BMC Genomics | |
Extensive duplication of the Wolbachia DNA in chromosome four of Drosophila ananassae | |
Julie C Dunning Hotopp3  Siv G E Andersson2  Luke J Tallon1  Sandra H Ott1  Melissa Flowers1  Karsten Sieber1  Robin Bromley1  Nikhil Kumar1  Lisa Klasson2  | |
[1] Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, MD 21201, USA;Department of Cell and Molecular Biology, Molecular Evolution, Uppsala University, Uppsala, Sweden;Department of Microbiology & Immunology, University of Maryland School of Medicine, Baltimore, MD 21201, USA | |
关键词: Heterochromatin; Underreplication; Symbiosis; Horizontal gene transfer; Lateral gene transfer; Wolbachia; Drosophila ananassae; | |
Others : 1127361 DOI : 10.1186/1471-2164-15-1097 |
|
received in 2014-08-08, accepted in 2014-12-03, 发布年份 2014 | |
【 摘 要 】
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.
【 授权许可】
2014 Klasson et al.; licensee BioMed Central.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20150220121516863.pdf | 7995KB | download | |
Figure 9. | 75KB | Image | download |
Figure 8. | 86KB | Image | download |
Figure 7. | 39KB | Image | download |
Figure 6. | 155KB | Image | download |
Figure 5. | 98KB | Image | download |
Figure 4. | 56KB | Image | download |
Figure 3. | 73KB | Image | download |
Figure 2. | 103KB | Image | download |
Figure 1. | 98KB | Image | download |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.
Figure 6.
Figure 7.
Figure 8.
Figure 9.
【 参考文献 】
- [1]Hazkani-Covo E, Zeller RM, Martin W: Molecular poltergeists: mitochondrial DNA copies (numts) in sequenced nuclear genomes. PLoS Genet 2010, 6(2):e1000834.
- [2]Stouthamer R, Breeuwer JA, Hurst GD: Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol 1999, 53:71-102.
- [3]Werren JH: Biology of Wolbachia. Annu Rev Entomol 1997, 42:587-609.
- [4]Zug R, Hammerstein P: Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS One 2012, 7(6):e38544.
- [5]Fast EM, Toomey ME, Panaram K, Desjardins D, Kolaczyk ED, Frydman HM: Wolbachia enhance Drosophila stem cell proliferation and target the germline stem cell niche. Science 2011, 334(6058):990-992.
- [6]Dunning Hotopp JC: Horizontal gene transfer between bacteria and animals. Trends Genet 2011, 27(4):157-163.
- [7]Robinson KM, Sieber KB, Dunning Hotopp JC: A review of bacteria-animal lateral gene transfer may inform our understanding of diseases like cancer. PLoS Genet 2013, 9(10):e1003877.
- [8]Kondo N, Nikoh N, Ijichi N, Shimada M, Fukatsu T: Genome fragment of Wolbachia endosymbiont transferred to X chromosome of host insect. Proc Natl Acad Sci U S A 2002, 99(22):14280-14285.
- [9]Nikoh N, Tanaka K, Shibata F, Kondo N, Hizume M, Shimada M, Fukatsu T: Wolbachia genome integrated in an insect chromosome: evolution and fate of laterally transferred endosymbiont genes. Genome Res 2008, 18(2):272-280.
- [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: Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 2007, 317(5845):1753-1756.
- [11]Fenn K, Conlon C, Jones M, Quail MA, Holroyd NE, Parkhill J, Blaxter M: Phylogenetic relationships of the Wolbachia of nematodes and arthropods. PLoS Pathog 2006, 2(10):e94.
- [12]Nikoh N, McCutcheon JP, Kudo T, Miyagishima SY, Moran NA, Nakabachi A: Bacterial genes in the aphid genome: absence of functional gene transfer from Buchnera to its host. PLoS Genet 2010, 6(2):e1000827.
- [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, et al.: Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 2010, 327(5963):343-348.
- [14]Aikawa T, Anbutsu H, Nikoh N, Kikuchi T, Shibata F, Fukatsu T: Longicorn beetle that vectors pinewood nematode carries many Wolbachia genes on an autosome. Proc Biol Sci 2009, 276(1674):3791-3798.
- [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: Presence of extensive Wolbachia symbiont insertions discovered in the genome of its host Glossina morsitans morsitans. PLoS Negl Trop Dis 2014, 8(4):e2728.
- [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: Endosymbiont DNA in endobacteria-free filarial nematodes indicates ancient horizontal genetic transfer. PLoS One 2010, 5(6):e11029.
- [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: Genomics of Loa loa, a Wolbachia-free filarial parasite of humans. Nat Genet 2013, 45(5):495-500.
- [18]Koutsovoulos G, Makepeace B, Tanya VN, Blaxter M: Palaeosymbiosis revealed by genomic fossils of Wolbachia in a strongyloidean nematode. PLoS Genet 2014, 10(6):e1004397.
- [19]Klasson L, Kambris Z, Cook PE, Walker T, Sinkins SP: Horizontal gene transfer between Wolbachia and the mosquito Aedes aegypti. BMC Genomics 2009, 10:33. BioMed Central Full Text
- [20]Woolfit M, Iturbe-Ormaetxe I, McGraw EA, O’Neill SL: An ancient horizontal gene transfer between mosquito and the endosymbiotic bacterium Wolbachia pipientis. Mol Biol Evol 2009, 26(2):367-374.
- [21]Korochkina S, Barreau C, Pradel G, Jeffery E, Li J, Natarajan R, Shabanowitz J, Hunt D, Frevert U, Vernick KD: A mosquito-specific protein family includes candidate receptors for malaria sporozoite invasion of salivary glands. Cell Microbiol 2006, 8(1):163-175.
- [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: Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell 2013, 153(7):1567-1578.
- [23]Nikoh N, Nakabachi A: Aphids acquired symbiotic genes via lateral gene transfer. BMC Biol 2009, 7:12. BioMed Central Full Text
- [24]Wu B, Novelli J, Jiang D, Dailey HA, Landmann F, Ford L, Taylor MJ, Carlow CK, Kumar S, Foster JM, Slatko BE: Interdomain lateral gene transfer of an essential ferrochelatase gene in human parasitic nematodes. Proc Natl Acad Sci U S A 2013, 110(19):7748-7753.
- [25]Kumar N, Creasy T, Sun Y, Flowers M, Tallon LJ, Dunning Hotopp JC: Efficient subtraction of insect rRNA prior to transcriptome analysis of Wolbachia-Drosophila lateral gene transfer. BMC Res Notes 2012, 5:230. BioMed Central Full Text
- [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, et al.: Evolution of genes and genomes on the Drosophila phylogeny. Nature 2007, 450(7167):203-218.
- [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: The mosaic genome structure of the Wolbachia wRi strain infecting Drosophila simulans. Proc Natl Acad Sci U S A 2009, 106(14):5725-5730.
- [28]Li H, Durbin R: Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25(14):1754-1760.
- [29]Salzberg SL, Dunning Hotopp JC, Delcher AL, Pop M, Smith DR, Eisen MB, Nelson WC: Serendipitous discovery of Wolbachia genomes in multiple Drosophila species. Genome Biol 2005, 6(3):R23. BioMed Central Full Text
- [30]Iturbe-Ormaetxe I, Riegler M, O’Neill SL: New names for old strains? Wolbachia wSim is actually wRi. Genome Biol 2005, 6(7):401. author reply 401 BioMed Central Full Text
- [31]Choi JY, Aquadro CF: 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 2014, 31(9):2457-2471.
- [32]Ioannidis P, Johnston KL, Riley DR, Kumar N, White JR, Olarte KT, Ott S, Tallon LJ, Foster JM, Taylor MJ, Dunning Hotopp JC: Extensively duplicated and transcriptionally active recent lateral gene transfer from a bacterial Wolbachia endosymbiont to its host filarial nematode Brugia malayi. BMC Genomics 2013, 14(1):639. BioMed Central Full Text
- [33]Schaeffer SW, Bhutkar A, McAllister BF, Matsuda M, Matzkin LM, O’Grady 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, et al.: Polytene chromosomal maps of 11 Drosophila species: the order of genomic scaffolds inferred from genetic and physical maps. Genetics 2008, 179(3):1601-1655.
- [34]Edgar BA, Orr-Weaver TL: Endoreplication cell cycles: more for less. Cell 2001, 105(3):297-306.
- [35]Yin H, Sweeney S, Raha D, Snyder M, Lin H: A high-resolution whole-genome map of key chromatin modifications in the adult Drosophila melanogaster. PLoS Genet 2011, 7(12):e1002380.
- [36]Tobari YN, Goni B, Tomimura Y, Matsuda M: Chromosomes. In Drosophila Ananassae: Genetical and Biological Aspects. Edited by Tobari YN. Tokyo: Japan Scientific Societies Press; 1993:289.
- [37]Bosco G, Campbell P, Leiva-Neto JT, Markow TA: Analysis of Drosophila species genome size and satellite DNA content reveals significant differences among strains as well as between species. Genetics 2007, 177(3):1277-1290.
- [38]Eaton ML, Prinz JA, MacAlpine HK, Tretyakov G, Kharchenko PV, MacAlpine DM: Chromatin signatures of the Drosophila replication program. Genome Res 2011, 21(2):164-174.
- [39]Spradling AC, Bellen HJ, Hoskins RA: Drosophila P elements preferentially transpose to replication origins. Proc Natl Acad Sci U S A 2011, 108(38):15948-15953.
- [40]Ashburner M, Golic GK, Hawley RS: Drosophila: A Laboratory Handbook. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 2005.
- [41]Das A, Mohanty S, Stephan W: Inferring the population structure and demography of Drosophila ananassae from multilocus data. Genetics 2004, 168(4):1975-1985.
- [42]Riddle NC, Elgin SC: The dot chromosome of Drosophila: insights into chromatin states and their change over evolutionary time. Chromosome Res 2006, 14(4):405-416.
- [43]Singh ND, Larracuente AM, Sackton TB, Clark AG: Comparative genomics on the Drosophila phylogenetic tree. Annu Rev Ecol Evol Syst 2009, 40:459-480.
- [44]Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R: The sequence alignment/Map format and SAMtools. Bioinformatics 2009, 25(16):2078-2079.
- [45]Fluorescence in situ hybridization combined with immunostaining on polytene chromosomes [http://www.igh.cnrs.fr/equip/cavalli/Lab%20Protocols/FISH-Immuno_Grimaud.pdf webcite]