Investigating hookworm genomes by comparative analysis of two Ancylostoma species

Mitreva, Makedonka; McCarter, James P.; Arasu, Prema; Hawdon, John M.; Martin, John; Dante, Mike; Wylie, Todd; Xu, Jian; Stajich, Jason E.; Kapulkin, Wadim; Clifton, Sandra W.; Waterston, Robert H.; Wilson, Richard K.

doi:10.1186/1471-2164-6-58

Cited by 49 publications

(48 citation statements)

References 72 publications

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“…Peptides predicted to be species-specific were significantly shorter in length, on average, than peptides with matches in other species (Additional file 2: Figure S1). This explains in part, the perceived sequence specificity in lieu of finding homologs as reported previously [17]. …”

Section: Resultssupporting

confidence: 71%

Transcriptome analyses reveal protein and domain families that delineate stage-related development in the economically important parasitic nematodes, Ostertagia ostertagi and Cooperia oncophora

Heizer¹,

Zarlenga

Rosa³

et al. 2013

BMC Genomics

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BackgroundCooperia oncophora and Ostertagia ostertagi are among the most important gastrointestinal nematodes of cattle worldwide. The economic losses caused by these parasites are on the order of hundreds of millions of dollars per year. Conventional treatment of these parasites is through anthelmintic drugs; however, as resistance to anthelmintics increases, overall effectiveness has begun decreasing. New methods of control and alternative drug targets are necessary. In-depth analysis of transcriptomic data can help provide these targets.ResultsThe assembly of 8.7 million and 11 million sequences from C. oncophora and O. ostertagi, respectively, resulted in 29,900 and 34,792 transcripts. Among these, 69% and 73% of the predicted peptides encoded by C. oncophora and O. ostertagi had homologues in other nematodes. Approximately 21% and 24% were constitutively expressed in both species, respectively; however, the numbers of transcripts that were stage specific were much smaller (~1% of the transcripts expressed in a stage). Approximately 21% of the transcripts in C. oncophora and 22% in O. ostertagi were up-regulated in a particular stage. Functional molecular signatures were detected for 46% and 35% of the transcripts in C. oncophora and O. ostertagi, respectively. More in-depth examinations of the most prevalent domains led to knowledge of gene expression changes between the free-living (egg, L1, L2 and L3 sheathed) and parasitic (L3 exsheathed, L4, and adult) stages. Domains previously implicated in growth and development such as chromo domains and the MADF domain tended to dominate in the free-living stages. In contrast, domains potentially involved in feeding such as the zinc finger and CAP domains dominated in the parasitic stages. Pathway analyses showed significant associations between life-cycle stages and peptides involved in energy metabolism in O. ostertagi whereas metabolism of cofactors and vitamins were specifically up-regulated in the parasitic stages of C. oncophora. Substantial differences were observed also between Gene Ontology terms associated with free-living and parasitic stages.ConclusionsThis study characterized transcriptomes from multiple life stages from both C. oncophora and O. ostertagi. These data represent an important resource for studying these parasites. The results of this study show distinct differences in the genes involved in the free-living and parasitic life cycle stages. The data produced will enable better annotation of the upcoming genome sequences and will allow future comparative analyses of the biology, evolution and adaptation to parasitism in nematodes.

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Section: Resultssupporting

confidence: 71%

Transcriptome analyses reveal protein and domain families that delineate stage-related development in the economically important parasitic nematodes, Ostertagia ostertagi and Cooperia oncophora

Heizer¹,

Zarlenga

Rosa³

et al. 2013

BMC Genomics

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“…To identify bandit -like sequences in related hookworm species, the bandit transposase (342 amino acids) was queried against 4,953 polypeptides from A. ceylanicum [8] and 2,328 polypeptides from N. americanus [21]. Only the best homologous sequence is reported, including the identity and similarity values for the longest high-scoring segment pair (HSP) in each subject.…”

Section: Methodsmentioning

confidence: 99%

The bandit, a New DNA Transposon from a Hookworm—Possible Horizontal Genetic Transfer between Host and Parasite

et al. 2007

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BackgroundAn enhanced understanding of the hookworm genome and its resident mobile genetic elements should facilitate understanding of the genome evolution, genome organization, possibly host-parasite co-evolution and horizontal gene transfer, and from a practical perspective, development of transposon-based transgenesis for hookworms and other parasitic nematodes.Methodology/Principal FindingsA novel mariner-like element (MLE) was characterized from the genome of the dog hookworm, Ancylostoma caninum, and termed bandit. The consensus sequence of the bandit transposon was 1,285 base pairs (bp) in length. The new transposon was flanked by perfect terminal inverted repeats of 32 nucleotides in length with a common target site duplication TA, and it encoded an open reading frame (ORF) of 342 deduced amino acid residues. Phylogenetic comparisons confirmed that the ORF encoded a mariner-like transposase, which included conserved catalytic domains, and that the bandit transposon belonged to the cecropia subfamily of MLEs. The phylogenetic analysis also indicated that the Hsmar1 transposon from humans was the closest known relative of bandit, and that bandit and Hsmar1 constituted a clade discrete from the Tc1 subfamily of MLEs from the nematode Caenorhabditis elegans. Moreover, homology models based on the crystal structure of Mos1 from Drosophila mauritiana revealed closer identity in active site residues of the catalytic domain including Ser281, Lys289 and Asp293 between bandit and Hsmar1 than between Mos1 and either bandit or Hsmar1. The entire bandit ORF was amplified from genomic DNA and a fragment of the bandit ORF was amplified from RNA, indicating that this transposon is actively transcribed in hookworms.Conclusions/SignificanceA mariner-like transposon termed bandit has colonized the genome of the hookworm A. caninum. Although MLEs exhibit a broad host range, and are identified in other nematodes, the closest phylogenetic relative of bandit is the Hsmar1 element of humans. This surprising finding suggests that bandit was transferred horizontally between hookworm parasites and their mammalian hosts.

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“…We therefore first compared the generated sequences to genes known to exist in the model organism C. elegans (Table 2.). In addition to the two over-represented factors mentioned above ( If any of these conserved factors were later reported by others in descriptions of material from our libraries (Mitreva et al 2005), we do not here repeat analysis of relevant genes .…”

Section: Resultsmentioning

confidence: 99%

“…However we have attempted to retrospectively identify which of the above conserved factors are most prevalent when sampled with the larger SL1-cDNA set (Mitreva et al 2005). Based on the data included in Table 2, Table 2 lists additional homologues of C. elegans genes derived from clones from the SL1-capped cDNA libraries we provided, but strikingly absent from uncapped libraries provided by other collaborators.…”

Section: Resultsmentioning

confidence: 99%

Recombinant DNA resources for the comparative genomics ofAncylostoma ceylanicum

Wj¹,

Magalska²,

Janecka³

et al. 2016

Preprint

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We describe the construction and initial characterization of genomic resources (a set of recombinant DNA libraries, representing in total over 90, 000 independent plasmid clones), originating from the genome of a hamster adapted hookworm, Ancylostoma ceylanicum. First, with the improved methodology, we generated sets of SL1 (5'linker -GGTTAATTACCCAAGTTTGAG), and captured cDNAs from two different hookworm developmental stages: pre-infective L3 and parasitic adults. Second, we constructed a small insert (2-10kb) genomic library. Third, we generated a Bacterial Artificial Chromosome library (30-60kb). To evaluate the quality of our libraries we characterized sequence tags on randomly chosen clones and with first pass screening we generated almost a hundred novel hookworm sequence tags. The sequence tags detected two broad classes of genes: i. conserved nematode genes and ii. putative hookworm-specific proteins. Importantly, some of the identified genes encode proteins of general interest including potential targets for hookworm control. Additionally, we identified a syntenic region in the mitochondrial genome, where the gene order is shared between the freeliving nematode C. elegans and A. ceylanicum. Our results validate the use of recombinant DNA resources for comparative genomics of nematodes, including the freeliving genetic model organism C. elegans and closely related parasitic species. We discuss the potential and relevance of Ancylostoma ceylanicum data and resources generated by the recombinant DNA approach.

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Investigating hookworm genomes by comparative analysis of two Ancylostoma species

Abstract: Background: Hookworms, infecting over one billion people, are the mostly closely related major human parasites to the model nematode Caenorhabditis elegans. Applying genomics techniques to these species, we analyzed 3,840 and 3,149 genes from Ancylostoma caninum and A. ceylanicum.

Cited by 49 publications

References 72 publications

Transcriptome analyses reveal protein and domain families that delineate stage-related development in the economically important parasitic nematodes, Ostertagia ostertagi and Cooperia oncophora

Transcriptome analyses reveal protein and domain families that delineate stage-related development in the economically important parasitic nematodes, Ostertagia ostertagi and Cooperia oncophora

The bandit, a New DNA Transposon from a Hookworm—Possible Horizontal Genetic Transfer between Host and Parasite

Recombinant DNA resources for the comparative genomics ofAncylostoma ceylanicum

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