Sex-ratio deviation and sex-ratio distorting bacteria detected by multiplex PCR in the predatory mite Amblyseius swirskii (Acari: Phytoseiidae)

Pournajafi, Haniyeh; Khanjani, Mohammad; Soltani, Jalal

doi:10.22073/pja.v12i2.77489

Sex-ratio deviation and sex-ratio distorting bacteria detected by multiplex PCR in the predatory mite Amblyseius swirskii (Acari: Phytoseiidae)

Document Type : Original Article

Authors

Haniyeh Pournajafi

Mohammad Khanjani

Jalal Soltani

Plant Protection Department, Bu-Ali Sina University, Hamedan, Iran

https://doi.org/10.22073/pja.v12i2.77489

Abstract

The symbiotic relationship between microorganisms and arthropods is very common in nature. Some of the symbiotic microorganisms alter the normal sex-determining mechanisms in arthropods, causing sex-ratio deviation, killing males, and eventually leading to asexual reproduction and the possibility of species extinction. In the biocontrol of agricultural pests, predatory mites of the family Phytoseiidae are of great importance. Here, regarding the observance of sex-ratio deviation in Amblyseius swirskii (Acari: Phytoseiidae), the presence of three reproductive manipulator bacteria, i.e. Wolbachia, Rickettsia, and Cardinium were investigated in adult mites. Firstly, investigation of the female: male ratio in commercial mites showed that the ratio was about 42:58. Thus, there was an obvious deviation from the normal sex ratio (50:50). Therefore, to determine the presence of sex-determining bacteria, the whole DNA was extracted from A. swirski mites, or alternatively the adult mites were used. Using specific primers of the above-mentioned bacteria for WSP, gtlA, and 16S rDNA genes, multiplex PCR was applied. The PCR products were sequenced, and the sequences were processed using MEGA 6 software, blasted, and checked within the NCBI gene bank. The results indicated the simultaneous presence of Wolbachia sp. and Rickettsia sp. in A. swirskii in all individuals tested, which meant 100% colonization. Therefore, the sex-ratio deviation in this species could be explained by the presence of sex-ratio distorting symbionts, although more studies are needed to prove this concept. Moreover, using individual adult mites directly in PCR tubes as the sources of raw DNA saved time and reduced the costs and labors in detecting the bacteria. Multiplex PCR also decreased the need for reagents, enzymes, DNA templates, etc., and saved a significant amount of time.

Keywords

Endosymbiosis

maternally inherited bacteria

multiple infections

reproductive parasitism

Rickettsia

Wolbachia

Arthurs, S., McKenzie, C.L., Chen, J., Dogramaci, M., Brennan, M., Houben, K. & Osborne, L. (2009) Evaluation of Neoseiulus cucumeris and Amblyseius swirskii (Acari: Phytoseiidae) as biological control agents of chilli thrips, Scirtothrips dorsalis (Thysanoptera: Thripidae) on pepper. Biological Control, 49: 91–96.

Baumann, P. (2005) Biology bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annual Review Microbiology, 59: 155–89. DOI: 10.1146/annurev.micro.59.030804.121041

Caldera, E.J., Poulsen, M., Suen, G. & Currie, C.R. (2009) Insect symbioses: a case study of past, present, and future fungus-growing ant research. Environomental Entomology, 38: 78–92. DOI: 10.1603/022.038.0110

Cedola, C. & Polack, A. (2017) First record of Amblyseius swirskii (Acari: Phytoseiidae) from Argentina. Revista de la Sociedad Entomológica Argentina, 70: 3–4. DOI: 10.1186/1741-7007-6-27

Duron, O., Binetruy, F., Noël, V., Cremaschi, J., McCoy, K.D., Arnathau, C., Plantard, O., Goolsby, J., Pérez de León, A.A., Heylen, D.J.A., Van Oosten, A.R., Gottlieb, Y., Baneth, G., Guglielmone, A.A., Estrada-Peña, A., Opara, M.N., Zenner, L., Vavre, F. & Chevillon, C. (2017) Evolutionary changes in symbiont community structure in ticks. Molecular Ecology, 26: 2905–2921. DOI: 10.1111/mec.14094

Duron, O., Bouchon, D., Boutin, S., Bellamy, L., Zhou, L.Q., Engelstadter, J. & Hurst, G.D. (2008) The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biology, 6: 27. DOI: 10.1186/1741-7007-6-27

Enigl, M. & Schausberger, P. (2007) Incidence of the endosymbionts Wolbachia, Cardinium and Spiroplasma in phytoseiid mites and associated prey. Experimental and Applied Acarology, 42: 75–85. DOI: 10.1007/s10493-007-9080-3

Engelstadter, J. & Hurst, G.D.D. (2009) The ecology and evolution of microbes that manipulate host reproduction. Annual Review of Ecology, Evolution, and Systematics, 40: 127–149. DOI: 10.1146 /annurev.ecolsys.110308.120206

EPPO (European and Mediterranean Plant Protection Organization) (2013) Commercially used biological control agents - Arachnida, Acarina. Available from: https://www.eppo.int/media/ uploaded_images/RESOURCES/eppo_standards/pm6/pm6-03(5)-2021-en.pdf (Accessed on October 2022)

Famah Sourassou, N., Hanna, R., Breeuwer, J.A., Negloh, K., de Moraes, G.J. & Sabelis, M.W. (2014) The endosymbionts Wolbachia and Cardinium and their effects in three populations of the predatory mite Neoseiulus paspalivorus. Experimental and Applied Acarology, 64: 207–21. DOI: 10.1007/s10493-014-9820-0

Gotoh, T., Noda, H. & Hong, X.Y. (2003) Wolbachia distribution and cytoplasmic incompatibility based on a survey of 42 spider mite species (Acari: Tetranychidae) in Japan. Heredity, 91: 208–216. DOI: 10.1038/sj.hdy.6800329

Gotoh, T., Noda, H. & Ito, S. (2007a) Cardinium symbionts cause cytoplasmic incompatibility in spider mites. Heredity, 98: 13–20.

Gotoh, T., Sugasawa, J., Noda, H. & Kitashima, Y. (2007b) Wolbachia-induced cytoplasmic incompatibility in Japanese populations of Tetranychus urticae (Acari: Tetranychidae). Experimental and Applied Acarology, 42: 1–16. DOI: 10.1007/s10493-007-9072-3

Haine, E.R. (2008) Symbiont-mediated protection. Proceedings of the Royal Society B: Biological Sciences, 275: 353–61. DOI: 10.1098/rspb.2007.1211

Hoffman, K. (Ed.) (2014) Insect molecular biology and ecology. 1st edition. CRC Press, 428 pp. DOI: 10.1201/b17876

Hoy, M.A. (2013) Insect molecular genetics: An introduction to principles and applications. Elsevier Inc. San Diego, California, USA, 838 pp.

Hoy, M.A. & Jeyaprakash, A. (2005) Microbial diversity in the predatory mite Metaseiulus occidentalis (Acari: Phytoseiidae) and its prey, Tetranychus urticae (Acari: Tetranychidae). Biological Control, 32: 427–441. DOI: 10.1016/j.biocontrol.2004.12.012

Kade, N., Gueye-Ndiaye, A., Duverney, C. & de Moraes, G.J. (2011) Phytoseiid mites (Acari: Phytoseiidae) from Senegal. Acarologia, 51: 133–138. DOI: 10.1051/acarologia/20112001

Liu, Y., Miao, H. & Hong, X.Y. (2006) Distribution of the endosymbiotic bacterium Cardinium in Chinese populations of the carmine spider mite Tetranychus cinnabarinus (Acari: Tetranych-idae). Journal of Applied Entomology, 130: 523–529.

Masoomi-Aladizgeh, F., Jabbari, L., Khayam Nekouei, R. & Aalami, A. (2016) A simple and rapid system for DNA and RNA isolation from diverse plants using handmade kit. Protocol Exchange, DOI: 10.21203/rs.2.1347/v2

Moran, N.A., McCutcheon, J.P. & Nakabachi, A. (2008) Genomics and evolution of heritable bacterial symbionts. Annual Review of Genetics, 42: 165–190.

Ros, V.I.D. & Breeuwer, J.A.J. (2009) The effects of, and interactions between, Cardinium and Wolbachia in the doubly infected spider mite Bryobia sarothamni. Heredity, 102: 413–422.

Ros, V.I.D., Fleming, V.M., Feil, E.J. & Breeuwer, J.A.J. (2012) Diversity and recombination in Wolbachia and Cardinium from Bryobia spider mites. BMC Microbiology, 12: S13. DOI: 10.118 6/1471-2180-12-S1-S13

Staudacher, H., Schimmel, B.C.J., Lamers, M.M., Wybouw, N., Groot, A.T. & Kant, M.R. (2017) Independent effects of a herbivore's bacterial symbionts on its performance and induced plant defences. International Journal of Oral Science, 18: 182. DOI: 10.3390/ijms18010182

Stouthamer, R., Breeuwer, J.A. & Hurst, G.D. (1999) Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annual Review Microbiology, 53: 71–102. DOI: 10.1146/annurev.micro. 53.1.71

Suh, E., Sim, C., Park, J.J. & Cho, K. (2015) Inter-population variation for Wolbachia induced reproductive incompatibility in the haplodiploid mite Tetranychus urticae. Experimental and Applied Acarology, 65: 55–71.

Swirski, E., Amitai, S. & Dorzia, N. (1967) Laboratory studies on the feeding, development and oviposition of the predacious mite Amblyseius rubini Swirski and Amitai and Amblyseius swirski Athias-Henriot (Acari: Phytoseiidae) on various kinds of food substances. Israel Journal of Agricultural Research, 17: 101–119.

Weeks, A.R., Velten, R. & Stouthamer, R. (2003) Incidence of a new sex-ratio-distorting endosym-biotic bacterium among arthropods. Proceedings of the Royal Society B: Biological Sciences, 270: 1857–1865. DOI: 10.1098/rspb.2003.2425

Weinert, L.A., Araujo-Jnr, E.V., Ahmed, M.Z. & Welch, J.J. (2015) The incidence of bacterial endosymbionts in terrestrial arthropods. Proceedings of the Royal Society of London, 282: 20150249. DOI: 10.1098/rspb.2015.0249

Weiss, B. & Aksoy, S. (2011) Microbiome influences on insect host vector competence. Trends Parasitology, 27: 514–522. DOI: 10.1016/j.pt.2011.05.001

Werren, J.H., Baldo, L. & Clark, M.E. (2008) Wolbachia: master manipulators of invertebrate biology. Nature Reviews Microbiology, 6: 741–751. DOI: 10.1038/nrmicro1969

Xie, R.R., Chen, X.L. & Hong, X.Y. (2011) Variable fitness and reproductive effects of Wolbachia infection in populations of the two-spotted spider mite Tetranychus urticae Koch in China. Applied Entomology and Zoology, 46: 95–102. DOI: 10.1007/s13355-010-0014-x

Xie, R.R., Sun, J.T., Xue, X.F. & Hong, X.Y. (2016) Cytoplasmic incompatibility and fitness benefits in the two-spotted spider mite Tetranychus urticae (red form) doubly infected with Wolbachia and Cardinium. Systematic and Applied Acarology, 21: 1161–1173. DOI: 10.11158/saa.21.9.1

Zchori-Fein, E. & Perlman, S.J. (2004) Distribution of the bacterial symbiont Cardinium in arthropods. Molecular Ecology, 13: 2009–2016. DOI: 10.1111/j.1365-294X.2004.02203.x

Zhang, Y.K., Chen, Y.T., Yang, K. & Hong, X.Y. (2016) A review of prevalence and phylogeny of the bacterial symbiont Cardinium in mites (subclass: Acari). Systematic and Applied Acarology, 21: 978–990. DOI: 10.11158/saa.21.7.11

Zhao, D.X., Chen, D.S., Ge, C., Gotoh, T. & Hong, X.Y. (2013a) Multiple Infections with Cardinium and two strains of Wolbachia in the spider mite Tetranychus phaselus Ehara: Revealing new forces driving the spread of Wolbachia. PLoS ONE, 8: e54964. DOI: 10.1371/journal.pone.0054 964

Zhao, D.X., Zhang, X.F. & Hong, X.Y. (2013b) Host-symbiont interactions in spider mite Tetranychus truncates doubly infected with Wolbachia and Cardinium. Environomental Entomology, 42: 445–452. DOI: 10.1603/EN12354

Zélé, F., Weill, M. & Magalhães, S. (2018) Identification of spider-mite species and their endosym-bionts using multiplex PCR. Experimental and Applied Acarology, 74: 123–138. DOI: 10.1007/ s10493-018-0224-4

Zhu, L.Y., Zhang, K.J., Zhang, Y.K., Ge, C., Gotoh, T. & Hong, X.Y. (2012) Wolbachia strengthens Cardinium-induced cytoplasmic incompatibility in the spider mite Tetranychus piercei McGregor. Current Microbiology, 65: 516–523. DOI: 10.1007/s00284-012-0190-8