Zurück zum Zitat Buren WF (1972) Revisionary studies on the taxonomy of the imported fire ants. J Ga Entomol So 7:1–26 Buren WF (1972) Revisionary studies on the taxonomy of the imported fire ants. J Ga Entomol So 7:1–26
3.
Zurück zum Zitat Callcott AMA, Collins HL (1996) Invasion and range expansion of imported fire ants (Hymenoptera: Formicidae) in North America from 1918–1995. Fla Entomol 79:240–251CrossRef Callcott AMA, Collins HL (1996) Invasion and range expansion of imported fire ants (Hymenoptera: Formicidae) in North America from 1918–1995. Fla Entomol 79:240–251CrossRef
4.
Zurück zum Zitat Chen Y, Becnel JJ, Valles SM (2012) RNA viruses infecting pest insects. In: Vega F, Kaya HK (eds) Insect Pathology. Elsevier, Amsterdam, pp 133–170CrossRef Chen Y, Becnel JJ, Valles SM (2012) RNA viruses infecting pest insects. In: Vega F, Kaya HK (eds) Insect Pathology. Elsevier, Amsterdam, pp 133–170CrossRef
5.
Zurück zum Zitat Craggs JK, Ball JK, Thomson BJ, Irving WL, Grabowska AM (2001) Development of a strand-specific RT-PCR based assay to detect the replicative form of Hepatitis C virus RNA. J Virol Methods 94:111–120CrossRef Craggs JK, Ball JK, Thomson BJ, Irving WL, Grabowska AM (2001) Development of a strand-specific RT-PCR based assay to detect the replicative form of Hepatitis C virus RNA. J Virol Methods 94:111–120CrossRef
6.
Zurück zum Zitat Deyrup M, Cover S (2004) A new species of Odontomachus ant (Hymenoptera: Formicidae) from inland ridges of Florida, with a key to Odontomachus of the United States. Fla Entomol 87:136–144CrossRef Deyrup M, Cover S (2004) A new species of Odontomachus ant (Hymenoptera: Formicidae) from inland ridges of Florida, with a key to Odontomachus of the United States. Fla Entomol 87:136–144CrossRef
7.
Zurück zum Zitat Fisher BL, Cover SP (2007) Ants of North America, a guide to the genera. University of California Press, BerkeleyCrossRef Fisher BL, Cover SP (2007) Ants of North America, a guide to the genera. University of California Press, BerkeleyCrossRef
8.
Zurück zum Zitat Hashimoto Y, Valles SM (2008) Infection characteristics of Solenopsis invicta virus 2 in the red imported fire ant, Solenopsis invicta. J Invertebr Pathol 99:136–140CrossRef Hashimoto Y, Valles SM (2008) Infection characteristics of Solenopsis invicta virus 2 in the red imported fire ant, Solenopsis invicta. J Invertebr Pathol 99:136–140CrossRef
9.
Zurück zum Zitat Hsu HW, Chiu MC, Shoemaker D, Yang CCS (2018) Viral infections in fire ants lead to reduced foraging activity and dietary changes.Sci Rep-Uk8 Hsu HW, Chiu MC, Shoemaker D, Yang CCS (2018) Viral infections in fire ants lead to reduced foraging activity and dietary changes.Sci Rep-Uk8
10.
Zurück zum Zitat Hsu HW, Chiu MC, Shih CJ, Matsuura K, Yang CS (2019) Apoptosis as a primary defense mechanism in response to viral infection in invasive fire ant Solenopsis invicta. Virology 531:255–259CrossRef Hsu HW, Chiu MC, Shih CJ, Matsuura K, Yang CS (2019) Apoptosis as a primary defense mechanism in response to viral infection in invasive fire ant Solenopsis invicta. Virology 531:255–259CrossRef
11.
Zurück zum Zitat Klein D, Janda P, Steinborn R, Muller M, Salmons B, Gunzburg WH (1999) Proviral load determination of different feline immunodeficiency virus isolates using real-time polymerase chain reaction: influence of mismatches on quantification. Electrophoresis 20:291–299CrossRef Klein D, Janda P, Steinborn R, Muller M, Salmons B, Gunzburg WH (1999) Proviral load determination of different feline immunodeficiency virus isolates using real-time polymerase chain reaction: influence of mismatches on quantification. Electrophoresis 20:291–299CrossRef
12.
Zurück zum Zitat Lacey LA, Frutos R, Kaya HK, Vail P (2001) Insect pathogens as biological control agents: Do they have a future? Biol cont 21:230–248CrossRef Lacey LA, Frutos R, Kaya HK, Vail P (2001) Insect pathogens as biological control agents: Do they have a future? Biol cont 21:230–248CrossRef
13.
Zurück zum Zitat MacGown JA (2003) Ants (Formicidae) of the Southeastern United States. Mississippi State University, Mississippi MacGown JA (2003) Ants (Formicidae) of the Southeastern United States. Mississippi State University, Mississippi
14.
Zurück zum Zitat Manfredini F, Shoemaker D, Grozinger CM (2016) Dynamic changes in host-virus interactions associated with colony founding and social environment in fire ant queens (Solenopsis invicta). Ecol Evol 6:233–244CrossRef Manfredini F, Shoemaker D, Grozinger CM (2016) Dynamic changes in host-virus interactions associated with colony founding and social environment in fire ant queens (Solenopsis invicta). Ecol Evol 6:233–244CrossRef
15.
Zurück zum Zitat Oi DH, Porter SD, Valles SM (2015) A review of the biological control of fire ants (Hymenoptera: Formicidae). Myrmecological News 21:101–116 Oi DH, Porter SD, Valles SM (2015) A review of the biological control of fire ants (Hymenoptera: Formicidae). Myrmecological News 21:101–116
16.
Zurück zum Zitat Oi DH, Valles SM, Porter SD, Cavanaugh C, White G, Henke J (2019) Introduction of fire ant biological control agents into the Coachella Valley of California. Fla Entomol 102:284–286CrossRef Oi DH, Valles SM, Porter SD, Cavanaugh C, White G, Henke J (2019) Introduction of fire ant biological control agents into the Coachella Valley of California. Fla Entomol 102:284–286CrossRef
17.
Zurück zum Zitat Olendraite I, Lukhovitskaya NI, Porter SD, Valles SM, Firth AE (2017) Polycipiviridae: a proposed new family of polycistronic picorna-like RNA viruses. J Gen Virol 98:2368–2378CrossRef Olendraite I, Lukhovitskaya NI, Porter SD, Valles SM, Firth AE (2017) Polycipiviridae: a proposed new family of polycistronic picorna-like RNA viruses. J Gen Virol 98:2368–2378CrossRef
18.
Zurück zum Zitat Olendraite I, Brown K, Valles SM, Firth AE, Chen YP, Guerin DMA, Hashimoto Y, Herrero S, de Miranda JR, Ryabov E, Lefkowitz EJ, Davison AJ, Siddell SG, Simmonds P, Sabanadzovic S, Smith DB, Orton RJ, Knowles NJ, Consortium IR (2019) ICTV Virus Taxonomy Profile: Polycipiviridae. J Gen Virol 100:554–555CrossRef Olendraite I, Brown K, Valles SM, Firth AE, Chen YP, Guerin DMA, Hashimoto Y, Herrero S, de Miranda JR, Ryabov E, Lefkowitz EJ, Davison AJ, Siddell SG, Simmonds P, Sabanadzovic S, Smith DB, Orton RJ, Knowles NJ, Consortium IR (2019) ICTV Virus Taxonomy Profile: Polycipiviridae. J Gen Virol 100:554–555CrossRef
19.
Zurück zum Zitat Pereira RM (2003) Areawide suppression of fire ant populations in pastures: Project update. J Agric Urban Entomol 20:123–130 Pereira RM (2003) Areawide suppression of fire ant populations in pastures: Project update. J Agric Urban Entomol 20:123–130
20.
Zurück zum Zitat Porter SD, Valles SM, Oi DH (2013) Host specificity and colony impacts of Solenopsis invicta virus 3. J Invertebr Pathol 114:1–6CrossRef Porter SD, Valles SM, Oi DH (2013) Host specificity and colony impacts of Solenopsis invicta virus 3. J Invertebr Pathol 114:1–6CrossRef
21.
Zurück zum Zitat Porter SD, Valles SM, Wild AL, Dieckmann R, Plowes NJR (2015) Solenopsis invicta virus 3: further host-specificity tests with native Solenopsis ants (Hymenoptera: Formicidae). Fla Entomol 98:122–125CrossRef Porter SD, Valles SM, Wild AL, Dieckmann R, Plowes NJR (2015) Solenopsis invicta virus 3: further host-specificity tests with native Solenopsis ants (Hymenoptera: Formicidae). Fla Entomol 98:122–125CrossRef
22.
Zurück zum Zitat Porter SD, Gavilanez-Slone JM, Valles SM (2016) Solenopsis invicta virus 3: infection tests with adult honey bees (Hymenoptera: Apidae). Fla Entomol 99:729–733CrossRef Porter SD, Gavilanez-Slone JM, Valles SM (2016) Solenopsis invicta virus 3: infection tests with adult honey bees (Hymenoptera: Apidae). Fla Entomol 99:729–733CrossRef
23.
Zurück zum Zitat Rabeling C, Cover SP, Johnson RA, Mueller UG (2007) A review of the North American species of the fungus-gardening ant genus Trachymyrmex (Hymenoptera: Formicidae). Zootaxa:1–53 Rabeling C, Cover SP, Johnson RA, Mueller UG (2007) A review of the North American species of the fungus-gardening ant genus Trachymyrmex (Hymenoptera: Formicidae). Zootaxa:1–53
24.
Zurück zum Zitat SAS (2009) Base SAS 9.2 procedures guide. SAS Institute, Cary, NC SAS (2009) Base SAS 9.2 procedures guide. SAS Institute, Cary, NC
25.
Zurück zum Zitat Trager JC, MacGown JA, Trager MD (2007) Revision of the nearctic endemic Formica pallidefulva group. In: Snelling RR, Fisher BL, Ward PS (eds) Advances in ant systematics (Hymenoptera: Formicidae): homage to E O Wilson–50 years of contributions. Plazi.org Trager JC, MacGown JA, Trager MD (2007) Revision of the nearctic endemic Formica pallidefulva group. In: Snelling RR, Fisher BL, Ward PS (eds) Advances in ant systematics (Hymenoptera: Formicidae): homage to E O Wilson–50 years of contributions. Plazi.org
26.
Zurück zum Zitat Tschinkel WR (2006) The fire ants. The Belknap Press of Harvard University Press, Cambridge Tschinkel WR (2006) The fire ants. The Belknap Press of Harvard University Press, Cambridge
27.
Zurück zum Zitat Valles SM, Strong CA, Dang PM, Hunter WB, Pereira RM, Oi DH, Shapiro AM, Williams DF (2004) A picorna-like virus from the red imported fire ant, Solenopsis invicta: initial discovery, genome sequence, and characterization. Virology 328:151–157CrossRef Valles SM, Strong CA, Dang PM, Hunter WB, Pereira RM, Oi DH, Shapiro AM, Williams DF (2004) A picorna-like virus from the red imported fire ant, Solenopsis invicta: initial discovery, genome sequence, and characterization. Virology 328:151–157CrossRef
28.
Zurück zum Zitat Valles SM, Strong CA, Hashimoto Y (2007) A new positive-strand RNA virus with unique genome characteristics from the red imported fire ant, Solenopsis invicta. Virology 365:457–463CrossRef Valles SM, Strong CA, Hashimoto Y (2007) A new positive-strand RNA virus with unique genome characteristics from the red imported fire ant, Solenopsis invicta. Virology 365:457–463CrossRef
29.
Zurück zum Zitat Valles SM, Strong CA, Oi DH, Porter SD, Pereira RM, Vander Meer RK, Hashimoto Y, Hooper-Bui LM, Sanchez-Arroyo H, Davis T, Karpakakunjaram V, Vail KM, Fudd Graham LC, Briano JA, Calcaterra LA, Gilbert LE, Ward R, Ward K, Oliver JB, Taniguchi G, Thompson DC (2007) Phenology, distribution, and host specificity of Solenopsis invicta virus-1. J Invertebr Pathol 96:18–27CrossRef Valles SM, Strong CA, Oi DH, Porter SD, Pereira RM, Vander Meer RK, Hashimoto Y, Hooper-Bui LM, Sanchez-Arroyo H, Davis T, Karpakakunjaram V, Vail KM, Fudd Graham LC, Briano JA, Calcaterra LA, Gilbert LE, Ward R, Ward K, Oliver JB, Taniguchi G, Thompson DC (2007) Phenology, distribution, and host specificity of Solenopsis invicta virus-1. J Invertebr Pathol 96:18–27CrossRef
30.
Zurück zum Zitat Valles SM, Hashimoto Y (2009) Isolation and characterization of Solenopsis invicta virus 3, a new postive-strand RNA virus infecting the red imported fire ant, Solenopsis invicta. Virology 388:354–361CrossRef Valles SM, Hashimoto Y (2009) Isolation and characterization of Solenopsis invicta virus 3, a new postive-strand RNA virus infecting the red imported fire ant, Solenopsis invicta. Virology 388:354–361CrossRef
31.
Zurück zum Zitat Valles SM, Varone L, Ramirez L, Briano J (2009) Multiplex detection of Solenopsis invicta viruses – 1, -2, and – 3. J Virol Methods 162:276–279CrossRef Valles SM, Varone L, Ramirez L, Briano J (2009) Multiplex detection of Solenopsis invicta viruses – 1, -2, and – 3. J Virol Methods 162:276–279CrossRef
32.
Zurück zum Zitat Valles SM, Oi DH, Porter SD (2010) Seasonal variation and the co-occurrence of four pathogens and a group of parasites among monogyne and polygyne fire ant colonies. Biol Control 54:342–348CrossRef Valles SM, Oi DH, Porter SD (2010) Seasonal variation and the co-occurrence of four pathogens and a group of parasites among monogyne and polygyne fire ant colonies. Biol Control 54:342–348CrossRef
33.
Zurück zum Zitat Valles SM, Oi DH, Plowes RM, Sanchez-Arroyo H, Varone L, Conant P, Webb G (2013) Geographic distribution suggests that Solenopsis invicta is the host of predilection for Solenopsis invicta virus 1. J Invertebr Pathol 113:232–236CrossRef Valles SM, Oi DH, Plowes RM, Sanchez-Arroyo H, Varone L, Conant P, Webb G (2013) Geographic distribution suggests that Solenopsis invicta is the host of predilection for Solenopsis invicta virus 1. J Invertebr Pathol 113:232–236CrossRef
34.
Zurück zum Zitat Valles SM, Porter SD, Choi MY, Oi DH (2013) Successful transmission of Solenopsis invicta virus 3 to Solenopsis invicta fire ant colonies in oil, sugar, and cricket bait formulations. J Invertebr Pathol 113:198–204CrossRef Valles SM, Porter SD, Choi MY, Oi DH (2013) Successful transmission of Solenopsis invicta virus 3 to Solenopsis invicta fire ant colonies in oil, sugar, and cricket bait formulations. J Invertebr Pathol 113:198–204CrossRef
35.
Zurück zum Zitat Valles SM, Shoemaker D, Wurm Y, Strong CA, Varone L, Becnel JJ, Shirk PD (2013) Discovery and molecular characterization of an ambisense densovirus from South American populations of Solenopsis invicta. Biol Cont 67:431–439CrossRef Valles SM, Shoemaker D, Wurm Y, Strong CA, Varone L, Becnel JJ, Shirk PD (2013) Discovery and molecular characterization of an ambisense densovirus from South American populations of Solenopsis invicta. Biol Cont 67:431–439CrossRef
36.
Zurück zum Zitat Valles SM, Oi DH (2014) Successful transmission of Solenopsis invicta virus 3 to field colonies of Solenopsis invicta (Hymenoptera: Formicidae). Fla Entomol 97:1244–1246CrossRef Valles SM, Oi DH (2014) Successful transmission of Solenopsis invicta virus 3 to field colonies of Solenopsis invicta (Hymenoptera: Formicidae). Fla Entomol 97:1244–1246CrossRef
37.
Zurück zum Zitat Valles SM, Porter SD, Firth AE (2014) Solenopsis invicta virus 3: pathogensis and stage specificity in red imported fire ants. Virology 461:66–71CrossRef Valles SM, Porter SD, Firth AE (2014) Solenopsis invicta virus 3: pathogensis and stage specificity in red imported fire ants. Virology 461:66–71CrossRef
38.
Zurück zum Zitat Valles SM, Chen Y, Firth A, Guerin DM, Herrero S, De Miranda J, Ryabov E (2017) ICTV Virus Taxonomy Profile: Iflaviridae. J Gen Virol 98:527–528CrossRef Valles SM, Chen Y, Firth A, Guerin DM, Herrero S, De Miranda J, Ryabov E (2017) ICTV Virus Taxonomy Profile: Iflaviridae. J Gen Virol 98:527–528CrossRef
39.
Zurück zum Zitat Valles SM, Chen Y, Firth AE, Guerin DM, Hashimoto Y, Herrero S, de Miranda JR, Ryabov E, Ictv Report C (2017) ICTV Virus Taxonomy Profile: Dicistroviridae. J Gen Virol 98:355–356CrossRef Valles SM, Chen Y, Firth AE, Guerin DM, Hashimoto Y, Herrero S, de Miranda JR, Ryabov E, Ictv Report C (2017) ICTV Virus Taxonomy Profile: Dicistroviridae. J Gen Virol 98:355–356CrossRef
40.
Zurück zum Zitat Valles SM, Porter SD, Calcaterra LA (2018) Prospecting for viral natural enemies of the fire ant Solenopsis invicta in Argentina. PLoS ONE 13:e0192377CrossRef Valles SM, Porter SD, Calcaterra LA (2018) Prospecting for viral natural enemies of the fire ant Solenopsis invicta in Argentina. PLoS ONE 13:e0192377CrossRef
41.
Zurück zum Zitat Valles SM, Porter SD (2019) Influence of temperature on the pathogenicity of Solenopsis invicta virus 3. J Invertebr Pathol 166:107217CrossRef Valles SM, Porter SD (2019) Influence of temperature on the pathogenicity of Solenopsis invicta virus 3. J Invertebr Pathol 166:107217CrossRef
42.
Zurück zum Zitat Valles SM, Rivers AR (2019) Nine new RNA viruses associated with the fire ant Solenopsis invicta from its native range. Virus Genes 55:368–380CrossRef Valles SM, Rivers AR (2019) Nine new RNA viruses associated with the fire ant Solenopsis invicta from its native range. Virus Genes 55:368–380CrossRef
Metadaten
Titel
Characterization of Solenopsis invicta virus 4, a polycipivirus infecting the red imported fire ant Solenopsis invicta
verfasst von
Steven M. Valles
David H. Oi
Jason B. Oliver
James J. Becnel
Publikationsdatum
13.09.2022
Verlag
Springer Vienna
Erschienen in
Archives of Virology / Ausgabe 12/2022
Print ISSN: 0304-8608
Elektronische ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-022-05587-4

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