Tahıl depoları ve çevresinin mikro faunasında Cardinium endosymbiontunun incelenmesi

Öz

Cardinium karasal ekosistem eklembacaklılarındaki üreme manipülatörü olarak bilinen endosimbiyotik bir bakteridir. Her ne kadar son dönemde çalışmalarla Cardinium konakçısı türler tespit edilse de, belki de daha az taksonomik grubun incelenmesinden dolayı prevalansı görece düşüktür. Bu çalışmada eklembacaklıların yayılışı için uygun koşullara sahip Türkiye’nin tahıl ambarlarındaki mikro-fauna örneklerinden Cardinium bakterisinin incelenmesi hedeflenmiştir. Bu amaçla tahıl ambarlarından ve çevresinden temin edilen Stratiolaelaps scimitus (Womersley, 1956) (Acari: Laelapidae), Entomobrya sp. (Collembola: Entomobryidae) ve Balaustium sp. (Acari: Actinotrichida) örneklerindeki Cardinium Clo primer seti kullanılarak incelenmiş ve Bemisia tabaci (Hemiptera: Aleyrodidae) endosimbiyontu ile mukayese edilmiştir. Sekans verilerine göre ambarlardan elde edilen ve yakın temasta bulunan S. scimitus ve Entomobrya sp.’teki Cardinium benzer homolojiye sahiptir. Bu veri bu iki takson arasında Cardinium’un yatay transferinin bir göstergesi olarak düşünülebilir. Ancak ne yazık ki elde edilen veri seti bunu kesin olarak kanıtlayamaz. Ayrıca Balaustium sp. ve B. tabaci endosimbiyontu Cardinium ise filogenetik olarak bunlardan uzaktır. Tahıl ambarı mikrofaunasında Cardinium endosimbiyontuna ilişkin ilk verilerin sunulduğu bu çalışmanın; özellikle küresel ısınma, azalan üretim ve artan gıda talebi nedeniyle baskı altındaki tarımsal üretimde zararlı türlerle mücadelede umut vaat eden üreme manipülatörü endosimbiyotik bakterilere yönelik çalışmalara katkı sunacağı düşünülmektedir. Ancak incelenen türlerin çeşitliliği, yayılışı ve habitatları içerisindeki ekolojik nişleri dikkate alındığında Cardinium prevalansının belirlenmesi için daha fazla çalışmaya ihtiyaç vardır.

Anahtar Kelimeler

• Balaustium
• Cardinium
• endosimbiyotik bakteri
• Entomobrya
• Stratiolaelaps scimitus

Investigation of Cardinium endosymbiont in the micro-fauna of granaries and surroundings

Öz

Cardinium is an endosymbiotic bacterium known as a reproductive manipulator in terrestrial ecosystem arthropods. Although Cardinium host species have been identified in recent studies, its prevalence is relatively low, perhaps due to the investigation of fewer taxonomic groups. This study was aimed to investigate Cardinium bacteria in micro-fauna samples in granaries of Turkey, which has suitable conditions for the distribution of arthropods. For this purpose, Stratiolaelaps scimitus (Womersley, 1956) (Acari: Laelapidae), Entomobrya sp. (Collembola: Entomobryidae), and Balaustium sp. (Acari: Actinotrichida) samples were investigated using the Cardinium Clo primer set and compared with the endosymbiont of Bemisia tabaci (Hemiptera: Aleyrodidae). It was determined that the Cardinium sequences from S. scimitus and Entomobrya sp., obtained from granaries and in close contact with each other, were quite similar and could be considered as a monophyletic group. This data can be considered as an indicator of horizontal transfer of Cardinium between these two taxa. However, Balaustium sp. and B. tabaci endosymbiont Cardinium are phylogenetically distant from them. It is thought that this study, which presents the first data on Cardinium endosymbiont in the granary microfauna, will contribute to studies on endosymbiotic bacteria, which are promising reproductive manipulators in the fight against harmful species, especially in agricultural production under pressure due to global warming, decreasing production, and increasing food demand. However, considering the diversity, distribution, and ecological niches of the studied species, more studies are needed to determine the prevalence of Cardinium.

Anahtar Kelimeler

• Balaustium
• Cardinium
• endosymbiotic bacteria
• Entomobrya
• Stratiolaelaps scimitus

Kaynakça

1. Aikawa T., Maehara N., Ichihara Y., Masuya H., Nakamura K., Anbutsu, H., 2022. Cytoplasmic incompatibility in the semivoltine longicorn beetle Acalolepta fraudatrix (Coleoptera: Cerambycidae) double infected with Wolbachia. Plos one, 17 (1), e0261928.
2. Aikawa T., Nikoh N., Anbutsu H., Togashi K., 2014. Prevalence of laterally transferred Wolbachia genes in Japanese pine sawyer, Monochamus alternatus (Coleoptera: Cerambycidae). Applied Entomology and Zoology, 49 (2), 337-346.
3. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J., 1990. Basic local alignment search tool. Journal of Molecular Biology, 215 (3), 403e410.
4. Baquero E., Jordana R., 2008. Redescription of Entomobrya quinquelineata Borner, 1901 (Collembola: Entomobryidae) and description of three new species. Zootaxa, 1821 (1), 1-12.
5. Bouchard C., Dibernardo A., Koffi J., Wood H., Leighton P. A., Lindsay L. R., 2019. Climate change and infectious diseases: the challenges: N increased risk of tick-borne diseases with climate and environmental changes. Canada Communicable Disease Report, 45 (4), 83.
6. Chaisiri K., McGarry J. W., Morand S., Makepeace B. L., 2015. Symbiosis in an overlooked microcosm: a systematic review of the bacterial flora of mites. Parasitology, 142 (9), 1152-1162.
7. Chang J., Masters A., Avery A., Werren J. H., 2010. A divergent Cardinium found in daddy long-legs (Arachnida: Opiliones). Journal of Invertebrate Pathology, 105 (3), 220-227.
8. Castaño-Meneses G., Palacios-Vargas J. G., Cutz-Pool L. Q., 2004. Feeding habits of Collembola and their ecological niche. Anales del Instituto de Biología. Serie Zoología, 75 (1), 135-142.

9. Doremus M. R., Stouthamer C. M., Kelly S. E., Schmitz-Esser S., Hunter M. S., 2020. Cardinium localization during its parasitoid wasp host’s development provides insights into cytoplasmic incompatibility. Frontiers in Microbiology, 11, 606399.
10. Doyle J. J., Doyle J. L., 1990. Isolation of plant DNA from fresh tissue. Focus, 12 (13), 39e40.
11. Folmer O., Black M., Hoeh W., Lutz R., Vrijenhoek R., 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3 (5), 294e299.
12. Gehrer L., Vorburger C., 2012. Parasitoids as vectors of facultative bacterial endosymbionts in aphids. Biological Letters, 8 (4), 613e615.
13. Gotoh T., Noda H., Ito S., 2007. Cardinium symbionts cause cytoplasmic incompatibility in spider mites. Heredity, 98 (1), 13-20.
14. Hall T. A., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symposium Series, 41 (41), 95e98.
15. Halliday R. B., 2001. Systematics and biology of the Australian species of Balaustium von heyden (Acari: Erythraeidae). Australian Journal of Entomology, 40, 326–330.
16. Hedges L. M., Brownlie J. C., O'Neill S. L., Johnson K. N., 2008. Wolbachia and virus protection in insects. Science, 322, 702.
17. Hiruta S. F., Shimano S., Shiba M., 2018. A preliminary molecular phylogeny shows Japanese and Austrian populations of the red mite Balaustium murorum (Acari: Trombidiformes: Erythraeidae) to be closely related. Experimental and Applied Acarology, 74 (3), 225-238.
18. Hosseini F. S., Shayanmehr M., Amiri Besheli B., 2016. Contribution to Collembola (Hexapoda, Entognatha) fauna from Golestan province, Iran. Journal of Insect Biodiversity and Systematics, 2 (3), 321-338.
19. Kageyama D., Narita S., Imamura T., Miyanoshita A., 2010. Detection and identification of Wolbachia endosymbionts from laboratory stocks of stored-product insect pests and their parasitoids. Journal of Stored Products Research, 46 (1), 13e19.
20. Kahrarian M., 2019. The checklist of Collembola (Hexapoda, Arthropoda) from west of Iran. Journal of Insect Biodiversity and Systematics, 5 (1), 33-46.
21. Kashkouli M., Fathipour Y., Mehrabadi M., 2021. The Crucial Role of the Endosymbiont Pantoea sp. in Morphology and Mating of the Pistachio Green Stink Bug, Brachynema germari (Hemiptera: Pentatomidae). Journal of Agricultural Science and Technology, 23 (1), 137-148.
22. Kimura M., 1980. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111-120.
23. Kumar S., Stecher G., Li M., Knyaz C., Tamura K., 2018. Mega X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35, 1547e1549.
24. Nakamura Y., Kawai S., Yukuhiro F., Ito S., Gotoh T., Kisimoto R., Yanase T., Matsumoto Y., Kageyama D., Noda H. 2009. Prevalence of Cardinium bacteria in planthoppers and spider mites and taxonomic revision of “Candidatus Cardinium hertigii” based on detection of a new Cardinium group from biting midges. Applied and Environmental Microbiology, 75 (21), 6757-6763.
25. Gomard Y., Flores O., Vittecoq M., Blanchon T., Toty C., Duron O., Mavingui P., Tortosa P., McCoy K. D. 2021. Changes in bacterial diversity, composition and interactions during the development of the seabird tick Ornithodoros maritimus (Argasidae). Microbial Ecology, 81 (3), 770-783.
26. Inci A., Yıldırım A., Düzlü O., Doganay M., Aksoy S., 2016. Tick-borne diseases in Turkey: A review based on one health perspective. PLOS Neglected Tropical Diseases, 10 (12), e0005021.
27. Ipekdal K., Kaya T., 2020. Screening stored wheat beetles for reproductive parasitic endosymbionts in central Turkey. Journal of Stored Products Research, 89, 101732.
28. Nakabachi A., Yamashita A., Toh H., Ishikawa H., Dunbar H. E., Moran N. A., Hattori M., 2006. The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science, 314, 267.
29. Navarro-Campos C., Wackers F. L., Pekas A., 2016. Impact of factitious foods and prey on the oviposition of the predatory mites Gaeolaelaps aculeifer and Stratiolaelaps scimitus (Acari: Laelapidae). Experimental and Applied Acarology, 70 (1), 69–78.
30. Noei J., Ersin F., Cakmak I., 2019. A new larval species of Balaustium (Acari: Actinotrichida: Erythraeidae) from Turkey. Turkish Journal of Zoology, 43 (1), 30-42.
31. Noei J., Asadollahzadeh S., Cakmak I., Hadizadeh A., 2017. A new larval species of Balaustium (Acari: Erythraeidae) from northern Iran and Turkey with a key to the genera of larval Balaustiinae and species of Balaustium. Systematic and Applied Acarology, 22 (12), 2218-2232.
32. Oliver K. M., Russell J. A., Moran N. A., Hunter M. S., 2003. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proceedings of the National Academy of Sciences, 100 (4), 1803-1807.
33. Özdikmen H., 2016. Dorcadionini of Turkey (Coleoptera: Cerambycidae). Journal of Natural History, 50 (37-38), 2399-2475.
34. Penz T., Schmitz-Esser S., Kelly S. E., Cass B. N., Müller A., Woyke T., Malfatti S. A., Hunter M. S., Horn M., 2012. Comparative genomics suggests an independent origin of cytoplasmic incompatibility in Cardinium hertigii. PLoS Genetics, 8 (10), e1003012.
35. Rondeau S., Giovenazzo P., Fournier V., 2018. Risk assessment and predation potential of Stratiolaelaps scimitus (Acari: Laelapidae) to control Varroa destructor (Acari: Varroidae) in honey bees. PloS one, 13 (12), e0208812.
36. Russell J.A., Moran N.A., 2006. Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proceedings of the Royal Society B: Biological Sciences, 273 (1586), 603e610.
37. Thompson J. D., Higgins D. G., Gibson T. J., 1994. ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22 (22), 4673e4680.
38. Telschow A., Hammerstein P., Werren J. H., 2005. The effect of Wolbachia versus genetic incompatibilities on reinforcement and speciation. Evolution, 59 (8), 1607-1619.
39. Tolley S. J. A., Nonacs P., Sapountzis P., 2019. Wolbachia horizontal transmission events in ants: what do we know and what can we learn? Frontiers in Microbiology, 10, 296.
40. Walter D. E., Campbell N. J. H., 2003. Exotic vs endemic biocontrol agents: would the real Stratiolaelaps miles (Berlese) (Acari: Mesostigmata: Laelapidae), please stand up? Biological Control, 26 (3), 253–269.
41. Werren J. H., Baldo L., Clark M. E., 2008. Wolbachia: master manipulators of invertebrate biology. Nature Reviews Microbiology, 6, 741–751.
42. Wright, E. M., Chambers, R. J. 1994. The biology of the predatory mite Hypoaspis miles (Acari: Laelapidae), a potential biological control agent of Bradysia paupera (Dipt.: Sciaridae). Entomophaga., 39 (2), 225–235.
43. Weeks A. R., Velten R., Stouthamer R., 2003. Incidence of a new sex-ratio-distorting endosymbiotic bacterium among arthropods. Proc. of the Royal Society B, 270, 1857e1865.
44. Yahyapour E., Vafaei-Shoushtari R., Shayanmehr M., Arbea J., 2018. A survey on Entomobryomorpha (Collembola) fauna in northern forests of Iran. Journal of Insect Biodiversity and Systematics, 4 (4), 307-316.
45. Zhao D., Hoffmann A. A., Zhang Z., Niu H., Guo H., 2018. Interactions between facultative symbionts Hamiltonella and Cardinium in Bemisia tabaci (Hemiptera: Aleyrodoidea): cooperation or conflict?. Journal of Economic Entomology, 111 (6), 2660-2666.
46. Zchori‐Fein E. I. N. A. T., Perlman S. J. 2004. Distribution of the bacterial symbiont Cardinium in arthropods. Molecular Ecology, 13 (7), 2009-2016.
47. Zug R., Hammerstein P., 2012. Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS One, 7, e38544.