Sex chromosome evolution in parasitic nematodes of humans

Foster, Jeremy M.; Grote, Alexandra; Mattick, John; Tracey, Alan S.; Tsai, Yu‐Chih; Chung, Matthew; Cotton, James A.; Clark, Tyson A.; Geber, Adam; Holroyd, Nancy; Korlach, Jonas; Li, Yichao; Libro, Silvia; Lustigman, Sara; Michalski, Michelle L.; Paulini, Michael; Rogers, Matthew B.; Teigen, Laura; Twaddle, Alan; Welch, Lonnie R.; Berriman, Matthew; Hotopp, Julie C. Dunning; Ghedin, Elodie

doi:10.1038/s41467-020-15654-6

Cited by 46 publications

(77 citation statements)

References 81 publications

(110 reference statements)

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“…The complete admixture of NigonD and NigonX loci in these spiruromorph X chromosome domains suggests ancient fusion, especially since the B. malayi and O. volvulus genomes are largely collinear both within non-fused chromosomes and within fused chromosome blocks (Foster et al, 2020). Because NigonX and NigonD are present, intermixed, in the X chromosomes of both Ascaridomorpha and Spiruromorpha, the NigonD-NigonX fusion could be ancestral to Spirurina.…”

Section: Resultsmentioning

confidence: 99%

“…Foster et al . (Foster et al, 2020) have argued, based on the presence on spiruromorph X chromosomes of NigonD loci (i.e loci mapping to C. elegans chromosome IV) that NigonD was the ancestral sex determination element of all Rhabditida, and that sex determination function transitioned to NigonX only later in rhabditid evolution. Foster et al .…”

Section: Discussionmentioning

confidence: 99%

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A telomere to telomere assembly ofOscheius tipulaeand the evolution of rhabditid nematode chromosomes

Rosa

Thomson

Trivedi

et al. 2020

Preprint

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Eukaryotic chromosomes have phylogenetic persistence. In many taxa, the number of chromosomes is related to the number of centromeres. However, in some groups, such as rhabditid nematodes, centromeric function is distributed across multiple sites on each chromosome. These holocentric chromosomes might, a priori, be expected to be permissive of large-scale chromosomal rearrangement, as chromosomal fragments could still partition correctly and fusions would not generate lethal conflict between multiple centromeres. Here, we explore the phylogenetic stability of nematode chromosomes using a new telomere-to-telomere assembly of the rhabditine nematode Oscheius tipulae generated from nanopore long reads. The 60 Mb O. tipulae genome is resolved into six chromosomal molecules. We find evidence of specific chromatin diminution at all telomeres. Comparing this chromosomal O. tipulae assembly with chromosomal assemblies of diverse rhabditid nematodes we identify seven ancestral chromosomal elements (Nigon elements), and present a model for the evolution of nematode chromosomes through rearrangement and fusion of these elements. We identify frequent fusion events involving NigonX, the element associated with the rhabditid X chromosome, and thus sex-chromosome associated gene sets differ markedly between species. Despite the karyotypic stability, gene order within chromosomes defined by Nigon elements is not conserved. Our model for nematode chromosome evolution provides a platform for investigation of the tensions between local genome rearrangement and karyotypic evolution in generating extant genome architectures.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

A telomere to telomere assembly ofOscheius tipulaeand the evolution of rhabditid nematode chromosomes

Rosa

Thomson

Trivedi

et al. 2020

Preprint

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“…Parasitic helminths are a diverse group of organisms for which significant efforts have been made to develop genomic resources 10 . For some species [11][12][13][14][15][16] , high-quality near-complete assemblies have been achieved using multiple complementary sequencing and mapping technologies, and usually with extensive manual improvement. Similar quality assemblies for a few other species are available from WormBase ParaSite 17 , but await formal description in the peer-reviewed literature.…”

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confidence: 99%

Genomic and transcriptomic variation defines the chromosome-scale assembly of Haemonchus contortus, a model gastrointestinal worm

et al. 2020

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Haemonchus contortus is a globally distributed and economically important gastrointestinal pathogen of small ruminants and has become a key nematode model for studying anthelmintic resistance and other parasite-specific traits among a wider group of parasites including major human pathogens. Here, we report using PacBio long-read and OpGen and 10X Genomics long-molecule methods to generate a highly contiguous 283.4 Mbp chromosome-scale genome assembly including a resolved sex chromosome for the MHco3(ISE).N1 isolate. We show a remarkable pattern of conservation of chromosome content with Caenorhabditis elegans, but almost no conservation of gene order. Short and long-read transcriptome sequencing allowed us to define coordinated transcriptional regulation throughout the parasite’s life cycle and refine our understanding of cis- and trans-splicing. Finally, we provide a comprehensive picture of chromosome-wide genetic diversity both within a single isolate and globally. These data provide a high-quality comparison for understanding the evolution and genomics of Caenorhabditis and other nematodes and extend the experimental tractability of this model parasitic nematode in understanding helminth biology, drug discovery and vaccine development, as well as important adaptive traits such as drug resistance.

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“…Here, we describe the first metabolic reconstruction and constraint-based models of B. malayi . Using the high quality genome sequence of B. malayi ( Ghedin et al, 2007 ; Foster et al, 2020 ), we first generated a network representation of the parasite’s metabolic capabilities. We integrated previously published stage-specific transcriptome datasets for both B. malayi and its Wolbachia endosymbiont ( Grote et al, 2017 ).…”

Section: Introductionmentioning

confidence: 99%

Modeling the metabolic interplay between a parasitic worm and its bacterial endosymbiont allows the identification of novel drug targets

Curran

Grote

Nursimulu

et al. 2020

eLife

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The filarial nematode Brugia malayi represents a leading cause of disability in the developing world, causing lymphatic filariasis in nearly 40 million people. Currently available drugs are not well-suited to mass drug administration efforts, so new treatments are urgently required. One potential vulnerability is the endosymbiotic bacteria Wolbachia—present in many filariae—which is vital to the worm. Genome scale metabolic networks have been used to study prokaryotes and protists and have proven valuable in identifying therapeutic targets, but have only been applied to multicellular eukaryotic organisms more recently. Here, we present iDC625, the first compartmentalized metabolic model of a parasitic worm. We used this model to show how metabolic pathway usage allows the worm to adapt to different environments, and predict a set of 102 reactions essential to the survival of B. malayi. We validated three of those reactions with drug tests and demonstrated novel antifilarial properties for all three compounds.

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Sex chromosome evolution in parasitic nematodes of humans

Cited by 46 publications

References 81 publications

A telomere to telomere assembly ofOscheius tipulaeand the evolution of rhabditid nematode chromosomes

A telomere to telomere assembly ofOscheius tipulaeand the evolution of rhabditid nematode chromosomes

Genomic and transcriptomic variation defines the chromosome-scale assembly of Haemonchus contortus, a model gastrointestinal worm

Modeling the metabolic interplay between a parasitic worm and its bacterial endosymbiont allows the identification of novel drug targets

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