Tác động của nhiễm Wolbachia đến các đặc tính liên quan đến khả năng sinh sản trong Drosophila melanogaster

Symbiosis - Tập 83 - Trang 163-172 - 2021
Svitlana V. Serga1,2, Oleksandr M. Maistrenko1,3, Nataliya P. Matiytsiv4, Alexander M. Vaiserman5, Iryna A. Kozeretska2
1Taras Shevchenko National University of Kyiv, Kyiv, Ukraine
2National Antarctic Scientific Center of Ukraine, Kyiv, Ukraine
3European Molecular Biology Laboratory, Structural and Computational Biology Unit, Heidelberg, Germany
4Department of Genetics and Biotechnology, Ivan Franko National University of Lviv, Lviv, Ukraine
5D.F. Chebotarev Institute of Gerontology, NAMS, Kyiv, Ukraine

Tóm tắt

Wolbachia là một ký sinh trùng nội bào ảnh hưởng đến một số lượng lớn các loài chân đốt, đảm bảo sự thành công trong các quần thể bằng cách ảnh hưởng đến sự sinh sản của vật chủ. Chủng wMel trong Drosophila melanogaster không gây ra những biến đổi mạnh mẽ đối với sự sinh sản giới tính. Do đó, chưa rõ làm thế nào mà tỷ lệ nhiễm khuẩn cao của vi khuẩn trong các quần thể của loài này được duy trì. Chủng wMel được phân loại thành hai nhóm kiểu gen - wMel và wMelCS. Kiểu gen wMel phổ biến trong các quần thể, trong khi wMelCS thì hiếm gặp. Trong nghiên cứu này, chúng tôi đã phân tích các đặc tính liên quan đến khả năng sinh sản trong các dòng isofemale từ quần thể tự nhiên độc nhất ở Uman (Ukraina Trung), nơi mà chúng tôi nhận thấy sự bảo tồn của kiểu gen wMelCS hiếm gặp mặc dù có sự biến động của tỷ lệ nhiễm khuẩn giữa các năm. Chúng tôi đã phân tích những tác động của kiểu gen Wolbachia và nền tảng di truyền của vật chủ đến các tham số sức sống quan trọng như độ nhạy cảm với lạnh và căng thẳng oxy hóa, khả năng sinh sản của con cái và tuổi thọ. Chúng tôi phát hiện ra rằng, trong quần thể được nghiên cứu, Wolbachia chỉ có tác động đến các đặc tính khả năng sinh sản trong một số kiểu gen Drosophila nhất định. Những tác động tích cực được thể hiện trong sự thay đổi đối với khả năng sinh sản, nhưng phải đánh đổi bằng tuổi thọ giảm và khả năng chống lại căng thẳng. Dựa trên những phát hiện này, chúng tôi kết luận rằng tác động của vi khuẩn lên khả năng sinh sản và các đặc tính liên quan đến căng thẳng là tùy thuộc vào ngữ cảnh và bị điều chỉnh bởi kiểu gen của vật chủ, ít nhất trong các dòng được thành lập từ quần thể ở Uman.

Từ khóa

#Wolbachia #Drosophila melanogaster #kiểu gen #khả năng sinh sản #tuổi thọ #áp lực môi trường

Tài liệu tham khảo

Adler MI, Cassidy EJ, Fricke C, Bonduriansky R (2013) The lifespan-reproduction trade-off under dietary restriction is sex-specific and context-dependent. Exp Gerontol 48:539–548. https://doi.org/10.1016/j.exger.2013.03.007 Albertson R, Tan V, Leads RR, Reyes M, Sullivan W, Casper-Lindley C (2013) Mapping Wolbachia distributions in the adult Drosophila brain. Cell Microbiol 15:1527–1544. https://doi.org/10.1111/cmi.12136 Alexandrov ID, Alexandrova MV, Goryacheva II, Rochina NV, Shaikevich EV, Zakharov IA (2007) Removing endosymbiotic Wolbachia specifically decreases lifespan of females and competitiveness in a laboratory strain of Drosophila melanogaster. Russ J Genet 43:1147–1152. https://doi.org/10.1134/S1022795407100080 Aljanabi S, Martinez I (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR- based techniques. Nucleic Acids Res 25:4692–4693. https://doi.org/10.1093/nar/25.22.4692 Braig HR, Guzman H, Tesh RB, O’Neill SL (1994) Replacement of the natural Wolbachia symbiont of Drosophila simulans with a mosquito counterpart. Nature 367:453–455. https://doi.org/10.1038/367453a0 Brennan LJ, Haukedal JA, Earle JC, Keddie B, Harris HL (2012) Disruption of redox homeostasis leads to oxidative DNA damage in spermatocytes of Wolbachia-infected Drosophila simulans. Insect Mol Biol 21:510–520. https://doi.org/10.1111/j.1365-2583.2012.01155.x Brownlie JC, Cass BN, Riegler M, Witsenburg JJ, Iturbe-Ormaetxe I, McGraw EA, O'Neill SL (2009) Evidence for metabolic provisioning by a common invertebrate Endosymbiont, Wolbachia pipientis, during periods of nutritional stress. PLoS Pathog 5:e1000368. https://doi.org/10.1371/journal.ppat.1000368 Bykov RA, Yudina MA, Gruntenko NE et al (2019) Prevalence and genetic diversity of Wolbachia endosymbiont and mtDNA in Palearctic populations of Drosophila melanogaster. BMC Evol Biol 19:48. https://doi.org/10.1186/s12862-019-1372-9 Capobianco F, Nandkumar S, Parker JD (2018) Wolbachia affects survival to different oxidative stressors dependent upon the genetic background in Drosophila melanogaster. Physiol Entomol 43:239–244. https://doi.org/10.1111/phen.12252 Charlat S, Ballard JWO, Merçot H (2004) What maintains noncytoplasmic incompatibility inducing Wolbachia in their hosts: a case study from a natural Drosophila yakuba population. J Evol Biol 17:322–330. https://doi.org/10.1046/j.1420-9101.2003.00676.x Chrostek E, Marialva MSP, Esteves SS, Weinert LA, Martinez J, Jiggins FM, Teixeira L (2013) Wolbachia variants induce differential protection to viruses in Drosophila melanogaster: a phenotypic and Phylogenomic analysis. PLoS Genet 9:e1003896. https://doi.org/10.1371/journal.pgen.1003896 Corbin C, Heyworth ER, Ferrari J, Hurst GDD (2017) Heritable symbionts in a world of varying temperature. Heredity (Edinb) 118:10–20 Duron O, Bouchon D, Boutin S, Bellamy L, Zhou L, Engelstädter J, Hurst GD (2008) The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol 6:27. https://doi.org/10.1186/1741-7007-6-27 Dyer KA, Jaenike J (2004) Evolutionarily stable infection by a male-killing endosymbiont in Drosophila innubila: molecular evidence from the host and parasite genomes. Genetics 168:1443–1455. https://doi.org/10.1534/genetics.104.027854 Fisher RA (1922) On the interpretation of χ 2 from contingency tables, and the calculation of P. J R Stat Soc 85:87. https://doi.org/10.2307/2340521 Flatt T (2011) Survival costs of reproduction in Drosophila. Exp Gerontol 46:369–375. https://doi.org/10.1016/j.exger.2010.10.008 Fowler K, Partridge L (1989) A cost of mating in female fruitflies. Nature 338:760–761. https://doi.org/10.1038/338760a0 Fry AJ, Palmer MR, Rand DM (2004) Variable fitness effects of Wolbachia infection in Drosophila melanogaster. Heredity (Edinb) 93:379–389. https://doi.org/10.1038/sj.hdy.6800514 Gruntenko NЕ, Ilinsky YY, Adonyeva NV, Burdina EV, Bykov RA, Menshanov PN, Rauschenbach IY (2017) Various Wolbachia genotypes differently influence host Drosophila dopamine metabolism and survival under heat stress conditions. BMC Evol Biol 17:252. https://doi.org/10.1186/s12862-017-1104-y Gundel PE, Rudgers JA, Ghersa CM (2011) Incorporating the process of vertical transmission into understanding of host-symbiont dynamics. Oikos 120:1121–1128. https://doi.org/10.1111/j.1600-0706.2011.19299.x Hamm CA, Begun DJ, Vo A, Smith CCR, Saelao P, Shaver AO, Jaenike J, Turelli M (2014) Wolbachia do not live by reproductive manipulation alone: infection polymorphism in Drosophila suzukii and D. subpulchrella. Mol Ecol 23:4871–4885. https://doi.org/10.1111/mec.12901 Harcombe W, Hoffmann AA (2004) Wolbachia effects in Drosophila melanogaster: in search of fitness benefits. J Invertebr Pathol 87:45–50. https://doi.org/10.1016/J.JIP.2004.07.003 Hedges LM, Brownlie JC, O’Neill SL, Johnson KN (2008) Wolbachia and virus protection in insects. Science 322:702. https://doi.org/10.1126/science.1162418 Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH (2008) How many species are infected with Wolbachia? — a statistical analysis of current data. FEMS Microbiol Lett 281:215–220. https://doi.org/10.1111/j.1574-6968.2008.01110.x Hoffmann AA (1988) Partial cytoplasmic incompatibility between two Australian populations of Drosophila melanogaster. Entomol Exp Appl 48:61–67. https://doi.org/10.1111/j.1570-7458.1988.tb02299.x Hoffmann AA, Clancy D, Duncan J (1996) Naturally-occurring Wolbachia infection in Drosophila simulans that does not cause cytoplasmic incompatibility. Heredity (Edinb) 76:1–8. https://doi.org/10.1038/hdy.1996.1 Hoffmann AA, Clancy DJ, Merton E (1994) Cytoplasmic incompatibility in Australian populations of Drosophila melanogaster. Genetics 136 Ilinsky YY, Zakharov IK (2007) The endosymbiont Wolbachia in Eurasian populations of Drosophila melanogaster. Russ J Genet 43:748–756. https://doi.org/10.1134/S102279540707006X Jünger MA, Rintelen F, Stocker H et al (2003) The drosophila forkhead transcription factor FOXO mediates the reduction in cell number associated with reduced insulin signaling. J Biol 2:20. https://doi.org/10.1186/1475-4924-2-20 Kriesner P, Conner WR, Weeks AR, Turelli M, Hoffmann AA (2016) Persistence of a Wolbachia infection frequency cline in Drosophila melanogaster and the possible role of reproductive dormancy. Evolution (N Y) 70:979–997. https://doi.org/10.1111/evo.12923 Kriesner P, Hoffmann AA, Lee SF, Turelli M, Weeks AR (2013) Rapid sequential spread of two Wolbachia variants in Drosophila simulans. PLoS Pathog 9:e1003607. https://doi.org/10.1371/journal.ppat.1003607 Layton EM, On J, Perlmutter JI, Bordenstein SR, Shropshire JD (2019) Paternal grandmother age affects the strength of Wolbachia-induced cytoplasmic incompatibility in Drosophila melanogaster MBio 10:. https://doi.org/10.1128/mBio.01879-19 Li YY, Floate KD, Fields PG, Pang BP (2014) Review of treatment methods to remove Wolbachia bacteria from arthropods. Symbiosis 62:1–15 Libert S, Chao Y, Chu X, Pletcher SD (2006) Trade-offs between longevity and pathogen resistance in Drosophila melanogaster are mediated by NF?B signaling. Aging Cell 5:533–543. https://doi.org/10.1111/j.1474-9726.2006.00251.x Maistrenko OM, Serga SV, Vaiserman AM, Kozeretska IA (2016) Longevity-modulating effects of symbiosis: insights from Drosophila–Wolbachia interaction. Biogerontology 17:785–803. https://doi.org/10.1007/s10522-016-9653-9 Maistrenko OM, Serga S V, Vaiserman AM, Kozeretska IA (2015) Effect of Wolbachia infection on aging and longevity-associated genes in Drosophila. In: Life Extension Martinez J, Ok S, Smith S, Snoeck K, Day JP, Jiggins FM (2015) Should Symbionts be Nice or selfish? Antiviral effects of Wolbachia are costly but reproductive parasitism is not. PLoS Pathog 11:e1005021. https://doi.org/10.1371/journal.ppat.1005021 McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Lošo T, Douglas AE, Dubilier N, Eberl G, Fukami T, Gilbert SF, Hentschel U, King N, Kjelleberg S, Knoll AH, Kremer N, Mazmanian SK, Metcalf JL, Nealson K, Pierce NE, Rawls JF, Reid A, Ruby EG, Rumpho M, Sanders JG, Tautz D, Wernegreen JJ (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci U S A 110:3229–3236. https://doi.org/10.1073/pnas.1218525110 Min KT, Benzer S (1997) Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc Natl Acad Sci U S A 94:10792–10796. https://doi.org/10.1073/pnas.94.20.10792 Nunes MDS, Nolte V, Schlötterer C (2008) Nonrandom Wolbachia infection status of Drosophila melanogaster strains with different mtDNA haplotypes. Mol Biol Evol 25:2493–2498. https://doi.org/10.1093/molbev/msn199 O’Neill SL (1998) Influential passengers: inherited microorganisms and arthropod reproduction. Q Rev Biol 73:514–515. https://doi.org/10.1086/420470 O’Neill SL, Giordano R, Colbert AM et al (1992) 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc Natl Acad Sci U S A 89:2699–2702. https://doi.org/10.1073/PNAS.89.7.2699 O’Shea KL, Singh ND (2015) Tetracycline-exposed Drosophila melanogaster males produce fewer offspring but a relative excess of sons. Ecol Evol 5:3130–3139. https://doi.org/10.1002/ece3.1535 Partridge L, Harvey PH (1988) The ecological context of life history evolution. Science (80- ) 241:1449–1455. https://doi.org/10.1126/science.241.4872.1449 Piper MDW, Partridge L (2018) Drosophila as a model for ageing. Biochim Biophys Acta - Mol Basis Dis 1864:2707–2717 R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.r-project.org. Accessed 11 Feb 2017 Riegler M, Sidhu M, Miller WJ, O’Neill SL (2005) Evidence for a global Wolbachia replacement in Drosophila melanogaster. Curr Biol 15:1428–1433. https://doi.org/10.1016/J.CUB.2005.06.069 Roshina NV, Symonenko AV, Krementsova AV et al (2018) Drosophila melanogaster inhabiting northern regions of European Russia are infected with Wolbachia which adversely affects their life span. Vavilov J Genet Breed 22:568–573. https://doi.org/10.18699/VJ18.396 Ross PA, Wiwatanaratanabutr I, Axford JK, White VL, Endersby-Harshman NM, Hoffmann AA (2017) Wolbachia infections in Aedes aegypti differ markedly in their response to cyclical heat stress. PLoS Pathog 13:e1006006. https://doi.org/10.1371/journal.ppat.1006006 Serga S, Maistrenko O, Rozhok A, Mousseau T, Kozeretska I (2014) Fecundity as one of possible factors contributing to the dominance of the wMel genotype of Wolbachia in natural populations of Drosophila melanogaster. Symbiosis 63:11–17. https://doi.org/10.1007/s13199-014-0283-1 Serga S V., Kovalenko PA, Gora N V., et al (2019) Low prevalence of wolbachia infection in ukrainian populations of drosophila. Mikrobiol Zh 81:84–89. https://doi.org/10.15407/microbiolj81.02.084 Serga SV, Kozeretskaia IA (2013) The puzzle of Wolbachia spreading out through natural populations of Drosophila melanogaster. Zh Obshch Biol 74:99–111 Solignac M, Vautrin D, Des FR-C rendus de l’Académie, 1994 U (1994) Widespread occurence of the proteobacteria Wolbachia and partial cytoplasmic incompatibility in Drosophila melanogaster. Elsevier Teixeira L, Ferreira Á, Ashburner M (2008) The bacterial Symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 6:e1000002. https://doi.org/10.1371/journal.pbio.1000002 Truitt AM, Kapun M, Kaur R, Miller WJ (2019) Wolbachia modifies thermal preference in <scp> Drosophila melanogaster </scp>. Environ Microbiol 21:3259–3268. https://doi.org/10.1111/1462-2920.14347 Tukey JW (1949) Comparing individual means in the analysis of variance. Biometrics 5:99–114. https://doi.org/10.2307/3001913 Turelli M, Hoffmann AA (1995) Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations. Genetics 140 Turelli M, Hoffmann AA (1991) Rapid spread of an inherited incompatibility factor in California Drosophila. Nature 353:440–442. https://doi.org/10.1038/353440a0 Veneti Z, Zabalou S, Papafotiou G, Paraskevopoulos C, Pattas S, Livadaras I, Markakis G, Herren JK, Jaenike J, Bourtzis K (2012) Loss of reproductive parasitism following transfer of male-killing Wolbachia to Drosophila melanogaster and Drosophila simulans. Heredity (Edinb) 109:306–312. https://doi.org/10.1038/hdy.2012.43 Verspoor RL, Haddrill PR (2011) Genetic diversity, population structure and Wolbachia infection status in a worldwide sample of Drosophila melanogaster and D. simulans populations. PLoS One 6:e26318. https://doi.org/10.1371/journal.pone.0026318 Wang L, Zhou C, He Z, Wang ZG, Wang JL, Wang YF (2012) Wolbachia infection decreased the resistance of Drosophila to Lead. PLoS One 7:e32643. https://doi.org/10.1371/journal.pone.0032643 Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751. https://doi.org/10.1038/nrmicro1969 Wong ZS, Brownlie JC, Johnson KN (2015) Oxidative stress correlates with Wolbachia-mediated antiviral protection in Wolbachia-Drosophila associations. Appl Environ Microbiol 81:3001–3005. https://doi.org/10.1128/AEM.03847-14 Yamada R, Floate KD, Riegler M, O’Neill SL (2007) Male development time influences the strength of wolbachia-induced cytoplasmic incompatibility expression in Drosophila melanogaster. Genetics 177:801–808. https://doi.org/10.1534/genetics.106.068486 Zhou W, Rousset F, O’Neil S (1998) Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proceedings Biol Sci 265:509–515. https://doi.org/10.1098/rspb.1998.0324