C. elegans as a new tractable host to study infections by animal pathogenic oomycetes

Grover, Manish; Barkoulas, Michalis

doi:10.1371/journal.ppat.1009316

Cited by 9 publications

(5 citation statements)

References 36 publications

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“…To discover new oomycete pathogens infecting C. elegans , we turned to a site in Bedfordshire in England, where Haptoglossa infections had been previously observed. Haptoglossa is a basal group of oomycetes that diverged before the Saprolegnian and Peronosporalean clades ( Hakariya et al., 2007 ; Hakariya et al., 2009 ; Beakes et al., 2012 ; Spies et al., 2016 ; Grover and Barkoulas, 2021 ). We used C. elegans N2 animals as a pathogen trap and infected worms were identified by the presence of sausage-like thalli, which appeared initially smooth ( Figures 1A, B ) and later developed short exit tubes to release infectious spores ( Figure 1C ).…”

Section: Resultsmentioning

confidence: 99%

Infection of C. elegans by Haptoglossa Species Reveals Shared Features in the Host Response to Oomycete Detection

Grover

Fasseas

Essmann

et al. 2021

Front. Cell. Infect. Microbiol.

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Oomycetes are a group of eukaryotic organisms that includes many important pathogens of animals and plants. Within this group, the Haptoglossa genus is characterised by the presence of specialised gun cells carrying a harpoon-like infection apparatus. While several Haptoglossa pathogens have been morphologically described, there are currently no host systems developed to study the infection process or host responses in the lab. In this study, we report that Haptoglossa species are potent natural pathogens of Caenorhabditis nematodes. Using electron microscopy, we characterise the infection process in C. elegans and demonstrate that the oomycete causes excessive tissue degradation upon entry in the body cavity, whilst leaving the host cuticle intact. We also report that the host transcriptional response to Haptoglossa infection shares similarities with the response against the oomycete Myzocytiopsis humicola, a key example of which is the induction of chitinase-like (chil) genes in the hypodermis. We demonstrate that this shared feature of the host response can be mounted by pathogen detection without any infection, as previously shown for M. humicola. These results highlight similarities in the nematode immune response to natural infection by phylogenetically distinct oomycetes.

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Section: Resultsmentioning

confidence: 99%

Infection of C. elegans by Haptoglossa Species Reveals Shared Features in the Host Response to Oomycete Detection

Grover

Fasseas

Essmann

et al. 2021

Front. Cell. Infect. Microbiol.

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“…The 2 independent incursions of pPolB2 subfamilies into the terrestrial and marine nematodes, from the oomycete and marine mollusc Polinton families, respectively, indicate that the transfers are consistent with the native ecosystems of different groups of nematodes. In this context, we note that terrestrial nematodes can serve as hosts for natural oomycete infection, which could have facilitated the transfer ( Osman et al 2018 ; Grover and Barkoulas 2021 ), whereas marine nematodes most likely shared environments, such as sediment, with prevalent marine molluscs. Although Polinton virions so far have not been observed, the conservation of the MCPs and mCPs, the packaging ATPase, and the maturation PRO across the entire diversity of Polintons strongly suggest that such particles exist.…”

Section: Discussionmentioning

confidence: 98%

DNA Polymerase Diversity Reveals Multiple Incursions of Polintons During Nematode Evolution

Jeong,

Sundrani,

Hall

et al. 2023

Molecular Biology and Evolution

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Polintons are double-stranded DNA, virus-like self-synthesizing transposons widely found in eukaryotic genomes. Recent metagenomic discoveries of Polinton-like viruses are consistent with the hypothesis that Polintons invade eukaryotic host genomes through infectious viral particles. Nematode genomes contain multiple copies of Polintons and provide an opportunity to explore the natural distribution and evolution of Polintons during this process. We performed an extensive search of Polintons across nematode genomes, identifying multiple full-length Polinton copies in several species. We provide evidence of both ancient Polinton integrations and recent mobility in strains of the same nematode species. In addition to the major nematode Polinton family, we identified a group of Polintons that are overall closely related to the major family but encode a distinct protein-primed DNA polymerase B (pPolB) that is related to homologs from a different group of Polintons present outside of the Nematoda. Phylogenetic analyses on the pPolBs support the evolutionary scenarios in which these extrinsic pPolBs that seem to derive from Polinton families present in oomycetes and molluscs replaced the canonical pPolB in subsets of Polintons found in terrestrial and marine nematodes, respectively, suggesting interphylum horizontal gene transfers. The pPolBs of the terrestrial nematode and oomycete Polintons share a unique feature, an insertion of an HNH nuclease domain, whereas the pPolBs in the marine nematode Polintons share an insertion of a VSR nuclease domain with marine mollusc pPolBs. We hypothesize that horizontal gene transfer occurs among Polintons from widely different but cohabiting hosts.

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“…While oomycetes resemble fungi in their morphology and growth as filamentous threads known as mycelia and nutrient acquisition through absorption, they are classified with the stramenopiles, which includes the brown algae and diatoms that have lost plastids and are phylogenetically distant from kingdom Fungi (Beakes et al 2012, Keeling and Burki 2019). Oomycetes occur as part of healthy ecosystems, are an important component to soil biodiversity and play important roles in ecosystem processes (Gomez-Aparico 2012, Bever 2015, Geisen 2015) by functioning as saprotrophs that degrade organic material, pathogens and parasites of invertebrates, vertebrates, plants and fungi (Beakes et al 2012, Jiang et al 2013, Spies et al 2016, Grover and Barkoulas 2021). As pathogens, these organisms may limit host population sizes thereby affecting ecosystems processes, including primary and secondary production, biogeochemical cycles, disturbance regimes, and physical structure (Garnas et al 2011, Cobb et al 2012, Sato et al 2012, Avila et al 2016).…”

Section: Introductionmentioning

confidence: 99%

Oomycete communities in lowland tropical forest soils vary in abundance and are composed of saprophytes and pathogens of seeds and seedlings of multiple plant species.

Broders,

Capador-Barreto,

Iriarte

et al. 2024

Preprint

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Premise: The soils in lowland tropics are teeming with microbial life which can impact plant community structure and diversity through plant-soil feedbacks. While bacteria and fungi have been the focus of most studies in the tropics, the oomycetes may have an outsized effect on seed and seedling health and survival, given their affinity for environments with increased precipitation and temperature. Methods: We assessed the diversity and pathogenicity of oomycete species present in a lowland tropical forest in Panama. We used both a culture dependent leaf-baiting assay and culture independent soil DNA metabarcoding methods to quantify zoospore abundance and species diversity. A subset of the isolates from the baiting assay were used to evaluate pathogenicity and aggressiveness on seedlings of three tree species. Key results: Oomycetes are ubiquitous and common members of the soil microbial community in lowland tropical forests and zoospore abundance was far greater compared to similar studies from temperate and mediterranean forests. We also observed variation in oomycete species ability to infect host plants. Species of Pythium were more aggressive, while species of Phytopythium caused less disease but were more diverse and commonly isolated from the soil. Finally, we found that individual hosts accumulate a distinct oomycete community and was the only factor that had an effect community structure. Conclusions: Collectively, these finding demonstrate that oomycetes are ubiquitous, host-generalist pathogens and saprophytes, that have the potential to impact seed and seedling survival in lowland tropical forests

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C. elegans as a new tractable host to study infections by animal pathogenic oomycetes

Cited by 9 publications

References 36 publications

Infection of C. elegans by Haptoglossa Species Reveals Shared Features in the Host Response to Oomycete Detection

Infection of C. elegans by Haptoglossa Species Reveals Shared Features in the Host Response to Oomycete Detection

DNA Polymerase Diversity Reveals Multiple Incursions of Polintons During Nematode Evolution

Oomycete communities in lowland tropical forest soils vary in abundance and are composed of saprophytes and pathogens of seeds and seedlings of multiple plant species.

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