Genome of the Giant Panda Roundworm Illuminates Its Host Shift and Parasitic Adaptation

Xie, Yue; Wang, Sen; Wu, Shizhou; Gao, Shenghan; Meng, Qingshu; Wang, Chengdong; Lan, Jingchao; Luo, Li; Zhou, Xuan; Xu, Jing; Gu, Xiaobin; He, Ran; Yang, Zijiang; Peng, Xuerong; Hu, Songnian; Yang, Guangyou

doi:10.1016/j.gpb.2021.08.002

Cited by 15 publications

(8 citation statements)

References 65 publications

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“…Positive selection was considered the driving force of host adaptation in the parasite genome (Xie et al., 2021). Therefore, we identified the positively selected genes in the S. scabiei genome.…”

Section: Discussionmentioning

confidence: 99%

Comparative genomics of Sarcoptes scabiei provide new insights into adaptation to permanent parasitism and within‐host species divergence

Wang

et al. 2022

Transbounding Emerging Dis

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Sarcoptes scabiei is the causative agent of a highly contagious skin disease in humans and more than 100 mammals. Here, we reported the first chromosome‐level reference genome of S. scabiei isolated from rabbits, with a contig N50 size of 5.92 Mb, a total assembled length of 57.30 Mb, ∼12.65% repetitive sequences and 9333 predicted protein‐coding genes. The phylogenetic tree based on 1338 shared high‐confidence single‐copy orthologous genes estimated that the mammalian ectoparasite S. scabiei and the plant‐feeding mite Tetranychus urticae separated ∼340 million years ago. Both neighbour‐joining tree and principal component analysis of 20 mite populations isolated from four hosts (humans, pigs, dogs and rabbits) distributed in three countries (China, Australia and the USA) consistently supported genetic subdivisions according to host species rather than geographical location. The demographic history of S. scabiei reconstructed by multiple sequentially Markovian coalescent analysis suggested that S. scabiei isolated from rabbits, humans, dogs and pigs diverged ∼5000 years ago. Investigation of the homeobox (Hox) genes revealed that S. scabiei contains 8 of 10 canonical Hox genes that are present in the arthropod ancestor, and the absence of the Abd‐A gene may correlate with the long gap between their front and back legs. Comparative genomics demonstrated that genes specific to scabies mites were mainly enriched in nutrition digestive systems, whereas genes in the families that involved detoxification (cytochrome P450, carboxyl/cholinesterases and the ATP‐binding cassette transporter C group) were extremely contracted compared with that of other mites analysed in this study. Selective sweep analysis of mite populations from various pairs of two out of the four host species revealed that the strongest selective sweep signals were mainly enriched in cysteine‐type peptidase activity and apoptosis. The results provided clues for the mechanisms of S. scabiei adaptation to a permanent parasitic lifestyle and knowledge that would enable further control of this highly contagious skin disease.

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Section: Discussionmentioning

confidence: 99%

Comparative genomics of Sarcoptes scabiei provide new insights into adaptation to permanent parasitism and within‐host species divergence

Wang

et al. 2022

Transbounding Emerging Dis

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“…It is well known that parasite excretory–secretory (ES) proteins function as bioactive molecules that directly interact with the host immune system. In previous study, we successfully predicted and annotated the secretory proteome by using the whole-genome and transcriptome data of B. schroederi [ 38 ]. At the same time, we found that many of the previously reported proteases and protease inhibitors involved in the parasite–host interaction were also abundant in the secretory proteome of B. schroederi .…”

Section: Discussionmentioning

confidence: 99%

A novel cysteine protease inhibitor in Baylisascaris schroederi migratory larvae regulates inflammasome activation through the TLR4–ROS–NLRP3 pathway

Xie

et al. 2022

Parasites Vectors

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Background Giant pandas (Ailuropoda melanoleuca) are the obligate host of the parasitic roundworm Baylisascaris schroederi. The infection of giant pandas with B. schroederi is very common. At present, little is known about the mechanism of immune interaction between B. schroederi and the host. As an important component of innate immunity, the NOD-like receptor 3 (NLRP3) inflammasome plays an important role in host immune response and the occurrence and development of infectious diseases. Methods We analyzed the regulation of NLRP3 inflammasome activation in monocyte-derived macrophages (MDMs) by the recombinant B. schroederi migratory larvae cysteine protease inhibitor rBsCPI-1, knowing from a previous study that the CPI-1 is highly expressed in B. schroederi migratory larvae. We first determined the effects of rBsCPI-1 and excretory–secretory products of B. schroederi migratory larvae on cell proliferation using the CCK-8 and LDH release assays. We then analyzed NLRP3 inflammasome activation, pyroptosis and pro-inflammatory cytokine release by quantitative-PCR, western blotting and enzyme-linked immunosorbent assay. The signaling pathway of rBsCPI-1 to activate NLRP3 inflammasomes was analyzed in activation and inhibition experiments. Finally, the effects of rBsCPI-1 on inflammasome activation in mice immunized with rBsCPI-1 were analyzed. Results The activation and inhibition experiments revealed that rBsCPI-1 induced inflammasome activation through the TLR4–ROS–NLRP3 signaling pathway, with reactive oxygen species (ROS) not only functioning as an activator of the NLRP3 inflammasome, but also an activation product of the NLRP3 inflammasome. rBsCPI-1 promoted the activation and assembly of the NLRP3 inflammasome, which further converted the pro-inflammatory cytokines interleukin (IL)-1β and IL-18 into mature active forms. At the same time, caspase-1 cleaved gasdermin D to trigger cell pyroptosis. The results of animal immunization experiments further confirmed that rBsCPI-1 could induce the activation of the NLRP3 inflammasome. Conclusions rBsCPI-1 activates the inflammasome through the TLR4–ROS–NLRP3 signaling pathway and further induces the pyroptosis of MDMs and release of pro-inflammatory factors IL-1β and IL-18, thus promoting the occurrence and development of the inflammatory response in the host. Graphical abstract

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“…20-22 Recently, PDE has also been discovered in other free-living nematodes from Clade V, including other Oscheius species and some Caenorhabditis and Auanema species [Gonzalez de la Rosa, Stevens, Pires-daSilva and Blaxter, personal communications], and Mesorhabditis . 50 Other parasitic nematodes (Clade III Parascaris and Toxocara , 21 Baylisascaris , 51 and Clade IV Strongyloides 52 ) also exhibit DNA break and sequence loss, illustrating the broad phylogenetic distribution of PDE in nematodes. However, other well-studied nematodes, including C. elegans , do not undergo PDE.…”

Section: Discussionmentioning

confidence: 99%

The Nematode Oscheius tipulae as A Genetic Model for Programmed DNA Elimination

Dockendorff

Estrem

Reed

et al. 2022

Preprint

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Programmed DNA elimination (PDE) is a notable exception to the paradigm of genome integrity. In metazoa, PDE often occurs during early embryogenesis, coincident with germline to somatic cell differentiation. During PDE, portions of genomic DNA are lost, resulting in reduced somatic genomes. Recent studies have described the sequences lost and chromosome behavior in metazoa. However, a system for studying the mechanisms and consequences of PDE in metazoa is lacking. Here, we established a functional and genetic model for PDE in the free-living nematode Oscheius tipulae, a member of the Rhabditidae family, which includes Caenorhabditis elegans. O. tipulae was recently suggested to eliminate DNA. Using staged embryos, we show that O. tipulae PDE occurs during embryogenesis at the 2-16 cell stages, similar to the human/pig parasitic nematode Ascaris. We identified a conserved motif, named Sequence For Elimination (SFE), for all 12 break sites on the six chromosomes at the junction of retained and eliminated DNA. SFE mutants exhibit a "fail-to-eliminate" phenotype only at the modified sites. END-seq revealed that breaks can occur at multiple positions within the SFE, with extensive end resection followed by telomere addition to both retained and eliminated ends. We identified through END-seq in the wild-type embryos, genome sequencing of SFE mutants, and comparative genomics of 23 wild isolates a large number of functional SFEs at the chromosome ends. We suggest these alternative SFEs provide flexibility in the sequences eliminated and a fail-safe mechanism for PDE. These studies establish O. tipulae as a new, attractive model to study the mechanisms and consequences of PDE in a metazoan.

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Genome of the Giant Panda Roundworm Illuminates Its Host Shift and Parasitic Adaptation

Cited by 15 publications

References 65 publications

Comparative genomics of Sarcoptes scabiei provide new insights into adaptation to permanent parasitism and within‐host species divergence

Comparative genomics of Sarcoptes scabiei provide new insights into adaptation to permanent parasitism and within‐host species divergence

A novel cysteine protease inhibitor in Baylisascaris schroederi migratory larvae regulates inflammasome activation through the TLR4–ROS–NLRP3 pathway

The Nematode Oscheius tipulae as A Genetic Model for Programmed DNA Elimination

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