Comparative genomics provides insights into the lifestyle and reveals functional heterogeneity of dark septate endophytic fungi

Knapp, Dániel G.; Németh, Julianna B.; Barry, Kerrie; Hainaut, Matthieu; Henrissat, Bernard; Johnson, Jenifer; Kuo, Alan; Lim, Joanne; Lipzen, Anna; Nolan, Matt; Ohm, Robin A.; Tamás, László; Grigoriev, Igor V.; Spatafora, Joseph W.; Nagy, László G.; Kovács, Gábor M.

doi:10.1038/s41598-018-24686-4

Cited by 146 publications

(123 citation statements)

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“…Depending on the lifestyle (saprotrophic, pathogenic or mutualistic) and the habitat, the way of gaining nutrients and energy may vary. In particular qualitative and quantitative differences in terms of CAZymes can be potent reporters of fungal lifestyle [38,[40][41][42]. In the present study, diverging CAZyme repertoires among species or species groups sharing the same ecology were identified.…”

Section: Discussionmentioning

confidence: 61%

Comparative genomics applied to Mucor species with different lifestyles

et al. 2020

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Background: Despite a growing number of investigations on early diverging fungi, the corresponding lineages have not been as extensively characterized as Ascomycota or Basidiomycota ones. The Mucor genus, pertaining to one of these lineages is not an exception. To this date, a restricted number of Mucor annotated genomes is publicly available and mainly correspond to the reference species, Mucor circinelloides, and to medically relevant species. However, the Mucor genus is composed of a large number of ubiquitous species as well as few species that have been reported to specifically occur in certain habitats. The present study aimed to expand the range of Mucor genomes available and identify potential genomic imprints of adaptation to different environments and lifestyles in the Mucor genus. Results: In this study, we report four newly sequenced genomes of Mucor isolates collected from non-clinical environments pertaining to species with contrasted lifestyles, namely Mucor fuscus and Mucor lanceolatus, two species used in cheese production (during ripening), Mucor racemosus, a recurrent cheese spoiler sometimes described as an opportunistic animal and human pathogen, and Mucor endophyticus, a plant endophyte. Comparison of these new genomes with those previously available for six Mucor and two Rhizopus (formerly identified as M. racemosus) isolates allowed global structural and functional description such as their TE content, core and species-specific genes and specialized genes. We proposed gene candidates involved in iron metabolism; some of these genes being known to be involved in pathogenicity; and described patterns such as a reduced number of CAZymes in the species used for cheese ripening as well as in the endophytic isolate that might be related to adaptation to different environments and lifestyles within the Mucor genus. Conclusions: This study extended the descriptive data set for Mucor genomes, pointed out the complexity of obtaining a robust phylogeny even with multiple genes families and allowed identifying contrasting potentially lifestyle-associated gene repertoires. The obtained data will allow investigating further the link between genetic and its biological data, especially in terms of adaptation to a given habitat.

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Section: Discussionmentioning

confidence: 61%

Comparative genomics applied to Mucor species with different lifestyles

et al. 2020

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“…g . (49)) profiles, as predicted from genomes, that may be associated with different lifestyles. By comparing the predicted molecular repertoires for Tetracladium both among strains from different ecological niches within the genus and to those of better studied functional groups it may be possible to gain insight into the ecology of Tetracladium .…”

Section: Introductionmentioning

confidence: 99%

Broad geographical and ecological diversity from similar genomic toolkits in the ascomycete genusTetracladium

Anderson

Marvanová

2020

Preprint

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18The ascomycete genus Tetracladium is best known for containing aquatic hyphomycetes, which are 19 important decomposers in stream food webs. However, some species of Tetracladium are thought 20 to be multifunctional and are also endobionts in plants. Suprisingly, Tetracladium sequences are 21 increasingly being reported from metagenomics and metabarcoding studies of both plants and soils 22 world-wide. It is not clear how these sequences are related to the described species and little is 23 known about the non-aquatic biology of these fungi. Here, the genomes of 24 Tetracladium strains, 24 including all described species, were sequenced and used to resolve relationships among taxa and to 25 improve our understanding of ecological and genomic diversity in this group. All genome-sequenced 26 Tetracladium fungi form a monophyletic group. Conspecific strains of T. furcatum from both aquatic 27 saprotrophic and endobiont lifestyles and a putative cold-adapted clade are identified. Analysis of 28 ITS sequences from water, soil, and plants from around the world reveals that multifunctionality 29 may be widespread through the genus. Further, frequent reports of these fungi from extreme 30 environments suggest they may have important but unknown roles in those ecosystems. Patterns of 31 predicted carbohydrate active enzymes (CAZyme) and secondary metabolites in the Tetracladium 32 genomes are more similar to each other than to other ascomycetes, regardless of ecology, 33 suggesting a strong role for phylogeny shaping genome content in the genus. Tetracladium genomes 34 are enriched for pectate lyase domains (including PL3-2), GH71 α-1,3-glucanase domains and CBM24 35 α-1,3-glucan/mutan binding modules, and both GH32 and CBM38, inulinase and inulin binding 36 modules. These results indicate that these fungi are well-suited to digesting pectate and pectin in 37 leaves when living as aquatic hyphomycetes, and inulin when living as root endobionts. Enrichment 38 for α-1,3-glucanase domains may be associated with interactions with biofilm forming 39 microorganisms in root and submerged leaf environments. 42 important decomposers in stream ecosystems. The group is polyphyletic, its members are classified 43 in various orders and families of Ascomycetes and Basidiomycetes. These fungi thrive on leaves and 44 other plant debris that enter streams and other water bodies from terrestrial plants. In the process, 45 carbon and nutrients from recalcitrant plant compounds, including cellulose and lignin, become 46 accessible to diverse consumers in the stream food web (reviewed in (1, 2)). Up to 99% of the carbon 47 in some streams enters as plant debris that is largely inaccessible to aquatic consumers without the 48 degradative activity of these fungi (3, 4). Aquatic hyphomycete adaptations to stream environments 49 include the production of asexual propagules (conidia) while under water. These spores are often 50 branched, typically tetraradiate, or sigmoid, readily detachable from the fungus (e.g. from 51 conidiophores) and passi...

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“…Two characteristic, frequent and common DSEs of such ecosystems are Periconia macrospinosa and Cadophora sp., which generally colonise grass and non-grass hosts, respectively (Knapp et al 2012). The complete genomes of both DSEs have recently been sequenced and analysed (Knapp et al 2018). When isolates of P. macrospinosa were used in in vitro experiments with Arabidopsis thaliana, the effect of the DSE varied according to the plant ecotype (Mandyam et al 2013).…”

Section: Introductionmentioning

confidence: 99%

Impact of dark septate endophytes on tomato growth and nutrient uptake

Yakti

Kovács

Vági

et al. 2018

Plant Ecology & Diversity

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Background: Dark septate endophytes (DSEs) represent a form-group of ascomycetous fungi that inhabit the roots of a wide range of plant species, but our knowledge on their interaction with the host plants is still limited. Aims: This study was conducted to examine the effect of DSEs on the nutrition and growth of tomato (Solanum lycopersicum) in order to assess their potential application in horticultural plant production. Methods: The capacity of two model DSE species, Periconia macrospinosa and Cadophora sp. to mobilise different forms of N and P (organic and inorganic) was analysed, and an in vitro bio assay with tomato plantlets was applied to screen the compatibility of these fungi with the plant. Pot-culture experiments with and without compartments were conducted to study the effects of these DSEs on the growth and nutrient uptake of tomato plants grown with organic and inorganic N and P sources. Results: Periconia macrospinosa, but not Cadophora sp., increased the root and shoot biomass of tomato plants when organic nutrient resources were present, and both DSEs promoted shoot growth when cultivated with inorganic fertilisers. Analysis of N and P concentrations indicated that the growth response of tomato with inorganic fertilisation was not based on DSE-improved plant nutrition. However, P. macrospinosa improved N uptake from organic sources. Conclusion: The positive effects of DSEs seem to be due to nutrient mobilisation rather than to hyphal transport to the plant.

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Comparative genomics provides insights into the lifestyle and reveals functional heterogeneity of dark septate endophytic fungi

Cited by 146 publications

References 100 publications

Comparative genomics applied to Mucor species with different lifestyles

Comparative genomics applied to Mucor species with different lifestyles

Broad geographical and ecological diversity from similar genomic toolkits in the ascomycete genusTetracladium

Impact of dark septate endophytes on tomato growth and nutrient uptake

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