Naming the untouchable – environmental sequences and niche partitioning as taxonomical evidence in fungi

ABSTRACT Due to their submerged and cryptic lifestyle, the vast majority of fungal species are difficult to observe and describe morphologically, and many remain known to science only from sequences detected in environmental samples. The lack of practices to delimit and name most fungal species is a...

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Main Authors: Faheema Kalsoom Khan, Kerri Kluting, Jeanette Tångrot, Hector Urbina, Tea Ammunet, Shadi Eshghi Sahraei, Martin Rydén, Martin Ryberg, Anna Rosling
Format: Article
Language:English
Published: BMC 2020-11-01
Series:IMA Fungus
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Online Access:http://link.springer.com/article/10.1186/s43008-020-00045-9
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author Faheema Kalsoom Khan
Kerri Kluting
Jeanette Tångrot
Hector Urbina
Tea Ammunet
Shadi Eshghi Sahraei
Martin Rydén
Martin Ryberg
Anna Rosling
author_facet Faheema Kalsoom Khan
Kerri Kluting
Jeanette Tångrot
Hector Urbina
Tea Ammunet
Shadi Eshghi Sahraei
Martin Rydén
Martin Ryberg
Anna Rosling
author_sort Faheema Kalsoom Khan
collection DOAJ
description ABSTRACT Due to their submerged and cryptic lifestyle, the vast majority of fungal species are difficult to observe and describe morphologically, and many remain known to science only from sequences detected in environmental samples. The lack of practices to delimit and name most fungal species is a staggering limitation to communication and interpretation of ecology and evolution in kingdom Fungi. Here, we use environmental sequence data as taxonomical evidence and combine phylogenetic and ecological data to generate and test species hypotheses in the class Archaeorhizomycetes (Taphrinomycotina, Ascomycota). Based on environmental amplicon sequencing from a well-studied Swedish pine forest podzol soil, we generate 68 distinct species hypotheses of Archaeorhizomycetes, of which two correspond to the only described species in the class. Nine of the species hypotheses represent 78% of the sequenced Archaeorhizomycetes community, and are supported by long read data that form the backbone for delimiting species hypothesis based on phylogenetic branch lengths. Soil fungal communities are shaped by environmental filtering and competitive exclusion so that closely related species are less likely to co-occur in a niche if adaptive traits are evolutionarily conserved. In soil profiles, distinct vertical horizons represent a testable niche dimension, and we found significantly differential distribution across samples for a well-supported pair of sister species hypotheses. Based on the combination of phylogenetic and ecological evidence, we identify two novel species for which we provide molecular diagnostics and propose names. While environmental sequences cannot be automatically translated to species, they can be used to generate phylogenetically distinct species hypotheses that can be further tested using sequences as ecological evidence. We conclude that in the case of abundantly and frequently observed species, environmental sequences can support species recognition in the absences of physical specimens, while rare taxa remain uncaptured at our sampling and sequencing intensity.
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spelling doaj-art-50a7bfb4fd5c41e98a98532f29aa12722025-02-03T00:09:08ZengBMCIMA Fungus2210-63592020-11-0111111210.1186/s43008-020-00045-9Naming the untouchable – environmental sequences and niche partitioning as taxonomical evidence in fungiFaheema Kalsoom Khan0Kerri Kluting1Jeanette Tångrot2Hector Urbina3Tea Ammunet4Shadi Eshghi Sahraei5Martin Rydén6Martin Ryberg7Anna Rosling8Department of Ecology and Genetics, Evolutionary Biology, Uppsala UniversityDepartment of Ecology and Genetics, Evolutionary Biology, Uppsala UniversityDepartment of Molecular Biology, National Bioinformatics Infrastructure Sweden (NBIS), SciLifeLab, Umeå UniversityDepartment of Ecology and Genetics, Evolutionary Biology, Uppsala UniversityDepartment of Ecology and Genetics, Evolutionary Biology, Uppsala UniversityDepartment of Ecology and Genetics, Evolutionary Biology, Uppsala UniversityDepartment of Ecology and Genetics, Evolutionary Biology, Uppsala UniversityDepartment of Organismal Biology, Systematic Biology, Uppsala UniversityDepartment of Ecology and Genetics, Evolutionary Biology, Uppsala UniversityABSTRACT Due to their submerged and cryptic lifestyle, the vast majority of fungal species are difficult to observe and describe morphologically, and many remain known to science only from sequences detected in environmental samples. The lack of practices to delimit and name most fungal species is a staggering limitation to communication and interpretation of ecology and evolution in kingdom Fungi. Here, we use environmental sequence data as taxonomical evidence and combine phylogenetic and ecological data to generate and test species hypotheses in the class Archaeorhizomycetes (Taphrinomycotina, Ascomycota). Based on environmental amplicon sequencing from a well-studied Swedish pine forest podzol soil, we generate 68 distinct species hypotheses of Archaeorhizomycetes, of which two correspond to the only described species in the class. Nine of the species hypotheses represent 78% of the sequenced Archaeorhizomycetes community, and are supported by long read data that form the backbone for delimiting species hypothesis based on phylogenetic branch lengths. Soil fungal communities are shaped by environmental filtering and competitive exclusion so that closely related species are less likely to co-occur in a niche if adaptive traits are evolutionarily conserved. In soil profiles, distinct vertical horizons represent a testable niche dimension, and we found significantly differential distribution across samples for a well-supported pair of sister species hypotheses. Based on the combination of phylogenetic and ecological evidence, we identify two novel species for which we provide molecular diagnostics and propose names. While environmental sequences cannot be automatically translated to species, they can be used to generate phylogenetically distinct species hypotheses that can be further tested using sequences as ecological evidence. We conclude that in the case of abundantly and frequently observed species, environmental sequences can support species recognition in the absences of physical specimens, while rare taxa remain uncaptured at our sampling and sequencing intensity.http://link.springer.com/article/10.1186/s43008-020-00045-9Archaeorhizomyces victor nom. seq.Archaeorhizomyces secundus nom. seq.BiodiversityDark matter fungi/dark taxaRealized nicheVoucherless taxa
spellingShingle Faheema Kalsoom Khan
Kerri Kluting
Jeanette Tångrot
Hector Urbina
Tea Ammunet
Shadi Eshghi Sahraei
Martin Rydén
Martin Ryberg
Anna Rosling
Naming the untouchable – environmental sequences and niche partitioning as taxonomical evidence in fungi
IMA Fungus
Archaeorhizomyces victor nom. seq.
Archaeorhizomyces secundus nom. seq.
Biodiversity
Dark matter fungi/dark taxa
Realized niche
Voucherless taxa
title Naming the untouchable – environmental sequences and niche partitioning as taxonomical evidence in fungi
title_full Naming the untouchable – environmental sequences and niche partitioning as taxonomical evidence in fungi
title_fullStr Naming the untouchable – environmental sequences and niche partitioning as taxonomical evidence in fungi
title_full_unstemmed Naming the untouchable – environmental sequences and niche partitioning as taxonomical evidence in fungi
title_short Naming the untouchable – environmental sequences and niche partitioning as taxonomical evidence in fungi
title_sort naming the untouchable environmental sequences and niche partitioning as taxonomical evidence in fungi
topic Archaeorhizomyces victor nom. seq.
Archaeorhizomyces secundus nom. seq.
Biodiversity
Dark matter fungi/dark taxa
Realized niche
Voucherless taxa
url http://link.springer.com/article/10.1186/s43008-020-00045-9
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