Skip to main content
SpringerLink
Log in

Nine new RNA viruses associated with the fire ant Solenopsis invicta from its native range

  • Published:
Virus Genes Aims and scope Submit manuscript

Abstract

The red imported fire ant (Solenopsis invicta) escaped its natural enemies when it was introduced into North America in the 1930s from South America. US efforts have focused on discovery of natural enemies, like viruses, to provide sustainable control of the ant. Nine new virus genomes were sequenced from the invasive fire ant Solenopsis invicta using metagenomic RNA sequencing. The virus genomes were verified by Sanger sequencing and random amplification of cDNA ends reactions. In addition to the nine new virus genomes, the previously described Solenopsis viruses were also detected, including Solenopsis invicta virus 1 (SINV-1), SINV-2, SINV-3, SINV-4, SINV-5, and Solenopsis invicta densovirus. The virus sequences came from S. invicta workers, larvae, pupae, and dead workers taken from midden piles collected from across the ant’s native range in Formosa, Argentina. One of the new virus genomes (Solenopsis invicta virus 6) was also detected in populations of North American S. invicta. Phylogenetic analysis of the RNA dependent RNA polymerase, the entire nonstructural polyprotein, and genome characteristics were used to tentatively taxonomically place these new virus genome sequences; these include four new species of Dicistroviridae, one Polycipiviridae, one Iflaviridae, one Totiviridae, and two genome sequences that were too taxonomically divergent to be placed with certainty. The S. invicta virome is the best characterized from any ant species and includes 13 positive-sense, single-stranded RNA viruses (Solenopsis invicta virus 1 to Solenopsis invicta virus 13), one double-stranded RNA virus (Solenopsis midden virus), and one double-stranded DNA virus (Solenopsis invicta densovirus). These new additions to the S. invicta virome offer potentially new classical biological control agents for S. invicta.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Briano J, Calcaterra L, Varone L (2012) Fire ants (Solenopsis spp.) and their natural enemies in southern South America. Psyche. https://doi.org/10.1155/2012/198084

    Article  Google Scholar 

  4. Buchfink B, Xie C, Huson DH (2015) Fast and sensitive protein alignment using DIAMOND. Nat Methods 12:59–60

    Article  CAS  PubMed  Google Scholar 

  5. Caldera EJ, Ross KG, DeHeer CJ, Shoemaker D (2008) Putative native source of the invasive fire ant Solenopsis invicta in the USA. Biol Invasions 10:1457–1479

    Article  Google Scholar 

  6. Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Chen Y, Becnel JJ, Valles SM (2012) RNA viruses infecting pest insects. In: Vega F, Kaya HK (eds) Insect pathology. Elsevier, Amsterdam, pp 133–170

    Chapter  Google Scholar 

  8. Cooling M, Gruber MAM, Hoffmann BD, Sebastien A, Lester PJ (2017) A metatranscriptomic survey of the invasive yellow crazy ant, Anoplolepis gracilipes, identifies several potential viral and bacterial pathogens and mutualists. Insectes Soc 64:197–207

    Article  Google Scholar 

  9. Diaz-Munoz SL, Sanjuan R, West S (2017) Sociovirology: conflict, cooperation, and communication among viruses. Cell Host Microbe 22:437–441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Dolja VV, Boyko VP, Agranovsky AA, Koonin EV (1991) Phylogeny of capsid proteins of rod-shaped and filamentous RNA plant viruses: two families with distinct patterns of sequence and probably structure conservation. Virology 184:79–86

    Article  CAS  PubMed  Google Scholar 

  11. Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinform 5:1–19

    Article  CAS  Google Scholar 

  12. Ge X, Li Y, Yang X, Zhang H, Zhou P, Zhang Y, Shi Z (2012) Metagenomic analysis of viruses from bat fecal samples reveals many novel viruses in insectivorous bats in China. J Virol 86:4620–4630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Gruber MAM, Cooling M, Baty JW, Buckley K, Friedlander A, Quinn O, Russell J, Sebastien A, Lester PJ (2017) Single-stranded RNA viruses infecting the invasive Argentine ant, Linepithema humile. Sci Rep 7:3304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    Article  CAS  PubMed  Google Scholar 

  15. Huerta-Cepas J, Serra F, Bork P (2016) ETE 3: Reconstruction, analysis, and visualization of phylogenomic data. Mol Biol Evol 33:1635–1638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Huson DH, Mitra S, Ruscheweyh HJ, Weber N, Schuster SC (2011) Integrative analysis of environmental sequences using MEGAN4. Genome Res 21:1552–1560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Jang CJ, Jan E (2010) Modular domains of the Dicistroviridae intergenic internal ribosome entry site. RNA 16:1182–1195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Johansson H, Dhaygude K, Lindstrom S, Helantera H, Sundstrom L, Trontti K (2013) A metatranscriptomic approach to the identification of microbiota associated with the ant Formica exsecta. PLoS ONE 8:e79777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282

    CAS  PubMed  Google Scholar 

  20. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Koonin EV, Wolf YI, Nagasaki K, Dolja VV (2008) The big bang of picorna-like virus evolution antedates the radiation of eukaryotic supergroups. Nat Rev Microbiol 6:925–939

    Article  CAS  PubMed  Google Scholar 

  22. Koyama S, Urayama S, Ohmatsu T, Sassa Y, Sakai C, Takata M, Hayashi S, Nagai M, Furuya T, Moriyama H, Satoh T, Ono S, Mizutani T (2015) Identification, characterization and full-length sequence analysis of a novel dsRNA virus isolated from the arboreal ant Camponotus yamaokai. J Gen Virol 96:1930–1937

    Article  CAS  PubMed  Google Scholar 

  23. Koyama S, Sakai C, Thomas CE, Nunoura T, Urayama S (2016) A new member of the family Totiviridae associated with arboreal ants (Camponotus nipponicus). Arch Virol 161:2043–2045

    Article  CAS  PubMed  Google Scholar 

  24. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Lacey LA, Frutos R, Kaya HK, Vail P (2001) Insect pathogens as biological control agents: do they have a future? Biol Control 21:230–248

    Article  Google Scholar 

  26. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Le Gall O, Christian P, Fauquet CM, King AM, Knowles NJ, Nakashima N, Stanway G, Gorbalenya AE (2008) Picornavirales, a proposed order of positive-sense single-stranded RNA viruses with a pseudo-T = 3 virion architecture. Arch Virol 153:715–727

    Article  CAS  PubMed  Google Scholar 

  28. Le SQ, Gascuel O (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25:1307–1320

    Article  CAS  PubMed  Google Scholar 

  29. Lefort V, Longueville JE, Gascuel O (2017) SMS: Smart model selection in PhyML. Mol Biol Evol 34:2422–2424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Liu S, Vijayendran D, Bonning BC (2011) Next generation sequencing technologies for insect virus discovery. Viruses 3:1849–1869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. 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 6:233–244

    Article  PubMed  Google Scholar 

  32. Marchler-Bauer A, Bo Y, Han LY, He JE, Lanczycki CJ, Lu SN, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lu F, Marchler GH, Song JS, Thanki N, Wang ZX, Yamashita RA, Zhang DC, Zheng CJ, Geer LY, Bryant SH (2017) CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res 45:D200–D203

    Article  CAS  PubMed  Google Scholar 

  33. Oi DH, Valles SM (2009) Fire ant control with entomopathogens in the USA. In: Hajek AE, Glare TR, O’Callaghan M (eds) Use of microbes for control and eradication of invasive arthropods. Springer Science, New York, pp 237–258

    Chapter  Google Scholar 

  34. Oi DH, Valles SM, Porter SD, Cavanaugh C, White G, Henke J (2018) Introduction of fire ant biological control agents into the Coachella Valley of California. Fla Entomol, in press

  35. 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 98:2368–2378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Pereira RM (2003) Areawide suppression of fire ant populations in pastures: project update. J Agric Urban Entomol 20:123–130

    Google Scholar 

  37. Pfingsten JS, Costantino DA, Kieft JS (2007) Conservation and diversity among the three-dimensional folds of the Dicistroviridae intergenic region IRESes. J Mol Biol 370:856–869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Porter SD, Fowler HG, Mackay WP (1992) Fire ant mound densities in the United States and Brazil (Hymenoptera: Formicidae). J Econ Entomol 85:1154–1161

    Article  Google Scholar 

  39. Porter SD, Williams DF, Patterson RS, Fowler HG (1997) Intercontinental differences in the abundance of Solenopsis fire ants (Hymenoptera: Formicidae): escape from natural enemies? Environ Entomol 26:373–384

    Article  Google Scholar 

  40. Porter SD, Valles SM, Oi DH (2013) Host specificity and colony impacts of Solenopsis invicta virus 3. J Invertebr Pathol 114:1–6

    Article  PubMed  Google Scholar 

  41. 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). Florida Entomol 98:122–125

    Article  Google Scholar 

  42. Roberts JMK, Anderson DL, Durr PA (2018) Metagenomic analysis of Varroa-free Australian honey bees (Apis mellifera) shows a diverse Picornavirales virome. J Gen Virol 99:818–826

    Article  CAS  PubMed  Google Scholar 

  43. Shi M, Lin XD, Tian JH, Chen LJ, Chen X, Li CX, Qin XC, Li J, Cao JP, Eden JS, Buchmann J, Wang W, Xu J, Holmes EC, Zhang YZ (2016) Redefining the invertebrate RNA virosphere. Nature 540(7634):539

    Article  CAS  PubMed  Google Scholar 

  44. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Tschinkel WR (2006) The fire ants. The Belknap Press of Harvard University Press, Cambridge

    Google Scholar 

  46. 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 328:151–157

    Article  CAS  PubMed  Google Scholar 

  47. 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 365:457–463

    Article  CAS  PubMed  Google Scholar 

  48. Valles SM, Strong CA, Hunter WB, Dang PM, Pereira RM, Oi DH, Williams DF (2008) Expressed sequence tags from the red imported fire ant, Solenopsis invicta: annotation and utilization for discovery of viruses. J Invertebr Pathol 99:74–81

    Article  CAS  PubMed  Google Scholar 

  49. 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 388:354–361

    Article  CAS  PubMed  Google Scholar 

  50. Valles SM (2012) Positive-strand RNA viruses infecting the red imported fire ant, Solenopsis invicta. Psyche. https://doi.org/10.1155/2012/821591

    Article  Google Scholar 

  51. 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 113:198–204

    Article  PubMed  Google Scholar 

  52. 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 Control 67:431–439

    Article  Google Scholar 

  53. Valles SM, Oi DH (2014) Successful transmission of Solenopsis invicta virus 3 to field colonies of Solenopsis invicta (Hymenoptera: Formicidae). Florida Entomol 97:1244–1246

    Article  Google Scholar 

  54. Valles SM, Porter SD, Firth AE (2014) Solenopsis invicta virus 3: pathogensis and stage specificity in red imported fire ants. Virology 461:66–71

    Article  CAS  Google Scholar 

  55. Valles SM, Porter SD (2015) Dose response of red imported fire ant colonies to Solenopsis invicta virus 3. Arch Virol 160:2407–2413

    Article  CAS  PubMed  Google Scholar 

  56. Valles SM, Oi D, Becnel JJ, Wetterer JK, Lapolla JS, Firth AE (2016) Isolation and characterization of Nylanderia fulva virus 1, a positive-sense, single-stranded RNA virus infecting the tawny crazy ant, Nylanderia fulva. Virology 496:244–254

    Article  CAS  PubMed  Google Scholar 

  57. Valles SM, Chen Y, Firth A, Guerin DM, Herrero S, De Miranda J, Ryabov E (2017) ICTV virus taxonomy profile: Iflaviridae. J Gen Virol 98:527–528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. 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 98:355–356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Valles SM, Porter SD, Calcaterra LA (2018) Prospecting for viral natural enemies of the fire ant Solenopsis invicta in Argentina. PLoS ONE 13:e0192377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Viljakainen L, Holmberg I, Abril S, Jurvansuu J (2018) Viruses of invasive Argentine ants from the European Main supercolony: characterization, interactions and evolution. J Gen Virol 99:1129–1140

    Article  CAS  PubMed  Google Scholar 

  61. Vinson SB, Greenberg L (1986) The biology, physiology, and ecology of imported fire ants. In: Vinson SB (ed) Economic impact and control of social insects. Praeger Scientific, New York, pp 193–226

    Google Scholar 

  62. Vinson SB, Sorensen AA (1986) Imported fire ants: life history and impact. Texas A&M University, College Station

    Google Scholar 

  63. Wickner RB, Ghabrial SA, Nibert M, Patterson JL, Wang CC (2012) Totiviridae. In: King AM, Adams AL, Carsten EB, Lefkowitz EJ (eds) Virus taxonomy, ninth report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, Amsterdam, pp 639–650

    Google Scholar 

  64. Yang CC, Yu YC, Valles SM, Oi DH, Chen YC, Shoemaker D, Wu WJ, Shih CJ (2010) Loss of microbial (pathogen) infections associated with recent invasions of the red imported fire ant Solenopsis invicta. Biol Invas 12:3307–3318

    Article  Google Scholar 

  65. Yang YT, Nai YS, Lee SJ, Lee MR, Kim S, Kim JS (2016) A novel picorna-like virus, Riptortus pedestris virus-1 (RiPV-1), found in the bean bug, R. pedestris, after fungal infection. J Invertebr Pathol 141:57–65

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The use of trade, firm, and corporation names in this publication are for the information and convenience of the reader. Such use does not constitute an official endorsement or approval by the United States Department of Agriculture or the Agricultural Research Service of any product or service to the exclusion of others that may be suitable. We thank S.D. Porter, M. Guala, and L. Calcattera for ant collections. Ant collections were carried out under collecting permits issued by Subsecretaria de Recursos Naturales, Ordenamiento y Calidad Ambiental of the province of Formosa (Nota No. 108/13). Export permits were issued by the Secretaría de Ambiente y Desarrollo Sustentable (No. 24767) and the Servicio Nacional de Sanidad y Calidad Agroalimentaria (Nota DNPV No 747) of Argentina.

Author information

Authors and Affiliations

  1. Center for Medical, Agricultural and Veterinary Entomology, USDA-ARS, Gainesville, FL, USA

    Steven M. Valles

  2. Genomics and Bioinformatics Research Unit, USDA-ARS, Gainesville, FL, USA

    Adam R. Rivers

Authors
  1. Steven M. Valles
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Adam R. Rivers
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Steven M. Valles.

Ethics declarations

Conflict of interest

Steven Valles and Adam Rivers declare that they have no conflicts of interest.

Ethical approval

The research reported here did not involve any studies on human or vertebrate subjects.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Edited by Dr. A. Lorena Passarelli.

Electronic supplementary material

Below is the link to the electronic supplementary material.

11262_2019_1652_MOESM1_ESM.tiff

Supplementary material 1—Supplementary Fig. 1. Phylogenetic analysis of the RdRp region of new S. invicta virus genomes and those of the picorna-like superfamily identified by Koonin et al. [21]. Key to virus abbreviations and accession numbers are also found in the Koonin et al. [21] work(TIFF 1100 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Valles, S.M., Rivers, A.R. Nine new RNA viruses associated with the fire ant Solenopsis invicta from its native range. Virus Genes 55, 368–380 (2019). https://doi.org/10.1007/s11262-019-01652-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11262-019-01652-4

Keywords

Search

Navigation