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Genomic mechanisms accounting for the adaptation to parasitism in nematode-trapping fungi.

ABSTRACT: Orbiliomycetes is one of the earliest diverging branches of the filamentous ascomycetes. The class contains nematode-trapping fungi that form unique infection structures, called traps, to capture and kill free-living nematodes. The traps have evolved differently along several lineages and include adhesive traps (knobs, nets or branches) and constricting rings. We show, by genome sequencing of the knob-forming species Monacrosporium haptotylum and comparison with the net-forming species Arthrobotrys oligospora, that two genomic mechanisms are likely to have been important for the adaptation to parasitism in these fungi. Firstly, the expansion of protein domain families and the large number of species-specific genes indicated that gene duplication followed by functional diversification had a major role in the evolution of the nematode-trapping fungi. Gene expression indicated that many of these genes are important for pathogenicity. Secondly, gene expression of orthologs between the two fungi during infection indicated that differential regulation was an important mechanism for the evolution of parasitism in nematode-trapping fungi. Many of the highly expressed and highly upregulated M. haptotylum transcripts during the early stages of nematode infection were species-specific and encoded small secreted proteins (SSPs) that were affected by repeat-induced point mutations (RIP). An active RIP mechanism was revealed by lack of repeats, dinucleotide bias in repeats and genes, low proportion of recent gene duplicates, and reduction of recent gene family expansions. The high expression and rapid divergence of SSPs indicate a striking similarity in the infection mechanisms of nematode-trapping fungi and plant and insect pathogens from the crown groups of the filamentous ascomycetes (Pezizomycotina). The patterns of gene family expansions in the nematode-trapping fungi were more similar to plant pathogens than to insect and animal pathogens. The observation of RIP activity in the Orbiliomycetes suggested that this mechanism was present early in the evolution of the filamentous ascomycetes.

SUBMITTER: Meerupati T

PROVIDER: S-EPMC3828140 | biostudies-literature | 2013 Nov

REPOSITORIES: biostudies-literature

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Genomic mechanisms accounting for the adaptation to parasitism in nematode-trapping fungi.

Meerupati Tejashwari T Andersson Karl-Magnus KM Friman Eva E Kumar Dharmendra D Tunlid Anders A Ahrén Dag D

PLoS genetics 20131114 11

Orbiliomycetes is one of the earliest diverging branches of the filamentous ascomycetes. The class contains nematode-trapping fungi that form unique infection structures, called traps, to capture and kill free-living nematodes. The traps have evolved differently along several lineages and include adhesive traps (knobs, nets or branches) and constricting rings. We show, by genome sequencing of the knob-forming species Monacrosporium haptotylum and comparison with the net-forming species Arthrobot ...[more]

PMID: 24244185

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Project description:BackgroundNematode-trapping fungi are soil-living fungi that capture and kill nematodes using special hyphal structures called traps. They display a large diversity of trapping mechanisms and differ in their host preferences. To provide insights into the genetic basis for this variation, we compared the transcriptome expressed by three species of nematode-trapping fungi (Arthrobotrys oligospora, Monacrosporium cionopagum and Arthrobotrys dactyloides, which use adhesive nets, adhesive branches or constricting rings, respectively, to trap nematodes) during infection of two different plant-pathogenic nematode hosts (the root knot nematode Meloidogyne hapla and the sugar beet cyst nematode Heterodera schachtii).ResultsThe divergence in gene expression between the fungi was significantly larger than that related to the nematode species being infected. Transcripts predicted to encode secreted proteins and proteins with unknown function (orphans) were overrepresented among the highly expressed transcripts in all fungi. Genes that were highly expressed in all fungi encoded endopeptidases, such as subtilisins and aspartic proteases; cell-surface proteins containing the carbohydrate-binding domain WSC; stress response proteins; membrane transporters; transcription factors; and transcripts containing the Ricin-B lectin domain. Differentially expressed transcripts among the fungal species encoded various lectins, such as the fungal fruit-body lectin and the D-mannose binding lectin; transcription factors; cell-signaling components; proteins containing a WSC domain; and proteins containing a DUF3129 domain. A small set of transcripts were differentially expressed in infections of different host nematodes, including peptidases, WSC domain proteins, tyrosinases, and small secreted proteins with unknown function.ConclusionsThis is the first study on the variation of infection-related gene expression patterns in nematode-trapping fungi infecting different host species. A better understanding of these patterns will facilitate the improvements of these fungi in biological control programs, by providing molecular markers for screening programs and candidates for genetic manipulations of virulence and host preferences.

Project description:Publication of the genome from the clade I organism, Trichinella spiralis, has provided us an avenue to address more holistic problems in parasitology; namely the processes of adaptation and the evolution of parasitism. Parasitism among nematodes has evolved in multiple, independent events. Deciphering processes that drive species diversity and adaptation are keys to understanding parasitism and advancing control strategies. Studies have been put forth on morphological and physiological aspects of parasitism and adaptation in nematodes; however, data is now coming available to investigate adaptation, host switching and parasitism at the genomic level. Herein we compare proteomic data from the clade I parasite, Trichinella spiralis with data from Brugia malayi (clade III), Meloidogyne hapla and Meloidogyne incognita (clade IV), and free-living nematodes belonging to the genera Caenorhabditis and Pristionchus (clade V). We explore changes in protein family birth/death and expansion/reduction over the course of metazoan evolution using Homo sapiens, Drosophila melanogaster and Saccharomyces cerevisiae as outgroups for the phylum Nematoda. We further examine relationships between these changes and the ability and/or result of nematodes adapting to their environments. Data are consistent with gene loss occurring in conjunction with nematode specialization resulting from parasitic worms acclimating to well-defined, environmental niches. We observed evidence for independent, lateral gene transfer events involving conserved genes that may have played a role in the evolution of nematode parasitism. In general, parasitic nematodes gained proteins through duplication and lateral gene transfer, and lost proteins through random mutation and deletions. Data suggest independent acquisition rather than ancestral inheritance among the Nematoda followed by selective gene loss over evolutionary time. Data also show that parasitism and adaptation affected a broad range of proteins, especially those involved in sensory perception, metabolism, and transcription/translation. New protein gains with functions related to regulating transcription and translation, and protein family expansions with functions related to morphology and body development have occurred in association with parasitism. Further gains occurred as a result of lateral gene transfer and in particular, with the cyanase protein family In contrast, reductions and/or losses have occurred in protein families with functions related to metabolic process and signal transduction. Taking advantage of the independent occurrences of parasitism in nematodes, which enabled us to distinguish changes associated with parasitism from species specific niche adaptation, our study provides valuable insights into nematode parasitism at a proteome level using T. spiralis as a benchmark for early adaptation to or acquisition of parasitism.

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Genomic mechanisms accounting for the adaptation to parasitism in nematode-trapping fungi.

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Genomic mechanisms accounting for the adaptation to parasitism in nematode-trapping fungi.

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