Extensive duplication of the Wolbachia DNA in chromosome four of Drosophila ananassae
详细信息 查看全文
- 作者：Lisa Klasson (82)
Nikhil Kumar (83)
Robin Bromley (83)
Karsten Sieber (83)
Melissa Flowers (83)
Sandra H Ott (83)
Luke J Tallon (83)
Siv G E Andersson (82)
Julie C Dunning Hotopp (83) (84)
82. Department of Cell and Molecular Biology ; Molecular Evolution ; Uppsala University ; Uppsala ; Sweden
83. Institute for Genome Sciences ; University of Maryland School of Medicine ; Baltimore ; MD ; 21201 ; USA
84. Department of Microbiology & Immunology ; University of Maryland School of Medicine ; Baltimore ; MD ; 21201 ; USA - 关键词：Drosophila ananassae ; Wolbachia ; Lateral gene transfer ; Horizontal gene transfer ; Symbiosis ; Underreplication ; Heterochromatin
- 刊名：BMC Genomics
- 出版年：2014
- 出版时间：December 2014
- 年：2014
- 卷：15
- 期：1
- 全文大小：9,534 KB
- 参考文献：1. Hazkani-Covo, E, Zeller, RM, Martin, W (2010) Molecular poltergeists: mitochondrial DNA copies (numts) in sequenced nuclear genomes. PLoS Genet 6: pp. e1000834 CrossRef
2. Stouthamer, R, Breeuwer, JA, Hurst, GD (1999) Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol 53: pp. 71-102 CrossRef
3. Werren, JH (1997) Biology of Wolbachia. Annu Rev Entomol 42: pp. 587-609 CrossRef
4. 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: pp. e38544 CrossRef
5. Fast, EM, Toomey, ME, Panaram, K, Desjardins, D, Kolaczyk, ED, Frydman, HM (2011) Wolbachia enhance Drosophila stem cell proliferation and target the germline stem cell niche. Science 334: pp. 990-992 CrossRef
6. Dunning Hotopp, JC (2011) Horizontal gene transfer between bacteria and animals. Trends Genet 27: pp. 157-163 CrossRef
7. Robinson, KM, Sieber, KB, Dunning Hotopp, JC (2013) A review of bacteria-animal lateral gene transfer may inform our understanding of diseases like cancer. PLoS Genet 9: pp. e1003877 CrossRef
8. Kondo, N, Nikoh, N, Ijichi, N, Shimada, M, Fukatsu, T (2002) Genome fragment of Wolbachia endosymbiont transferred to X chromosome of host insect. Proc Natl Acad Sci U S A 99: pp. 14280-14285 CrossRef
9. Nikoh, N, Tanaka, K, Shibata, F, Kondo, N, Hizume, M, Shimada, M, Fukatsu, T (2008) Wolbachia genome integrated in an insect chromosome: evolution and fate of laterally transferred endosymbiont genes. Genome Res 18: pp. 272-280 CrossRef
10. Dunning Hotopp, JC, Clark, ME, Oliveira, DC, Foster, JM, Fischer, P, Torres, MC, Giebel, JD, Kumar, N, Ishmael, N, Wang, S, Ingram, J, Nene, RV, Shepard, J, Tomkins, J, Richards, S, Spiro, DJ, Ghedin, E, Slatko, BE, Tettelin, H, Werren, JH (2007) Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317: pp. 1753-1756 CrossRef
11. Fenn, K, Conlon, C, Jones, M, Quail, MA, Holroyd, NE, Parkhill, J, Blaxter, M (2006) Phylogenetic relationships of the Wolbachia of nematodes and arthropods. PLoS Pathog 2: pp. e94 CrossRef
12. Nikoh, N, McCutcheon, JP, Kudo, T, Miyagishima, SY, Moran, NA, Nakabachi, A (2010) Bacterial genes in the aphid genome: absence of functional gene transfer from Buchnera to its host. PLoS Genet 6: pp. e1000827 CrossRef
13. Werren, JH, Richards, S, Desjardins, CA, Niehuis, O, Gadau, J, Colbourne, JK, Beukeboom, LW, Desplan, C, Elsik, CG, Grimmelikhuijzen, CJ, Kitts, P, Lynch, JA, Murphy, T, Oliveira, DC, Smith, CD, van de Zande, L, Worley, KC, Zdobnov, EM, Aerts, M, Albert, S, Anaya, VH, Anzola, JM, Barchuk, AR, Behura, SK, Bera, AN, Berenbaum, MR, Bertossa, RC, Bitondi, MM, Bordenstein, SR, Bork, P (2010) Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327: pp. 343-348 CrossRef
14. Aikawa, T, Anbutsu, H, Nikoh, N, Kikuchi, T, Shibata, F, Fukatsu, T (2009) Longicorn beetle that vectors pinewood nematode carries many Wolbachia genes on an autosome. Proc Biol Sci 276: pp. 3791-3798 CrossRef
15. Brelsfoard, C, Tsiamis, G, Falchetto, M, Gomulski, LM, Telleria, E, Alam, U, Doudoumis, V, Scolari, F, Benoit, JB, Swain, M, Takac, P, Malacrida, AR, Bourtzis, K, Aksoy, S (2014) Presence of extensive Wolbachia symbiont insertions discovered in the genome of its host Glossina morsitans morsitans. PLoS Negl Trop Dis 8: pp. e2728 CrossRef
16. McNulty, SN, Foster, JM, Mitreva, M, Dunning Hotopp, JC, Martin, J, Fischer, K, Wu, B, Davis, PJ, Kumar, S, Brattig, NW, Slatko, BE, Weil, GJ, Fischer, PU (2010) Endosymbiont DNA in endobacteria-free filarial nematodes indicates ancient horizontal genetic transfer. PLoS One 5: pp. e11029 CrossRef
17. Desjardins, CA, Cerqueira, GC, Goldberg, JM, Dunning Hotopp, JC, Haas, BJ, Zucker, J, Ribeiro, JM, Saif, S, Levin, JZ, Fan, L, Zeng, Q, Russ, C, Wortman, JR, Fink, DL, Birren, BW, Nutman, TB (2013) Genomics of Loa loa, a Wolbachia-free filarial parasite of humans. Nat Genet 45: pp. 495-500 CrossRef
18. Koutsovoulos, G, Makepeace, B, Tanya, VN, Blaxter, M (2014) Palaeosymbiosis revealed by genomic fossils of Wolbachia in a strongyloidean nematode. PLoS Genet 10: pp. e1004397 CrossRef
19. Klasson, L, Kambris, Z, Cook, PE, Walker, T, Sinkins, SP (2009) Horizontal gene transfer between Wolbachia and the mosquito Aedes aegypti. BMC Genomics 10: pp. 33 CrossRef
20. Woolfit, M, Iturbe-Ormaetxe, I, McGraw, EA, O鈥橬eill, SL (2009) An ancient horizontal gene transfer between mosquito and the endosymbiotic bacterium Wolbachia pipientis. Mol Biol Evol 26: pp. 367-374 CrossRef
21. Korochkina, S, Barreau, C, Pradel, G, Jeffery, E, Li, J, Natarajan, R, Shabanowitz, J, Hunt, D, Frevert, U, Vernick, KD (2006) A mosquito-specific protein family includes candidate receptors for malaria sporozoite invasion of salivary glands. Cell Microbiol 8: pp. 163-175 CrossRef
22. Husnik, F, Nikoh, N, Koga, R, Ross, L, Duncan, RP, Fujie, M, Tanaka, M, Satoh, N, Bachtrog, D, Wilson, AC, von Dohlen, CD, Fukatsu, T, McCutcheon, JP (2013) Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell 153: pp. 1567-1578 CrossRef
23. Nikoh, N, Nakabachi, A (2009) Aphids acquired symbiotic genes via lateral gene transfer. BMC Biol 7: pp. 12 CrossRef
24. Wu, B, Novelli, J, Jiang, D, Dailey, HA, Landmann, F, Ford, L, Taylor, MJ, Carlow, CK, Kumar, S, Foster, JM, Slatko, BE (2013) Interdomain lateral gene transfer of an essential ferrochelatase gene in human parasitic nematodes. Proc Natl Acad Sci U S A 110: pp. 7748-7753 CrossRef
25. Kumar, N, Creasy, T, Sun, Y, Flowers, M, Tallon, LJ, Dunning Hotopp, JC (2012) Efficient subtraction of insect rRNA prior to transcriptome analysis of Wolbachia-Drosophila lateral gene transfer. BMC Res Notes 5: pp. 230 CrossRef
26. Clark, AG, Eisen, MB, Smith, DR, Bergman, CM, Oliver, B, Markow, TA, Kaufman, TC, Kellis, M, Gelbart, W, Iyer, VN, Pollard, DA, Sackton, TB, Larracuente, AM, Singh, ND, Abad, JP, Abt, DN, Adryan, B, Aguade, M, Akashi, H, Anderson, WW, Aquadro, CF, Ardell, DH, Arguello, R, Artieri, CG, Barbash, DA, Barker, D, Barsanti, P, Batterham, P, Batzoglou, S, Begun, D (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450: pp. 203-218 CrossRef
27. Klasson, L, Westberg, J, Sapountzis, P, Naslund, K, Lutnaes, Y, Darby, AC, Veneti, Z, Chen, L, Braig, HR, Garrett, R, Bourtzis, K, Andersson, SG (2009) The mosaic genome structure of the Wolbachia wRi strain infecting Drosophila simulans. Proc Natl Acad Sci U S A 106: pp. 5725-5730 CrossRef
28. Li, H, Durbin, R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: pp. 1754-1760 CrossRef
29. Salzberg, SL, Dunning Hotopp, JC, Delcher, AL, Pop, M, Smith, DR, Eisen, MB, Nelson, WC (2005) Serendipitous discovery of Wolbachia genomes in multiple Drosophila species. Genome Biol 6: pp. R23 CrossRef
30. Iturbe-Ormaetxe, I, Riegler, M, O鈥橬eill, SL (2005) New names for old strains? Wolbachia wSim is actually wRi. Genome Biol 6: pp. 401 CrossRef
31. Choi, JY, Aquadro, CF (2014) The coevolutionary period of wolbachia pipientis infecting drosophila ananassae and its impact on the evolution of the host germline stem cell regulating genes. Mol Biol Evol 31: pp. 2457-2471 CrossRef
32. Ioannidis, P, Johnston, KL, Riley, DR, Kumar, N, White, JR, Olarte, KT, Ott, S, Tallon, LJ, Foster, JM, Taylor, MJ, Dunning Hotopp, JC (2013) Extensively duplicated and transcriptionally active recent lateral gene transfer from a bacterial Wolbachia endosymbiont to its host filarial nematode Brugia malayi. BMC Genomics 14: pp. 639 CrossRef
33. Schaeffer, SW, Bhutkar, A, McAllister, BF, Matsuda, M, Matzkin, LM, O鈥橤rady, PM, Rohde, C, Valente, VL, Aguade, M, Anderson, WW, Edwards, K, Garcia, AC, Goodman, J, Hartigan, J, Kataoka, E, Lapoint, RT, Lozovsky, ER, Machado, CA, Noor, MA, Papaceit, M, Reed, LK, Richards, S, Rieger, TT, Russo, SM, Sato, H, Segarra, C, Smith, DR, Smith, TF, Strelets, V, Tobari, YN (2008) Polytene chromosomal maps of 11 Drosophila species: the order of genomic scaffolds inferred from genetic and physical maps. Genetics 179: pp. 1601-1655 CrossRef
34. Edgar, BA, Orr-Weaver, TL (2001) Endoreplication cell cycles: more for less. Cell 105: pp. 297-306 CrossRef
35. Yin, H, Sweeney, S, Raha, D, Snyder, M, Lin, H (2011) A high-resolution whole-genome map of key chromatin modifications in the adult Drosophila melanogaster. PLoS Genet 7: pp. e1002380 CrossRef
36. Tobari, YN, Goni, B, Tomimura, Y, Matsuda, M Chromosomes. In: Tobari, YN eds. (1993) Drosophila Ananassae: Genetical and Biological Aspects. Japan Scientific Societies Press, Tokyopp. 289
37. Bosco, G, Campbell, P, Leiva-Neto, JT, Markow, TA (2007) Analysis of Drosophila species genome size and satellite DNA content reveals significant differences among strains as well as between species. Genetics 177: pp. 1277-1290 CrossRef
38. Eaton, ML, Prinz, JA, MacAlpine, HK, Tretyakov, G, Kharchenko, PV, MacAlpine, DM (2011) Chromatin signatures of the Drosophila replication program. Genome Res 21: pp. 164-174 CrossRef
39. Spradling, AC, Bellen, HJ, Hoskins, RA (2011) Drosophila P elements preferentially transpose to replication origins. Proc Natl Acad Sci U S A 108: pp. 15948-15953 CrossRef
40. Ashburner, M, Golic, GK, Hawley, RS (2005) Drosophila: A Laboratory Handbook. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
41. Das, A, Mohanty, S, Stephan, W (2004) Inferring the population structure and demography of Drosophila ananassae from multilocus data. Genetics 168: pp. 1975-1985 CrossRef
42. Riddle, NC, Elgin, SC (2006) The dot chromosome of Drosophila: insights into chromatin states and their change over evolutionary time. Chromosome Res 14: pp. 405-416 CrossRef
43. Singh, ND, Larracuente, AM, Sackton, TB, Clark, AG (2009) Comparative genomics on the Drosophila phylogenetic tree. Annu Rev Ecol Evol Syst 40: pp. 459-480 CrossRef
44. Li, H, Handsaker, B, Wysoker, A, Fennell, T, Ruan, J, Homer, N, Marth, G, Abecasis, G, Durbin, R (2009) The sequence alignment/Map format and SAMtools. Bioinformatics 25: pp. 2078-2079 CrossRef
45. Fluorescence in situ hybridization combined with immunostaining on polytene chromosomes. [http://www.igh.cnrs.fr/equip/cavalli/Lab%20Protocols/FISH-Immuno_Grimaud.pdf] - 刊物主题：Life Sciences, general; Microarrays; Proteomics; Animal Genetics and Genomics; Microbial Genetics and Genomics; Plant Genetics & Genomics;
- 出版者：BioMed Central
- ISSN：1471-2164
文摘
Background Lateral gene transfer (LGT) from bacterial Wolbachia endosymbionts has been detected in ~20% of arthropod and nematode genome sequencing projects. Many of these transfers are large and contain a substantial part of the Wolbachia genome. Results Here, we re-sequenced three D. ananassae genomes from Asia and the Pacific that contain large LGTs from Wolbachia. We find that multiple copies of the Wolbachia genome are transferred to the Drosophila nuclear genome in all three lines. In the D. ananassae line from Indonesia, the copies of Wolbachia DNA in the nuclear genome are nearly identical in size and sequence yielding an even coverage of mapped reads over the Wolbachia genome. In contrast, the D. ananassae lines from Hawaii and India show an uneven coverage of mapped reads over the Wolbachia genome suggesting that different parts of these LGTs are present in different copy numbers. In the Hawaii line, we find that this LGT is underrepresented in third instar larvae indicative of being heterochromatic. Fluorescence in situ hybridization of mitotic chromosomes confirms that the LGT in the Hawaii line is heterochromatic and represents ~20% of the sequence on chromosome 4 (dot chromosome, Muller element F). Conclusions This collection of related lines contain large lateral gene transfers composed of multiple Wolbachia genomes that constitute >2% of the D. ananassae genome (~5 Mbp) and partially explain the abnormally large size of chromosome 4 in D. ananassae.