Comparing the mitochondrial genomes of Wolbachia-dependent and independent filarial nematode species

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  McNulty, Samantha N ^a   Mullin, Andrew S ^a   Vaughan, Jefferson A ^b   Tkach, Vasyl V ^b   Weil, Gary J ^a   Fischer, Peter U ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH DAKOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA; RNA; TRANSFER RNA; MITOCHONDRIAL PROTEIN; RIBOSOME RNA;

ACANTHOCHEILONEMA VITEAE; ARTICLE; BRUGIA MALAYI; CHANDLERELLA QUISCALI; DIROFILARIA IMMITIS; GENE EXPRESSION; GENETIC CODE; LOA LOA; MITOCHONDRIAL GENOME; MITOCHONDRIAL VOLUME; NEMATODE; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCHOCERCA FLEXUOSA; ONCHOCERCA VOLVULUS; PHYLOGENY; RNA STRUCTURE; SETARIA DIGITATA; SPECIES COMPARISON; WOLBACHIA; WUCHERERIA BANCROFTI; ANIMAL; CHEMISTRY; CLASSIFICATION; CONFORMATION; FILARIOIDEA; GENETICS; LOA; METABOLISM; ONCHOCERCA;

ACANTHOCHEILONEMA VITEAE; BRUGIA MALAYI; DIROFILARIA IMMITIS; ENDOBACTERIA; LOA LOA; NEMATODA; ONCHOCERCA; ONCHOCERCA VOLVULUS; SETARIA DIGITATA; WOLBACHIA; WUCHERERIA BANCROFTI;

ANIMALS; FILARIOIDEA; GENOME, MITOCHONDRIAL; LOA; MITOCHONDRIAL PROTEINS; NUCLEIC ACID CONFORMATION; ONCHOCERCA; PHYLOGENY; RNA, RIBOSOMAL; RNA, TRANSFER; WUCHERERIA BANCROFTI;

EID: 84862187635     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-145     Document Type: Article

References (43)

1. Bandi C, Anderson TJ, Genchi C, Blaxter ML. Phylogeny ofWolbachiain filarial nematodes. Proc Biol Sci 1998, 265(1413):2407-2413. 10.1098/rspb.1998.0591, 1689538, 9921679.
2. Ferri E, Bain O, Barbuto M, Martin C, Lo N, Uni S, Landmann F, Baccei SG, Guerrero R, de Souza Lima S, Bandi C, Wanji S, Diagne M, Casiraghi M. New Insights into the Evolution ofWolbachiaInfections in Filarial Nematodes Inferred from a Large Range of Screened Species. PLoS One 2011, 6(6):e20843. 10.1371/journal.pone.0020843, 3120775, 21731626.
3. Kozek WJ, Marroquin HF. Intracytoplasmic bacteria inOnchocerca volvulus. AmJTrop Med Hyg 1977, 26(4):663-678.
4. Vincent AL, Ash LR, Frommes SP. The ultrastructure of adultBrugia malayi(Brug, 1927) (Nematoda: Filarioidea). J Parasitol 1975, 61(3):499-512. 10.2307/3279332, 1138041.
5. Hoerauf A, Mand S, Fischer K, Kruppa T, Marfo-Debrekyei Y, Debrah AY, Pfarr KM, Adjei O, Buttner DW. Doxycycline as a novel strategy against bancroftian filariasis-depletion ofWolbachiaendosymbionts fromWuchereria bancroftiand stop of microfilaria production. Med Microbiol Immunol 2003, 192(4):211-216. 10.1007/s00430-002-0174-6, 12684759.
6. Hoerauf A, Mand S, Volkmann L, Buttner M, Marfo-Debrekyei Y, Taylor M, Adjei O, Buttner DW. Doxycycline in the treatment of human onchocerciasis: Kinetics ofWolbachiaendobacteria reduction and of inhibition of embryogenesis in femaleOnchocercaworms. Microbes Infect 2003, 5(4):261-273. 10.1016/S1286-4579(03)00026-1, 12706439.
7. Hoerauf A, Nissen-Pahle K, Schmetz C, Henkle-Duhrsen K, Blaxter ML, Buttner DW, Gallin MY, Al-Qaoud KM, Lucius R, Fleischer B. Tetracycline therapy targets intracellular bacteria in the filarial nematodeLitomosoides sigmodontisand results in filarial infertility. J Clin Invest 1999, 103(1):11-18. 10.1172/JCI4768, 407866, 9884329.
8. Buttner DW, Wanji S, Bazzocchi C, Bain O, Fischer P. Obligatory symbioticWolbachiaendobacteria are absent fromLoa loa. Filaria J 2003, 2(1):10. 10.1186/1475-2883-2-10, 161789, 12801420.
9. McNulty SN, Fischer K, Mehus JO, Vaughan JA, Tkach VV, Weil GJ, Fischer PU. Absence of Wolbachia Endobacteria in Chandlerella quiscali , an Avian Filarial Parasite. J Parasitol 2012, 98(2):382-387. 10.1645/GE-2879.1, 22032328.
10. Plenge-Bonig A, Kromer M, Buttner DW. Light and electron microscopy studies onOnchocerca jakutensisandO. flexuosaof red deer show different host-parasite interactions. Parasitol Res 1995, 81(1):66-73. 10.1007/BF00932419, 7724516.
11. Andersson SG, Zomorodipour A, Andersson JO, Sicheritz-Ponten T, Alsmark UC, Podowski RM, Naslund AK, Eriksson AS, Winkler HH, Kurland CG. The genome sequence ofRickettsia prowazekiiand the origin of mitochondria. Nature 1998, 396(6707):133-140. 10.1038/24094, 9823893.
12. Dumler JS, Barbet AF, Bekker CP, Dasch GA, Palmer GH, Ray SC, Rikihisa Y, Rurangirwa FR. Reorganization of genera in the families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: unification of some species ofEhrlichiawithAnaplasma,CowdriawithEhrlichiaandEhrlichiawithNeorickettsia, descriptions of six new species combinations and designation ofEhrlichia equiand 'HGE agent' as subjective synonyms ofEhrlichia phagocytophila. Int J Syst Evol Microbiol 2001, 51(Pt 6):2145-2165.
13. Foster J, Ganatra M, Kamal I, Ware J, Makarova K, Ivanova N, Bhattacharyya A, Kapatral V, Kumar S, Posfai J, Vincze T, Ingram J, Moran L, Lapidus A, Omelchenko M, Kyrpides N, Ghedin E, Wang S, Goltsman E, Joukov V, Ostrovskaya O, Tsukerman K, Mazur M, Comb D, Koonin E, Slatko B. TheWolbachiagenome ofBrugia malayi: endosymbiont evolution within a human pathogenic nematode. PLoS Biol 2005, 3(4):e121. 10.1371/journal.pbio.0030121, 1069646, 15780005.
14. Strubing U, Lucius R, Hoerauf A, Pfarr KM. Mitochondrial genes for heme-dependent respiratory chain complexes are up-regulated after depletion ofWolbachiafrom filarial nematodes. Int J Parasitol 2010, 40(10):1193-1202. 10.1016/j.ijpara.2010.03.004, 20362581.
15. Werren JH, Baldo L, Clark ME. Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 2008, 6(10):741-751. 10.1038/nrmicro1969, 18794912.
16. Delgado AM, Cook JM. Effects of a sex-ratio distorting endosymbiont on mtDNA variation in a global insect pest. BMC Evol Biol 2009, 9:49. 10.1186/1471-2148-9-49, 2671496, 19257899.
17. Hurst GD, Jiggins FM. Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proc Biol Sci 2005, 272(1572):1525-1534. 10.1098/rspb.2005.3056, 1559843,1559843, 16048766.
18. Raychoudhury R, Grillenberger BK, Gadau J, Bijlsma R, van de Zande L, Werren JH, Beukeboom LW. Phylogeography ofNasonia vitripennis(Hymenoptera) indicates a mitochondrial-Wolbachiasweep in North America. Heredity 2010, 104(3):318-326. 10.1038/hdy.2009.160, 20087396.
19. Turelli M, Hoffmann AA. Rapid spread of an inherited incompatibility factor in CaliforniaDrosophila. Nature 1991, 353(6343):440-442. 10.1038/353440a0, 1896086.
20. Turelli M, Hoffmann AA, McKechnie SW. Dynamics of cytoplasmic incompatibility and mtDNA variation in naturalDrosophila simulanspopulations. Genetics 1992, 132(3):713-723. 1205209, 1468627.
21. Belanger DH, Perkins SL. Wolbachiainfection and mitochondrial diversity in the canine heartworm (Dirofilaria immitis). Mitochondrial DNA 2010, 21(6):227-233. 10.3109/19401736.2010.533765, 21171866.
22. Keddie EM, Higazi T, Unnasch TR. The mitochondrial genome ofOnchocerca volvulus: sequence, structure and phylogenetic analysis. Mol Biochem Parasitol 1998, 95(1):111-127. 10.1016/S0166-6851(98)00102-9, 9763293.
23. Hu M, Gasser RB, Abs El-Osta YG, Chilton NB. Structure and organization of the mitochondrial genome of the canine heartworm,Dirofilaria immitis. Parasitology 2003, 127(Pt 1):37-51.
24. Ghedin E, Wang S, Spiro D, Caler E, Zhao Q, Crabtree J, Allen JE, Delcher AL, Guiliano DB, Miranda-Saavedra D, Angiuoli SV, Creasy T, Amedeo P, Haas B, El-Sayed NM, Wortman JR, Feldblyum T, Tallon L, Schatz M, Shumway M, Koo H, Salzberg SL, Schobel S, Pertea M, Pop M, White O, Barton GJ, Carlow CK, Crawford MJ, Daub J, Dimmic MW, Estes CF, Foster JM, Ganatra M, Gregory WF, Johnson NM, Jin J, Komuniecki R, Korf I, Kumar S, Laney S, Li BW, Li W, Lindblom TH, Lustigman S, Ma D, Maina CV, Martin DM, McCarter JP, McReynolds L, Mitreva M, Nutman TB, Parkinson J, Peregrin-Alvarez JM, Poole C, Ren Q, Saunders L, Sluder AE, Smith K, Stanke M, Unnasch TR, Ware J, Wei AD, Weil G, Williams DJ, Zhang Y, Williams SA, Fraser-Liggett C, Slatko B, Blaxter ML, Scott AL. Draft genome of the filarial nematode parasiteBrugia malayi. Science 2007, 317(5845):1756-1760. 10.1126/science.1145406, 2613796, 17885136.
25. Yatawara L, Wickramasinghe S, Rajapakse RP, Agatsuma T. The complete mitochondrial genome ofSetaria digitata(Nematoda: Filarioidea): Mitochondrial gene content, arrangement and composition compared with other nematodes. Mol Biochem Parasitol 2010, 173(1):32-38. 10.1016/j.molbiopara.2010.05.004, 20470833.
26. Casiraghi M, Bain O, Guerrero R, Martin C, Pocacqua V, Gardner SL, Franceschi A, Bandi C. Mapping the presence ofWolbachia pipientison the phylogeny of filarial nematodes: evidence for symbiont loss during evolution. Int J Parasitol 2004, 34(2):191-203. 10.1016/j.ijpara.2003.10.004, 15037105.
27. McLaren DJ, Worms MJ, Laurence BR, Simpson MG. Micro-organisms in filarial larvae (Nematoda). Trans R Soc Trop Med Hyg 1975, 69(5-6):509-514.
28. McGarry HF, Pfarr K, Egerton G, Hoerauf A, Akue JP, Enyong P, Wanji S, Klager SL, Bianco AE, Beeching NJ, Taylor MJ. Evidence againstWolbachiasymbiosis inLoa loa. Filaria J 2003, 2(1):9. 10.1186/1475-2883-2-9, 161820, 12816546.
29. 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. 10.1371/journal.pone.0011029, 2882956, 20543958.
30. Casiraghi M, Anderson TJ, Bandi C, Bazzocchi C, Genchi C. A phylogenetic analysis of filarial nematodes: comparison with the phylogeny ofWolbachiaendosymbionts. Parasitology 2001, 122(Pt 1):93-103.
31. Anderson RC, Bain O. Keys to genera of the order Spirurida. Part 3. Diplotriaenoidea, Aproctoidea and Filarioidea. In CIH keys to the nematode parasites of vertebrates 1976, 59-116. Commonwealth Agricultural Bureau, Farnham Royal, UK, Anderson RC, Chabaud AG, Willmott S.
32. Wong LJ. Molecular genetics of mitochondrial disorders. Dev Disabil Res Rev 2010, 16(2):154-162. 10.1002/ddrr.104, 20818730.
33. Ash LR, Riley JM. Development of subperiodicBrugia malayiin the jird,Meriones unguiculatus, with notes on infections in other rodents. J Parasitol 1970, 56(5):969-973. 10.2307/3277515, 5504534.
34. Lucius R, Textor G. Acanthocheilonema viteae: rational design of the life cycle to increase production of parasite material using less experimental animals. Appl Parasitol 1995, 36(1):22-33.
35. Fischer P, Kipp W, Bamuhiga J, Binta-Kahwa J, Kiefer A, Buttner DW. Parasitological and clinical characterization ofSimulium neavei-transmitted onchocerciasis in western Uganda. Trop Med Parasitol 1993, 44(4):311-321.
36. Weil GJ, Kastens W, Susapu M, Laney SJ, Williams SA, King CL, Kazura JW, Bockarie MJ. The impact of repeated rounds of mass drug administration with diethylcarbamazine plus albendazole on bancroftian filariasis in Papua New Guinea. PLoS Negl Trop Dis 2008, 2(12):e344. 10.1371/journal.pntd.0000344, 2586652, 19065257.
37. Laslett D, Canback B. ARWEN: a program to detect tRNA genes in metazoan mitochondrial nucleotide sequences. Bioinformatics 2008, 24(2):172-175. 10.1093/bioinformatics/btm573, 18033792.
38. Carver T, Thomson N, Bleasby A, Berriman M, Parkhill J. DNAPlotter: circular and linear interactive genome visualization. Bioinformatics 2009, 25(1):119-120. 10.1093/bioinformatics/btn578, 2612626,2612626, 18990721.
39. Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24(8):1596-1599. 10.1093/molbev/msm092, 17488738.
40. Kuck P, Meusemann K. FASconCAT: Convenient handling of data matrices. Mol Phylogenet Evol 2010, 56(3):1115-1118. 10.1016/j.ympev.2010.04.024, 20416383.
41. Nylander JAA. MrModeltest v2. 2004, Program distributed by the author 2004, Evolutionary Biology Centre, Uppsala University, .
42. Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001, 17(8):754-755. 10.1093/bioinformatics/17.8.754, 11524383.
43. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19(12):1572-1574. 10.1093/bioinformatics/btg180, 12912839.