Chromosome-scale genome of the human blood fluke Schistosoma mekongi and its implications for public health

Abstract Background Schistosoma mekongi is a human blood fluke causing schistosomiasis that threatens approximately 1.5 million humans in the world. Nonetheless, the limited available S. mekongi genomic resources have hindered understanding of its biology and parasite-host interactions for disease m...

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Main Authors: Minyu Zhou, Lian Xu, Dahua Xu, Wen Chen, Jehangir Khan, Yue Hu, Hui Huang, Hang Wei, Yiqing Zhang, Phiraphol Chusongsang, Kanthi Tanasarnprasert, Xiang Hu, Yanin Limpanont, Zhiyue Lv
Format: Article
Language:English
Published: BMC 2023-11-01
Series:Infectious Diseases of Poverty
Subjects:
Online Access:https://doi.org/10.1186/s40249-023-01160-6
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author Minyu Zhou
Lian Xu
Dahua Xu
Wen Chen
Jehangir Khan
Yue Hu
Hui Huang
Hang Wei
Yiqing Zhang
Phiraphol Chusongsang
Kanthi Tanasarnprasert
Xiang Hu
Yanin Limpanont
Zhiyue Lv
author_facet Minyu Zhou
Lian Xu
Dahua Xu
Wen Chen
Jehangir Khan
Yue Hu
Hui Huang
Hang Wei
Yiqing Zhang
Phiraphol Chusongsang
Kanthi Tanasarnprasert
Xiang Hu
Yanin Limpanont
Zhiyue Lv
author_sort Minyu Zhou
collection DOAJ
description Abstract Background Schistosoma mekongi is a human blood fluke causing schistosomiasis that threatens approximately 1.5 million humans in the world. Nonetheless, the limited available S. mekongi genomic resources have hindered understanding of its biology and parasite-host interactions for disease management and pathogen control. The aim of our study was to integrate multiple technologies to construct a high-quality chromosome-level assembly of the S. mekongi genome. Methods The reference genome for S. mekongi was generated through integrating Illumina, PacBio sequencing, 10 × Genomics linked-read sequencing, and high-throughput chromosome conformation capture (Hi-C) methods. In this study, we conducted de novo assembly, alignment, and gene prediction to assemble and annotate the genome. Comparative genomics allowed us to compare genomes across different species, shedding light on conserved regions and evolutionary relationships. Additionally, our transcriptomic analysis focused on genes associated with parasite-snail interactions in S. mekongi infection. We employed gene ontology (GO) enrichment analysis for functional annotation of these genes. Results In the present study, the S. mekongi genome was both assembled into 8 pseudochromosomes with a length of 404 Mb, with contig N50 and scaffold N50 lengths of 1168 kb and 46,759 kb, respectively. We detected that 43% of the genome consists of repeat sequences and predicted 9103 protein-coding genes. We also focused on proteases, particularly leishmanolysin-like metalloproteases (M8), which are crucial in the invasion of hosts by 12 flatworm species. Through phylogenetic analysis, it was discovered that the M8 gene exhibits lineage-specific amplification among the genus Schistosoma. Lineage-specific expansion of M8 was observed in blood flukes. Additionally, the results of the RNA-seq revealed that a mass of genes related to metabolic and biosynthetic processes were up-regulated, which might be beneficial for cercaria production. Conclusions This study delivers a high-quality, chromosome-scale reference genome of S. mekongi, enhancing our understanding of the divergence and evolution of Schistosoma. The molecular research conducted here also plays a pivotal role in drug discovery and vaccine development. Furthermore, our work greatly advances the understanding of host-parasite interactions, providing crucial insights for schistosomiasis intervention strategies. Graphical Abstract
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spelling doaj.art-5aade6f3bdee4ca9bb965852eee1c1592023-12-03T12:40:22ZengBMCInfectious Diseases of Poverty2049-99572023-11-0112111710.1186/s40249-023-01160-6Chromosome-scale genome of the human blood fluke Schistosoma mekongi and its implications for public healthMinyu Zhou0Lian Xu1Dahua Xu2Wen Chen3Jehangir Khan4Yue Hu5Hui Huang6Hang Wei7Yiqing Zhang8Phiraphol Chusongsang9Kanthi Tanasarnprasert10Xiang Hu11Yanin Limpanont12Zhiyue Lv13Key Laboratory of Tropical Disease Control, Ministry of Education, Sun Yat-Sen UniversityKey Laboratory of Neuroregeneration, Ministry of Education and Jiangsu Province, Co-Innovation Center of Neuroregeneration, NMPA Key Laboratory for Research and Evaluation of Tissue Engineering Technology Products, Nantong UniversityKey Laboratory of Tropical Translational Medicine of Ministry of Education, College of Biomedical Information and Engineering, Hainan Medical UniversityKey Laboratory of Vascular Biology and Translational Medicine, Medical School, Hunan University of Chinese MedicineKey Laboratory of Tropical Disease Control, Ministry of Education, Sun Yat-Sen UniversityKey Laboratory of Tropical Disease Control, Ministry of Education, Sun Yat-Sen UniversityKey Laboratory of Tropical Disease Control, Ministry of Education, Sun Yat-Sen UniversityKey Laboratory of Tropical Disease Control, Ministry of Education, Sun Yat-Sen UniversityKey Laboratory of Tropical Disease Control, Ministry of Education, Sun Yat-Sen UniversityDepartment of Social and Environmental Medicine, Faculty of Tropical Medicine, Mahidol UniversityDepartment of Social and Environmental Medicine, Faculty of Tropical Medicine, Mahidol UniversityState Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Sciences, Hunan Normal UniversityDepartment of Social and Environmental Medicine, Faculty of Tropical Medicine, Mahidol UniversityKey Laboratory of Tropical Disease Control, Ministry of Education, Sun Yat-Sen UniversityAbstract Background Schistosoma mekongi is a human blood fluke causing schistosomiasis that threatens approximately 1.5 million humans in the world. Nonetheless, the limited available S. mekongi genomic resources have hindered understanding of its biology and parasite-host interactions for disease management and pathogen control. The aim of our study was to integrate multiple technologies to construct a high-quality chromosome-level assembly of the S. mekongi genome. Methods The reference genome for S. mekongi was generated through integrating Illumina, PacBio sequencing, 10 × Genomics linked-read sequencing, and high-throughput chromosome conformation capture (Hi-C) methods. In this study, we conducted de novo assembly, alignment, and gene prediction to assemble and annotate the genome. Comparative genomics allowed us to compare genomes across different species, shedding light on conserved regions and evolutionary relationships. Additionally, our transcriptomic analysis focused on genes associated with parasite-snail interactions in S. mekongi infection. We employed gene ontology (GO) enrichment analysis for functional annotation of these genes. Results In the present study, the S. mekongi genome was both assembled into 8 pseudochromosomes with a length of 404 Mb, with contig N50 and scaffold N50 lengths of 1168 kb and 46,759 kb, respectively. We detected that 43% of the genome consists of repeat sequences and predicted 9103 protein-coding genes. We also focused on proteases, particularly leishmanolysin-like metalloproteases (M8), which are crucial in the invasion of hosts by 12 flatworm species. Through phylogenetic analysis, it was discovered that the M8 gene exhibits lineage-specific amplification among the genus Schistosoma. Lineage-specific expansion of M8 was observed in blood flukes. Additionally, the results of the RNA-seq revealed that a mass of genes related to metabolic and biosynthetic processes were up-regulated, which might be beneficial for cercaria production. Conclusions This study delivers a high-quality, chromosome-scale reference genome of S. mekongi, enhancing our understanding of the divergence and evolution of Schistosoma. The molecular research conducted here also plays a pivotal role in drug discovery and vaccine development. Furthermore, our work greatly advances the understanding of host-parasite interactions, providing crucial insights for schistosomiasis intervention strategies. Graphical Abstracthttps://doi.org/10.1186/s40249-023-01160-6Schistosoma mekongiChromosome-scale genomeProteaseRNA-seq
spellingShingle Minyu Zhou
Lian Xu
Dahua Xu
Wen Chen
Jehangir Khan
Yue Hu
Hui Huang
Hang Wei
Yiqing Zhang
Phiraphol Chusongsang
Kanthi Tanasarnprasert
Xiang Hu
Yanin Limpanont
Zhiyue Lv
Chromosome-scale genome of the human blood fluke Schistosoma mekongi and its implications for public health
Infectious Diseases of Poverty
Schistosoma mekongi
Chromosome-scale genome
Protease
RNA-seq
title Chromosome-scale genome of the human blood fluke Schistosoma mekongi and its implications for public health
title_full Chromosome-scale genome of the human blood fluke Schistosoma mekongi and its implications for public health
title_fullStr Chromosome-scale genome of the human blood fluke Schistosoma mekongi and its implications for public health
title_full_unstemmed Chromosome-scale genome of the human blood fluke Schistosoma mekongi and its implications for public health
title_short Chromosome-scale genome of the human blood fluke Schistosoma mekongi and its implications for public health
title_sort chromosome scale genome of the human blood fluke schistosoma mekongi and its implications for public health
topic Schistosoma mekongi
Chromosome-scale genome
Protease
RNA-seq
url https://doi.org/10.1186/s40249-023-01160-6
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