Secondary metabolites of Hülle cells mediate protection of fungal reproductive and overwintering structures against fungivorous animals
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Evaluation Summary:
Hülle cells, a type of cells formed by fungal species of the genus Aspergillus, are specialized cells that surround the sexual fruiting bodies of ascomycete fungi and are thought to nurse the fruiting bodies during fungal development. In this work, Liu et al. suggest that these cells have a strong ecological impact because they contain specific secondary metabolites that help the fungus to "withstand" the attack by fungivorous animals, like springtails, and also inhibit sexual reproduction of other fungi. This work will likely have a major impact on our view on the development and ecology of fungi as well as on the ecological functions of secondary metabolites.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 and Reviewer #3 agreed to share their names with the authors.)
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Abstract
Fungal Hülle cells with nuclear storage and developmental backup functions are reminiscent of multipotent stem cells. In the soil, Hülle cells nurse the overwintering fruiting bodies of Aspergillus nidulans . The genome of A. nidulans harbors genes for the biosynthesis of xanthones. We show that enzymes and metabolites of this biosynthetic pathway accumulate in Hülle cells under the control of the regulatory velvet complex, which coordinates development and secondary metabolism. Deletion strains blocked in the conversion of anthraquinones to xanthones accumulate emodins and are delayed in maturation and growth of fruiting bodies. Emodin represses fruiting body and resting structure formation in other fungi. Xanthones are not required for sexual development but exert antifeedant effects on fungivorous animals such as springtails and woodlice. Our findings reveal a novel role of Hülle cells in establishing secure niches for A. nidulans by accumulating metabolites with antifeedant activity that protect reproductive structures from animal predators.
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Evaluation Summary:
Hülle cells, a type of cells formed by fungal species of the genus Aspergillus, are specialized cells that surround the sexual fruiting bodies of ascomycete fungi and are thought to nurse the fruiting bodies during fungal development. In this work, Liu et al. suggest that these cells have a strong ecological impact because they contain specific secondary metabolites that help the fungus to "withstand" the attack by fungivorous animals, like springtails, and also inhibit sexual reproduction of other fungi. This work will likely have a major impact on our view on the development and ecology of fungi as well as on the ecological functions of secondary metabolites.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested …
Evaluation Summary:
Hülle cells, a type of cells formed by fungal species of the genus Aspergillus, are specialized cells that surround the sexual fruiting bodies of ascomycete fungi and are thought to nurse the fruiting bodies during fungal development. In this work, Liu et al. suggest that these cells have a strong ecological impact because they contain specific secondary metabolites that help the fungus to "withstand" the attack by fungivorous animals, like springtails, and also inhibit sexual reproduction of other fungi. This work will likely have a major impact on our view on the development and ecology of fungi as well as on the ecological functions of secondary metabolites.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 and Reviewer #3 agreed to share their names with the authors.)
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Reviewer #1 (Public Review):
Hülle cells are formed by fungal species of the genus Aspergillus such as Aspergillus nidulans. These cells are unusual because they surround cleistothecia, the fruiting bodies of ascomycetes. Until now, the current hypothesis is that they mainly serve to nurse cleistothecia during development. It was a matter of debate whether this is the real function of these cells or whether they have additional functions. In the current manuscript the authors provide compelling evidence that these cells have a strong ecological impact as they contain specific secondary metabolites (SMs) helping the fungus to "withstand" the attack by fungivorous animals like springtails and furthermore, these SMs inhibit sexual reproduction of other fungi. This way the results of this manuscript have a major impact on our view on the …
Reviewer #1 (Public Review):
Hülle cells are formed by fungal species of the genus Aspergillus such as Aspergillus nidulans. These cells are unusual because they surround cleistothecia, the fruiting bodies of ascomycetes. Until now, the current hypothesis is that they mainly serve to nurse cleistothecia during development. It was a matter of debate whether this is the real function of these cells or whether they have additional functions. In the current manuscript the authors provide compelling evidence that these cells have a strong ecological impact as they contain specific secondary metabolites (SMs) helping the fungus to "withstand" the attack by fungivorous animals like springtails and furthermore, these SMs inhibit sexual reproduction of other fungi. This way the results of this manuscript have a major impact on our view on the development and ecology of fungi and at the same time also contribute to unravel the function of SMs.
Overall, the study is novel, highly informative with regard to fungal development and the ecology of fungi, and very well presented. The biology of Hülle cells is fascinating and there is only little information about this type of cells. In this paper the major function of Hülle cells was discovered. The introduction provides an excellent overview about the topic, methods are described in sufficient detail, results are clearly presented, most Figures are of high quality and in the discussion, the results are comprehensively interpreted.
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Reviewer #2 (Public Review):
The submitted manuscript sought to show that xanthones produced by Aspergillus nidulans are associated with Hulle cells that nurse cleistothecia. The authors present compelling evidence that xanthones are produced in Hulle cells during sexual development of A. nidulans. This raises important ecological questions about what important ecological interactions these compounds may have with cleistothecia. The authors investigate potential roles for these compounds in protecting the fungus from fungivory and in suppressing the growth of competing fungi. While these experiments do point to possible ecological functionalities of these compounds, more work is needed to clarify if these experiments represent interactions that could occur in nature and how such interactions might ultimately impact the fitness of A. …
Reviewer #2 (Public Review):
The submitted manuscript sought to show that xanthones produced by Aspergillus nidulans are associated with Hulle cells that nurse cleistothecia. The authors present compelling evidence that xanthones are produced in Hulle cells during sexual development of A. nidulans. This raises important ecological questions about what important ecological interactions these compounds may have with cleistothecia. The authors investigate potential roles for these compounds in protecting the fungus from fungivory and in suppressing the growth of competing fungi. While these experiments do point to possible ecological functionalities of these compounds, more work is needed to clarify if these experiments represent interactions that could occur in nature and how such interactions might ultimately impact the fitness of A. nidulans. The current ecological experiments do, however, point toward interesting possible functions of these compounds, offering rare direction to investigate the ecological function of a fungal secondary metabolite.
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Reviewer #3 (Public Review):
There are two major strengths this reviewer can find in this manuscript. First, the authors suggest a novel role of Hülle cells in providing benefits in the niche competition against other fungi and in protection of reproductive structures from animal predators by accumulating certain secondary metabolites. Despite the initial identification of Hülle cells in the late 19th century, previous studies on Hülle cells only suggested that these cells actively support and protect the developing fruiting bodies. It has remained largely speculative what advantage the energy-consuming production of Hülle cells confers or how this cell type contributes to the success of aspergilli. In this manuscript, the authors have elucidated an important protective role of Hülle cells ensuring the long-term survival of A. nidulans …
Reviewer #3 (Public Review):
There are two major strengths this reviewer can find in this manuscript. First, the authors suggest a novel role of Hülle cells in providing benefits in the niche competition against other fungi and in protection of reproductive structures from animal predators by accumulating certain secondary metabolites. Despite the initial identification of Hülle cells in the late 19th century, previous studies on Hülle cells only suggested that these cells actively support and protect the developing fruiting bodies. It has remained largely speculative what advantage the energy-consuming production of Hülle cells confers or how this cell type contributes to the success of aspergilli. In this manuscript, the authors have elucidated an important protective role of Hülle cells ensuring the long-term survival of A. nidulans in the semi-wildlife situation. This discovery could be perceived as a major breakthrough in expanding the knowledge of fungal biology, which can be included in textbooks for undergraduates to fungal experts. Moreover, these findings can provide insights into various fields; for example, these chemicals can be extracted from fungi or chemically synthesized and utilized as an insect repellent or fungicide. Second, the way how they draw conclusions is also the main strength of the manuscript. The authors have extensive expertise in metabolomic research and have revealed which proteins encoded by the mdp/xpt genes are exclusively located in Hülle cells and sexual hyphae by utilizing the GFP fusion technique and quantifying levels of each protein. Furthermore, they performed extensive metabolomic experiments on the mdp/xpt cluster metabolites with wild-type and all single null mutants of the cluster and unveiled the metabolite accumulation pattern of individual strains. Based on the results from these metabolomic data, the authors designed fungal and animal experiments to observe a potential role Hülle cells during interaction. This extensive metabolomic work is thorough and precise and the data support their conclusions well.
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