Foster, J. M. | bioRxiv Science

bioRxiv2024

Population genomics reveals an ancient origin of heartworms in canids

Heartworms (Dirofilaria immitis) are parasitic nematodes that cause significant cardiopulmonary-associated morbidity and mortality in canids worldwide. The global spread of heartworms is believed to have occurred alongside the dispersal of domesticated dogs. To test this theory, we analysed the genomes of 127 specimens collected from mammalian carnivore hosts across four continents. Here we show distinct genetic differences between heartworms from different continents, indicating a more ancient dispersal in canid hosts than previously recognised. Using admixture analyses, we find an Asian origin for Australian heartworms, consistent with the arrival of dingoes thousands of years ago. Finally, the genetic relatedness between European and Central American heartworms suggests that modern dispersal, likely associated with human colonisation of the Americas by Europeans, occurred with domesticated dogs. This work sheds light on the population dynamics and deep evolutionary history of a globally widespread parasite of veterinary significance.

evolutionary biology↗

bioRxiv2023

A novel family of sugar-specific phosphodiesterases that remove zwitterionic modifications of N-acetylglucosamine

The zwitterions phosphorylcholine (PC) and phosphoethanolamine (PE) are often found esterified to certain sugars in polysaccharides and glycoconjugates in a wide range of biological species. One such modification involves PC attachment to the 6-carbon of N-acetylglucosamine (GlcNAc-6-PC) in N-glycans and glycosphingolipids (GSLs) of parasitic nematodes, a modification that helps the parasite evade host immunity. Knowledge of enzymes involved in the synthesis and degradation of PC and PE modifications is limited. More detailed studies on such enzymes would contribute to a better understanding of the function of PC modifications and have potential application in the structural analysis of zwitterion-modified glycans. In this study, we used functional metagenomic screening to identify phosphodiesterases encoded in a human fecal DNA fosmid library that remove PC from GlcNAc-6-PC. A novel bacterial phosphodiesterase was identified and biochemically characterized. This enzyme (termed GlcNAc-PDase) shows remarkable substrate preference for GlcNAc-6-PC and GlcNAc-6-PE, with little or no activity on other zwitterion-modified hexoses. The identified GlcNAc-PDase protein sequence is a member of the large endonuclease/exonuclease/phosphatase (EEP) superfamily where it defines a distinct subfamily of related sequences of previously unknown function, mostly from Clostridium bacteria species. Finally, we demonstrate use of GlcNAc-PDase to confirm the presence of GlcNAc-6-PC in N-glycans and GSLs of the parasitic nematode Brugia malayi in a glycoanalytical workflow.

biochemistry↗

bioRxiv2020

Diminutive, degraded but dissimilar: Wolbachia genomes from filarial nematodes do not conform to a single paradigm

Wolbachia are alpha-proteobacteria symbionts infecting a large range of arthropod species and two different families of nematodes. Interestingly, these endosymbionts are able to induce diverse phenotypes in their hosts: they are reproductive parasites within many arthropods, nutritional mutualists within some insects and obligate mutualists within their filarial nematode hosts. Defining Wolbachia "species" is controversial and so they are commonly classified into 16 different phylogenetic lineages, termed supergroups, named A to S. However, available genomic data remains limited and not representative of the full Wolbachia diversity; indeed, of the 24 complete genomes and 55 draft genomes of Wolbachia available to date, 84% belong to supergroups A and B, exclusively composed of Wolbachia from arthropods. For the current study, we took advantage of a recently developed DNA enrichment method to produce four complete genomes and two draft genomes of Wolbachia from filarial nematodes. Two complete genomes, wCtub and wDcau, are the smallest Wolbachia genomes sequenced to date (863,988bp and 863,427bp, respectively), as well as the first genomes representing supergroup J. These genomes confirm the validity of this supergroup, a controversial clade due to weaknesses of the multi-locus system typing (MLST) approach. We also produced the first draft Wolbachia genome from a supergroup F filarial nematode representative (wMhie), two genomes from supergroup D (wLsig and wLbra) and the complete genome of wDimm from supergroup C. Our new data confirm the paradigm of smaller Wolbachia genomes from filarial nematodes containing low levels of transposable elements and the absence of intact bacteriophage sequences, unlike many Wolbachia from arthropods, where both are more abundant. However, we observe differences among the Wolbachia genomes from filarial nematodes: no global co-evolutionary pattern, strong synteny between supergroup C and supergroup J Wolbachia, and more transposable elements observed in supergroup D Wolbachia compared to the other supergroups. Metabolic pathway analysis indicates several highly conserved pathways (haem and nucleotide biosynthesis for example) as opposed to more variable pathways, such as vitamin B biosynthesis, which might be specific to certain host-symbiont associations. Overall, there appears to be no single Wolbachia- filarial nematode pattern of co-evolution or symbiotic relationship. Graphical abstract O_FIG_DISPLAY_L [Figure 1] M_FIG_DISPLAY C_FIG_DISPLAY RepositoriesData generated are available in GenBank: BioProject PRJNA593581; BioSample SAMN13482485 for wLsig, Wolbachia endosymbiont of Litomosoides sigmodontis (genome: CP046577); Biosample SAMN15190311 for the nematode host Litomosoides sigmodontis (genome: JABVXW000000000); BioSample SAMN13482488 for wDimm, Wolbachia endosymbiont of Dirofilaria (D.) immitis (genome: CP046578); Biosample SAMN15190314 for the nematode host Dirofilaria (D.) immitis (genome: JABVXT000000000); BioSample SAMN13482046 for wCtub, Wolbachia endosymbiont of Cruorifilaria tuberocauda (genome: CP046579); Biosample SAMN15190313 for the nematode host Cruorifilaria tuberocauda (genome: JABVXU000000000); BioSample SAMN13482057 for wDcau, Wolbachia endosymbiont of Dipetalonema caudispina (genome: CP046580); Biosample SAMN15190312 for the nematode host Dipetalonema caudispina (genome: JABVXV000000000); BioSample SAMN13482459 for wLbra, Wolbachia endosymbiont of Litomosoides brasiliensis (genome: WQM000000000); Biosample SAMN15190311 for the nematode host Litomosoides brasiliensis (genome: JABVXW000000000); BioSample SAMN13482487 for wMhie, Wolbachia endosymbiont of Madathamugadia hiepei (genome: WQMP00000000); Biosample SAMN15190315 for the nematode host Madathamugadia hiepei (genome: JABVXS000000000). The raw data are available in GenBank as Sequence Read Archive (SRA): SRR10903008 to SRR10903010; SRR10902913 to SRR10902914; SRR10900508 to SRR10900511; SRR10898805 to SRR10898806. Data summaryThe authors confirm all supporting data, code and protocols have been provided within the article or through supplementary data files. Eleven Supplementary tables and two supplementary files are available with the online version of this article. Impact StatementWolbachia are endosymbiotic bacteria infecting a large range of arthropod species and two different families of nematodes, characterized by causing diverse phenotypes in their hosts, ranging from reproductive parasitism to mutualism. While available Wolbachia genomic data are increasing, they are not representative of the full Wolbachia diversity; indeed, 84% of Wolbachia genomes available on the NCBI database to date belong to the two main studied clades (supergroups A and B, exclusively composed of Wolbachia from arthropods). The present study presents the assembly and analysis of four complete genomes and two draft genomes of Wolbachia from filarial nematodes. Our genomics comparisons confirm the paradigm that smaller Wolbachia genomes from filarial nematodes contain low levels of transposable elements and the absence of intact bacteriophage sequences, unlike many Wolbachia from arthropods. However, data show disparities among the Wolbachia genomes from filarial nematodes: no single pattern of co-evolution, stronger synteny between some clades (supergroups C and supergroup J) and more transposable elements in another clade (supergroup D). Metabolic pathway analysis indicates both highly conserved and more variable pathways, such as vitamin B biosynthesis, which might be specific to certain host-symbiont associations. Overall, there appears to be no single Wolbachia-filarial nematode pattern of symbiotic relationship.

genomics↗