Abstract
In the present study, near-complete mitochondrial (mt) genome sequences for Schistosoma japonicum from different regions in the Philippines and Japan were amplified and sequenced. Comparisons among S. japonicum from the Philippines, Japan, and China revealed a geographically based length difference in mt genomes, but the mt genomic organization and gene arrangement were the same. Sequence differences among samples from the Philippines and all samples from the three endemic areas were 0.57–2.12 and 0.76–3.85 %, respectively. The most variable part of the mt genome was the non-coding region. In the coding portion of the genome, protein-coding genes varied more than rRNA genes and tRNAs. The near-complete mt genome sequences for Philippine specimens were identical in length (14,091 bp) which was 4 bp longer than those of S. japonicum samples from Japan and China. This indel provides a unique genetic marker for S. japonicum samples from the Philippines. Phylogenetic analyses based on the concatenated amino acids of 12 protein-coding genes showed that samples of S. japonicum clustered according to their geographical origins. The identified mitochondrial indel marker will be useful for tracing the source of S. japonicum infection in humans and animals in Southeast Asia.
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Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104–2105
Beltran S, Galinier R, Allienne JF, Boissier J (2008) Cheap, rapid and efficient DNA extraction method to perform multilocus microsatellite genotyping on all Schistosoma mansoni stages. Mem Inst Oswaldo Cruz 103:501–503
Bergquist R, Tanner M (2010) Controlling schistosomiasis in Southeast Asia: a tale of two countries. Adv Parasitol 72:109–144
Blas BL, Rosales MI, Lipayon IL, Yasuraoka K, Matsuda H, Hayashi M (2004) The schistosomiasis problem in the Philippines: a review. Parasitol Int 53:127–134
Boore JL (1999) Animal mitochondrial genomes. Nucleic Acids Res 27:1767–1780
Bowles J, Hope M, Tiu WU, Liu X, McManus DP (1993) Nuclear and mitochondrial genetic markers highly conserved between Chinese and Philippine Schistosoma japonicum. Acta Trop 55:217–229
Chen F, Li J, Sugiyama H, Weng YB, Zou FC, Lin RQ, Yuan ZG, Song HQ, Zhu XQ, Zhao GH (2011) Comparative analysis of 18S and 28S rDNA sequences of Schistosoma japonicum from mainland China, the Philippines and Japan. J Anim Vet Adv 10:2010–2015
Chen F, Li J, Sugiyama H, Zhou DH, Song HQ, Zhao GH, Zhu XQ (2015) Genetic variability among Schistosoma japonicum isolates from the Philippines, Japan and China revealed by sequence analysis of three mitochondrial genes. Mitochondrial DNA 26:35–40
Chilton NB, Gasser RB, Beveridge I (1995) Differences in a ribosomal DNA sequence of morphologically indistinguishable species within the Hypodontus macropi complex (Nematoda: Strongyloidea). Int J Parasitol 25:647–651
Gray DJ, Williams GM, Li Y, McManus DP (2008) Transmission dynamics of Schistosoma japonicum in the lakes and marshlands of China. PLoS ONE 3:e4058
Hotez PJ, Molyneux DH, Fenwick A, Kumaresan J, Sachs SE, Sachs JD, Savioli L (2007) Control of neglected tropical diseases. N Engl J Med 357:1018–1027
Hu M, Jex AR, Campbell BE, Gasser RB (2007) Long PCR amplification of the entire mitochondrial genome from individual helminths for direct sequencing. Nat Protoc 2:2339–2344
Le TH, Blair D, Agatsuma T, Humair PF, Campbell NJ, Iwagami M, Littlewood DT, Peacock B, Johnston DA, Bartley J, Rollinson D, Herniou EA, Zarlenga DS, McManus DP (2000) Phylogenies inferred from mitochondrial gene orders—a cautionary tale from the parasitic flatworms. Mol Biol Evol 17:1123–1125
Le TH, Blair D, McManus DP (2002) Revisiting the question of limited genetic variation within Schistosoma japonicum. Ann Trop Med Parasitol 96:155–164
Leonardo LR, Rivera P, Saniel O, Villacorte E, Crisostomo B, Hernandez L, Baquilod M, Erce E, Martinez R, Velayudhan R (2008) Prevalence survey of schistosomiasis in Mindanao and the Visayas, The Philippines. Parasitol Int 57:246–251
Liu GH, Wang Y, Xu MJ, Zhou DH, Ye YG, Li JY, Song HQ, Lin RQ, Zhu XQ (2012) Characterization of the complete mitochondrial genomes of two whipworms Trichuris ovis and Trichuris discolor (Nematoda: Trichuridae). Infect Genet Evol 12:1635–1641
Lv Z, Wu Z, Zhang L, Ji P, Cai Y, Luo S, Wang H, Li H (2015) Genome mining offers a new starting point for parasitology research. Parasitol Res 114:399–409
Mullaney JM, Mills RE, Pittard WS, Devine SE (2010) Small insertions and deletions (INDELs) in human genomes. Hum Mol Genet 19:R131–R136
Nairz K, Zipperlen P, Schneider M (2007) FLP-Mapping: a universal, cost-effective, and automatable method for gene mapping. Methods Mol Biol 396:419–432
Olveda DU, Li Y, Olveda RM, Lam AK, McManus DP, Chau TN, Harn DA, Williams GM, Gray DJ, Ross AG (2014) Bilharzia in the Philippines: past, present, and future. Int J Infect Dis 18:52–56
Page RD (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Schistosoma japonicum Genome Sequencing and Functional Analysis Consortium (2009) The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 460:345–351
Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J (2006) Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis 6:411–425
Strimmer K, Von Haeseler A (1996) Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies. Mol Biol Evol 13:964–969
Sugiyama H, Kawanaka M, Kameoka Y, Nakamura M (1997) A novel cDNA clone of Schistosoma japonicum encoding the 34,000 Dalton eggshell precursor protein. Int J Parasitol 27:811–817
Swofford DL (2002) PAUP*: Phylogenetic Analysis Using Parsimony (and other methods). Sinauer Associates, Sunderland
Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882
Wang W, Dai JR, Liang YS, Huang YX, Coles GC (2009) Impact of the South-to-North water diversion project on the transmission of Schistosoma japonicum in China. Ann Trop Med Parasitol 103:17–29
Wu W, Feng A, Huang Y (2015) Research and control of advanced schistosomiasis japonica in China. Parasitol Res 114:17–27
Xianyi C, Liying W, Jiming C, Xiaonong Z, Jiang Z, Jiagang G, Xiaohua W, Engels D, Minggang C (2005) Schistosomiasis control in China: the impact of a 10-year World Bank loan project (1992–2001). Bull World Health Organ 83:43–48
Zarowiecki MZ, Huyse T, Littlewood DT (2007) Making the most of mitochondrial genomes—markers for phylogeny, molecular ecology and barcodes in Schistosoma (Platyhelminthes: Digenea). Int J Parasitol 37:1401–1418
Zhao GH, Li J, Mo XH, Li XY, Lin RQ, Zou FC, Weng YB, Song HQ, Zhu XQ (2012a) The second transcribed spacer rDNA sequence: an effective genetic marker for inter-species phylogenetic analysis of trematodes in the order Strigeata. Parasitol Res 111:1467–1472
Zhao GH, Li J, Blair D, Li XY, Elsheikha HM, Lin RQ, Zou FC, Zhu XQ (2012b) Biotechnological advances in the diagnosis, species differentiation and phylogenetic analysis of Schistosoma spp. Biotechnol Adv 30:1381–1389
Zhao GH, Li J, Song HQ, Li XY, Chen F, Lin RQ, Yuan ZG, Weng YB, Hu M, Zou FC, Zhu XQ (2012c) A specific PCR assay for the identification and differentiation of Schistosoma japonicum geographical isolates in mainland China based on analysis of mitochondrial genome sequences. Infect Genet Evol 12:1027–1036
Zhou YB, Liang S, Chen GX, Rea C, He ZG, Zhang ZJ, Wei JG, Zhao GM, Jiang QW (2011) An integrated strategy for transmission control of Schistosoma japonicum in a marshland area of China: findings from a five-year longitudinal survey and mathematical modeling. Am J Trop Med Hyg 85:83–88
Acknowledgments
This work is supported, in part, by the Pearl River Science and Technology New Star Project (Grant No. 2014J2200096), the President’s Foundation of Guangdong Academy of Agricultural Sciences (Grant No. 201413), the Science Fund for Creative Research Groups of Gansu Province (Grant No. 1210RJIA006), and the “Special Fund for Agro-scientific Research in the Public Interest” (Grant No. 201303037).
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Li, J., Chen, F., Sugiyama, H. et al. A specific indel marker for the Philippines Schistosoma japonicum revealed by analysis of mitochondrial genome sequences. Parasitol Res 114, 2697–2704 (2015). https://doi.org/10.1007/s00436-015-4475-2
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DOI: https://doi.org/10.1007/s00436-015-4475-2