Comparative genomics and phylogenomics of Trichostrongyloidea mitochondria reveal insights for molecular diagnosis and evolutionary biology of nematode worms

Santos, Lucíola Licínio de Castro Paixão; Prosdocimi, Francisco; Lima, Nicholas Costa Barroso; Costa, Igor Rodrigues da; Cardoso, Danielle Cunha; Drummond, Marcela Gonçalves; Brasil, Bruno S. A. F.; Bastianetto, Eduardo; Oliveira, Denise Aparecida Andrade de

doi:10.1016/j.genrep.2017.09.002

Cited by 2 publications

(9 citation statements)

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“…The characteristics associated with the secondary structures predicted for most tRNA genes include: a 7–8 bp acceptor stem (amino-acyl arm), a 5 bp anticodon stem and a T/U residue preceding. With the exception of T. spiralis (Lavrov and Brown, 2001 ), these characteristics are consistent with all previously published mt genomes for the Trichostrongyloidea (dos Santos et al, 2017 ) and Rhabditida [ C. elegans (Blaxter et al, 1998 )].…”

Section: Resultssupporting

confidence: 88%

“…The NZ_Hco_NP and NZ_Teci_NP mt genomes are 14,001 and 14,081 bp in length, respectively ( Figure 1 ) and are thus within the expected range. The reported mt genomes differ in size by ~16–54 bp than other H. contortus and T. circumcincta characterized strains, except for the 13.7 kb H. placei MHpl1 mt genome (dos Santos et al, 2017 ). The size discrepancies among the different strains primarily relate to A+T-rich control region expansions and longer non-coding regions between numerous transfer RNA genes.…”

Section: Resultsmentioning

confidence: 99%

“…The reconstruction of partial and complete mitochondrial genomes is becoming increasingly cost-effective with the advent of next-generation sequencing technology and recent advances in molecular parasitology tools, in particular for species identification and population genetics studies (Hu and Gasser, 2006 ; Jex et al, 2009 ). Despite these advances, only 12 species of Trichostrongyloid mt genomes are currently available in GenBank with only half of these represented by multiple strains (dos Santos et al, 2017 ). For these reasons, the complete mt genomes of New Zealand H. contortus NZ_Hco_NP (Palevich et al, 2019a , c ) and T. circumcincta NZ_Teci_NP (Choi et al, 2017 ; Palevich et al, 2019b ) field strains were sequenced and compared in detail to investigate the strain-level genetic differences of these two sibling Trichostrongyloidea species.…”

Section: Resultsmentioning

confidence: 99%

“…Both mt genomes are predicted to use the complete termination codons TAA. Nevertheless, cox 2 had a TAG translation termination codon similar to nad 3 of H. placei where not all termination codons were complete stop codons, typical of nematodes (Jex et al, 2008 ; dos Santos et al, 2017 ).…”

Section: Resultsmentioning

confidence: 99%

“…For example, regarding H. placei and H. contortus mt genomes, a divergence in nuclear ITS-2 rDNA between these two species has previously been reported as 1.3% (Stevenson et al, 1995 ). Whereas, differences between nucleotide sequences of H. placei and H. contortus mt genome PCGs ranged between 10 and 20% (Gasser et al, 2006 ; dos Santos et al, 2017 ). Taken together, our findings are in agreement with previous reports suggesting the use of the most conserved mt cox genes for investigating systematics and speciation in nematodes (Hu et al, 2004 ; Hu and Gasser, 2006 ; Zarowiecki et al, 2007 ), while the variation observed in nad mt genes would be more appropriate for population genetics studies (Jex et al, 2009 ).…”

Section: Resultsmentioning

confidence: 99%

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Characterization of the Complete Mitochondrial Genomes of Two Sibling Species of Parasitic Roundworms, Haemonchus contortus and Teladorsagia circumcincta

et al. 2020

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Haemonchus contortus and Teladorsagia circumcincta are among the two most pathogenic internal parasitic nematodes infecting small ruminants, such as sheep and goats, and are a global animal health issue. Accurate identification and delineation of Haemonchidae species is essential for development of diagnostic and control strategies with high resolution for Trichostrongyloidea infection in ruminants. Here, we describe in detail and compare the complete mitochondrial (mt) genomes of the New Zealand H. contortus and T. circumcincta field strains to improve our understanding of species- and strain-level evolution in these closely related roundworms. In the present study, we performed extensive comparative bioinformatics analyses on the recently sequenced complete mt genomes of the New Zealand H. contortus NZ_Hco_NP and T. circumcincta NZ_Teci_NP field strains. Amino acid sequences inferred from individual genes of each of the two mt genomes were compared, concatenated and subjected to phylogenetic analysis using Bayesian inference (BI), Maximum Likelihood (ML), and Maximum Parsimony (MP). The AT-rich mt genomes of H. contortus NZ_Hco_NP and T. circumcincta NZ_Teci_NP are 14,001 bp (A+T content of 77.4%) and 14,081 bp (A+T content of 77.3%) in size, respectively. All 36 of the typical nematode mt genes are transcribed in the forward direction in both species and comprise of 12 protein-encoding genes (PCGs), 2 ribosomal RNA ( rrn ) genes, and 22 transfer RNA ( trn ) genes. The secondary structures for the 22 trn genes and two rrn genes differ between H. contortus NZ_Hco_NP and T. circumcincta NZ_Teci_NP, however the gene arrangements of both are consistent with other Trichostrongylidea sequenced to date. Comparative analyses of the complete mitochondrial nucleotide sequences, PCGs, A+T rich and non-coding repeat regions of H. contortus NZ_Hco_NP and T. circumcincta NZ_Teci_NP further reinforces the high levels of diversity and gene flow observed among Trichostrongylidea, and supports their potential as ideal markers for strain-level identification from different hosts and geographical regions with high resolution for future studies. The complete mt genomes of H. contortus NZ_Hco_NP and T. circumcincta NZ_Teci_NP presented here provide useful novel markers for further studies of the meta-population connectivity and the genetic mechanisms driving evolution in nematode species.

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Section: Resultssupporting

confidence: 88%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

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Characterization of the Complete Mitochondrial Genomes of Two Sibling Species of Parasitic Roundworms, Haemonchus contortus and Teladorsagia circumcincta

et al. 2020

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The identification of small molecule inhibitors with anthelmintic activities that target conserved proteins among ruminant gastrointestinal nematodes

Jung,

Zarlenga,

Martin

et al. 2024

mBio

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Gastrointestinal nematode (GIN) infections are a major concern for the ruminant industry worldwide and result in significant production losses. Naturally occurring polyparasitism and increasing drug resistance that potentiate disease outcomes are observed among the most prevalent GINs of veterinary importance. Within the five major taxonomic clades, clade Va represents a group of GINs that predominantly affect the abomasum or small intestine of ruminants. However, the development of effective broad-spectrum anthelmintics against ruminant clade Va GINs has been challenged by a lack of comprehensive druggable genome resources. Here, we first assembled draft genomes for three clade Va species ( Cooperia oncophora , Trichostrongylus colubriformis , and Ostertagia ostertagi ) and compared them with closely related ruminant GINs. Genome-wide phylogenetic reconstruction showed a relationship among ruminant GINs structured by taxonomic classification. Orthogroup (OG) inference and functional enrichment analyses identified 220 clade Va-specific and Va-conserved OGs, enriched for functions related to cell cycle and cellular senescence. Further transcriptomic analysis identified 61 taxonomically and functionally conserved clade Va OGs that may function as drug targets for new broad-spectrum anthelmintics. Chemogenomic screening identified 11 compounds targeting homologs of these OGs, thus having potential anthelmintic activity. In in vitro phenotypic assays, three kinase inhibitors (digitoxigenin, K-252a, and staurosporine) exhibited broad-spectrum anthelmintic activities against clade Va GINs by obstructing the motility of exsheathed L3 (xL3) or molting of xL3 to L4. These results demonstrate valuable applications of the new ruminant GIN genomes in gaining better insights into their life cycles and offer a contemporary approach to discovering the next generation of anthelmintics. IMPORTANCE Gastrointestinal nematode (GIN) infections in ruminants are caused by parasites that inhibit normal function in the digestive tract of cattle, sheep, and goats, thereby causing morbidity and mortality. Coinfection and increasing drug resistance to current therapeutic agents will continue to worsen disease outcomes and impose significant production losses on domestic livestock producers worldwide. In combination with ongoing therapeutic efforts, advancing the discovery of new drugs with novel modes of action is critical for better controlling GIN infections. The significance of this study is in assembling and characterizing new GIN genomes of Cooperia oncophora , Ostertagia ostertagi, and Trichostrongylus colubriformis for facilitating a multi-omics approach to identify novel, biologically conserved drug targets for five major GINs of veterinary importance. With this information, we were then able to demonstrate the potential of commercially available compounds as new anthelmintics.

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Comparative genomics and phylogenomics of Trichostrongyloidea mitochondria reveal insights for molecular diagnosis and evolutionary biology of nematode worms

Cited by 2 publications

References 53 publications

Characterization of the Complete Mitochondrial Genomes of Two Sibling Species of Parasitic Roundworms, Haemonchus contortus and Teladorsagia circumcincta

Characterization of the Complete Mitochondrial Genomes of Two Sibling Species of Parasitic Roundworms, Haemonchus contortus and Teladorsagia circumcincta

The identification of small molecule inhibitors with anthelmintic activities that target conserved proteins among ruminant gastrointestinal nematodes

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