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Unveiling the function and regulation control of the DUF3129 family proteins in fungal infection of hosts.

ABSTRACT: Many prokaryotic and eukaryotic proteins contain domains of unknown function (DUFs). A DUF3129 family of proteins is widely encoded in the genomes of fungal pathogens. A few studies in plant and insect pathogens indicated that the DUF3129 genes are required for fungal penetration of host cuticles with an unclear mechanism. We found that a varied number of DUF3129 proteins is present in different fungal species and the proteins are evolutionarily diverged from each other at the inter- and intra-specific levels. By using the insect pathogenic fungus Metarhizium robertsii as a model, we performed experiments and found that the seven DUF3129 proteins encoded by this fungus are localized to cellular lipid droplets (LDs). Individual deletion of these genes did not affect fungal formation of the infection structure appressoria and the accumulation of LDs in fungal conidia. When compared with the wild-type (WT) strain, insect bioassays revealed that the virulence of most null mutants were significantly impaired during topical infection but not during injection of insects. Carbon starvation and the subsequent Western blot analysis indicated that the LD-specific perilipin protein was completely degraded in the WT cells whereas varied levels of perilipin could be detected in the mutant cells, which signified that depletion of LD content was delayed in mutant cells, and DUF3129 proteins are therefore involved in LD degradation. We also provided biochemical evidence that these DUF3129 genes are transcriptionally regulated by a yeast Ste12-like transcription factor. The findings of this study not only unveil the function of DUF3129 proteins but also better understand the diverse mechanism of fungus-host interactions. This article is part of the theme issue 'Biotic signalling sheds light on smart pest management'.

SUBMITTER: Huang W

PROVIDER: S-EPMC6367153 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The anaerobic gut fungi (AGF) inhabit the alimentary tracts of herbivores. In contrast to placental mammals, information regarding the identity, diversity, and community structure of AGF in marsupials is extremely sparse. Here, we characterized AGF communities in 61 fecal samples from 10 marsupial species belonging to four families in the order Diprotodontia: Vombatidae (wombats), Phascolarctidae (koalas), Phalangeridae (possums), and Macropodidae (kangaroos, wallabies, and pademelons). An amplicon-based diversity survey using the D2 region of the large ribosomal subunit as a phylogenetic marker indicated that marsupial AGF communities were dominated by eight genera commonly encountered in placental herbivores (Neocallimastix, Caecomyces, Cyllamyces, Anaeromyces, Orpinomyces, Piromyces, Pecoramyces, and Khoyollomyces). Community structure analysis revealed a high level of stochasticity, and ordination approaches did not reveal a significant role for the animal host, gut type, dietary preferences, or lifestyle in structuring marsupial AGF communities. Marsupial foregut and hindgut communities displayed diversity and community structure patterns comparable to AGF communities typically encountered in placental foregut hosts while exhibiting a higher level of diversity and a distinct community structure compared to placental hindgut communities. Quantification of AGF load using quantitative PCR indicated a significantly smaller load in marsupial hosts compared to their placental counterparts. Isolation efforts were only successful from a single red kangaroo fecal sample and yielded a Khoyollomyces ramosus isolate closely related to strains previously isolated from placental hosts. Our results suggest that AGF communities in marsupials are in low abundance and show little signs of selection based on ecological and evolutionary factors.IMPORTANCEThe AGF are integral part of the microbiome of herbivores. They play a crucial role in breaking down plant biomass in hindgut and foregut fermenters. The majority of research has been conducted on the AGF community in placental mammalian hosts. However, it is important to note that many marsupial mammals are also herbivores and employ a hindgut or foregut fermentation strategy for breaking down plant biomass. So far, very little is known regarding the AGF diversity and community structure in marsupial mammals. To fill this knowledge gap, we conducted an amplicon-based diversity survey targeting AGF in 61 fecal samples from 10 marsupial species. We hypothesize that, given the distinct evolutionary history and alimentary tract architecture, novel and unique AGF communities would be encountered in marsupials. Our results indicate that marsupial AGF communities are highly stochastic, present in relatively low loads, and display community structure patterns comparable to AGF communities typically encountered in placental foregut hosts. Our results indicate that marsupial hosts harbor AGF communities; however, in contrast to the strong pattern of phylosymbiosis typically observed between AGF and placental herbivores, the identity and gut architecture appear to play a minor role in structuring AGF communities in marsupials.

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Unveiling the function and regulation control of the DUF3129 family proteins in fungal infection of hosts.

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