Abstract
We analyzed extra chromosomal genomes of avian blood protozoa, Leucocytozoon caulleryi. One of the genomes, the mitochondrial genome was completely sequenced resulting 5,959 bp in length. This genome contained the identical gene organization and contents to that of other avian blood protozoa previously analyzed: three functional genes for cytochrome c oxidase subunit I, III, and cytochrome b with following sets of discontinuous and scrambled 15 ribosomal subunit RNA genes. In addition, the mitochondrial genome was estimated to have the tandem repeated structure as well as previously found in avian Plasmodium species. Furthermore, we found partial gene sequences of apicoplast DNA, another extra chromosomal genome, from L. caulleryi. These sequences were estimated as partial caseinolytic protease C and elongation factor Tu A genes. This report is the first description of two extra chromosomal genomes of L. caulleryi.

Similar content being viewed by others
References
Atkinson CT, Van-Riper C (1991) Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon and Haemoproteus. In: Loye JE, Zuk M (eds) Bird-parasite interactions: ecology, evolution and behaviour. University of Oxford Press, Oxford, pp 19–48
Cai X, Fuller AL, McDougald LR, Zhu G (2003) Apicoplast genome of the coccidian Eimeria tenella. Gene 321:39–46
Douglas SE (1999) Evolutionary history of plastids. Biol Bull 196:397–399
Douglas SE, Penny SL (1999) The plastid genome of the cryptophyte alga, Guillardia theta: complete sequence and conserved synteny groups confirm its common ancestry with red algae. J Mol Evol 48:236–244
Ginsburg H, Divo AA, Geary TG, Boland MT, Jensen JB (1986) Effects of mitochondrial inhibitors on intraerythrocytic Plasmodium falciparum in in vitro cultures. J Protozool 33:121–125
Hellgren O, Waldenstrom J, Bensch S (2004) A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. J Parasitol 90:797–802
Isobe T, Suzuki K, Yoshihara S (1991) Protection against chicken leucocytozoonosis provided by immunization with spleen homogenate infected with Leucocytozoon caulleryi. Avian Dis 35:559–562
Ito A, Gotanda T (2004) Field efficacy of recombinant R7 vaccine against chicken Leucocytozoonosis. J Vet Med Sci 66:483–487
Ito A, Gotanda T, Kobayashi S, Kume K, Sugimoto C, Matsumura T (2005) Increase of antibody titer against Leucocytozoon caulleryi by oral administration of recombinant R7 antigen. J Vet Med Sci 67:211–213
Joseph JT, Aldritt SM, Unnasch T, Puijalon O, Wirth DF (1989) Characterization of a conserved extrachromosomal element isolated from the avian malarial parasite Plasmodium gallinaceum. Mol Cell Biol 9:3621–3629
Martinsen ES, Perkins SL, Schall JJ (2008) A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): Evolution of life-history traits and host switches. Mol Phylogenet Evol 47:261–273
Morii T, Shiihara T, Lee YC, Manuel MF, Nakamura K, Iijima T, Hoji K (1981) Seroimmunological and parasitological surveys of Leucocytozoon caulleryi infection in chickens in several Asian countries. Int J Parasitol 11:187–190
Omori S, Sato Y, Isobe T, Yukawa M, Murata K (2007) Complete nucleotide sequences of the mitochondrial genomes of two avian malaria protozoa, Plasmodium gallinaceum and Plasmodium juxtanucleare. Parasitol Res 100:661–664
Perkins SL, Schall JJ (2002) A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. J Parasitol 88:972–978
Perkins SL, Sarkar IN, Carter R (2007) The phylogeny of rodent malaria parasites: simultaneous analysis across three genomes. Infect Genet Evol 7:74–83
Rathore D, Wahl AM, Sullivan M, McCutchan TF (2001) A phylogenetic comparison of gene trees constructed from plastid, mitochondrial and genomic DNA of Plasmodium species. Mol Biochem Parasitol 114:89–94
Sato Y, Hagihara M, Yamaguchi T, Yukawa M, Murata K (2007) Phylogenetic comparison of Leucocytozoon spp. from wild birds of Japan. J Vet Med Sci 69:55–59
Surolia N, Surolia A (2001) Triclosan offers protection against blood stages of malaria by inhibiting enoyl-ACP reductase of Plasmodium falciparum. Nat Med 7:167–173
Waller RF, Keeling PJ, Donald RG, Striepen B, Handman E, Lang-Unnasch N, Cowman AF, Besra GS, Roos DS, McFadden GI (1998) Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. Proc Natl Acad Sci U S A 95:12352–12357
Wilson RJ, Williamson DH, Preiser P (1994) Malaria and other Apicomplexans: the “plant” connection. Infect Agents Dis 3:29–37
Yu CY, Wang JS (2001) Role of chicken serum in inhibiting Leucocytozoon caulleryi development in Culicoides arakawae infected by membrane-feeding of infective blood meals. Parasitol Res 87:698–701
Acknowledgements
The authors are very grateful for Motohashi A. for her technical assistances. This study was partially supported by the Academic Frontier Project “Surveillance and control for zoonoses” and “High-Tech Research Center” Project for Private Universities matching funds subsidy from Ministry of Education, Culture, Sports, Science and Technology of Japan, Global Environment Research Fund of the Ministry of the Environment of Japan (F-062), Nihon University Research Grants, and a Grant-in-Aid for JSPS Fellows (No. 203886) from the Japan Society for the Promotion of Science.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Omori, S., Sato, Y., Hirakawa, S. et al. Two extra chromosomal genomes of Leucocytozoon caulleryi; complete nucleotide sequences of the mitochondrial genome and existence of the apicoplast genome. Parasitol Res 103, 953–957 (2008). https://doi.org/10.1007/s00436-008-1083-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-008-1083-4