Hanseniaspora smithiae sp. nov., a Novel Apiculate Yeast Species From Patagonian Forests That Lacks the Typical Genomic Domestication Signatures for Fermentative Environments

During a survey of Nothofagus trees and their parasitic fungi in Andean Patagonia (Argentina), genetically distinct strains of Hanseniaspora were obtained from the sugar-containing stromata of parasitic Cyttaria spp. Phylogenetic analyses based on the single-gene sequences (encoding rRNA and actin)...

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Main Authors: Neža Čadež, Nicolas Bellora, Ricardo Ulloa, Miha Tome, Hrvoje Petković, Marizeth Groenewald, Chris Todd Hittinger, Diego Libkind
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-07-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.679894/full
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author Neža Čadež
Nicolas Bellora
Ricardo Ulloa
Miha Tome
Hrvoje Petković
Marizeth Groenewald
Chris Todd Hittinger
Diego Libkind
author_facet Neža Čadež
Nicolas Bellora
Ricardo Ulloa
Miha Tome
Hrvoje Petković
Marizeth Groenewald
Chris Todd Hittinger
Diego Libkind
author_sort Neža Čadež
collection DOAJ
description During a survey of Nothofagus trees and their parasitic fungi in Andean Patagonia (Argentina), genetically distinct strains of Hanseniaspora were obtained from the sugar-containing stromata of parasitic Cyttaria spp. Phylogenetic analyses based on the single-gene sequences (encoding rRNA and actin) or on conserved, single-copy, orthologous genes from genome sequence assemblies revealed that these strains represent a new species closely related to Hanseniaspora valbyensis. Additionally, delimitation of this novel species was supported by genetic distance calculations using overall genome relatedness indices (OGRI) between the novel taxon and its closest relatives. To better understand the mode of speciation in Hanseniaspora, we examined genes that were retained or lost in the novel species in comparison to its closest relatives. These analyses show that, during diversification, this novel species and its closest relatives, H. valbyensis and Hanseniaspora jakobsenii, lost mitochondrial and other genes involved in the generation of precursor metabolites and energy, which could explain their slower growth and higher ethanol yields under aerobic conditions. Similarly, Hanseniaspora mollemarum lost the ability to sporulate, along with genes that are involved in meiosis and mating. Based on these findings, a formal description of the novel yeast species Hanseniaspora smithiae sp. nov. is proposed, with CRUB 1602H as the holotype.
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spelling doaj.art-00ba73bfdcac4bf9a3a4679c9eb9a02b2022-12-21T18:25:05ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-07-011210.3389/fmicb.2021.679894679894Hanseniaspora smithiae sp. nov., a Novel Apiculate Yeast Species From Patagonian Forests That Lacks the Typical Genomic Domestication Signatures for Fermentative EnvironmentsNeža Čadež0Nicolas Bellora1Ricardo Ulloa2Miha Tome3Hrvoje Petković4Marizeth Groenewald5Chris Todd Hittinger6Diego Libkind7Food Science and Technology Department, Biotechnical Faculty, University of Ljubljana, Ljubljana, SloveniaCentro de Referencia en Levaduras y Tecnología Cervecera (CRELTEC), Instituto Andino Patagónico de Tecnologías Biológicas y Geoambientales (IPATEC), Consejo Nacional de Investigaciones, Científicas y Técnicas (CONICET), Universidad Nacional del Comahue, Bariloche, ArgentinaLaboratorio de Bioprocesos, Instituto de Investigación y Desarrollo en Ingeniería de Procesos, Biotecnología y Energías Alternativas, Consejo Nacional de Investigaciones, Científicas y Técnicas (CONICET), Universidad Nacional del Comahue, Neuquén, ArgentinaFood Science and Technology Department, Biotechnical Faculty, University of Ljubljana, Ljubljana, SloveniaFood Science and Technology Department, Biotechnical Faculty, University of Ljubljana, Ljubljana, SloveniaWesterdijk Fungal Biodiversity Institute, Utrecht, NetherlandsLaboratory of Genetics, Center for Genomic Science Innovation, DOE Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, J. F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, WI, United StatesCentro de Referencia en Levaduras y Tecnología Cervecera (CRELTEC), Instituto Andino Patagónico de Tecnologías Biológicas y Geoambientales (IPATEC), Consejo Nacional de Investigaciones, Científicas y Técnicas (CONICET), Universidad Nacional del Comahue, Bariloche, ArgentinaDuring a survey of Nothofagus trees and their parasitic fungi in Andean Patagonia (Argentina), genetically distinct strains of Hanseniaspora were obtained from the sugar-containing stromata of parasitic Cyttaria spp. Phylogenetic analyses based on the single-gene sequences (encoding rRNA and actin) or on conserved, single-copy, orthologous genes from genome sequence assemblies revealed that these strains represent a new species closely related to Hanseniaspora valbyensis. Additionally, delimitation of this novel species was supported by genetic distance calculations using overall genome relatedness indices (OGRI) between the novel taxon and its closest relatives. To better understand the mode of speciation in Hanseniaspora, we examined genes that were retained or lost in the novel species in comparison to its closest relatives. These analyses show that, during diversification, this novel species and its closest relatives, H. valbyensis and Hanseniaspora jakobsenii, lost mitochondrial and other genes involved in the generation of precursor metabolites and energy, which could explain their slower growth and higher ethanol yields under aerobic conditions. Similarly, Hanseniaspora mollemarum lost the ability to sporulate, along with genes that are involved in meiosis and mating. Based on these findings, a formal description of the novel yeast species Hanseniaspora smithiae sp. nov. is proposed, with CRUB 1602H as the holotype.https://www.frontiersin.org/articles/10.3389/fmicb.2021.679894/fullapiculate yeastnew speciesphylogenomicsOGRIgene lossspeciation
spellingShingle Neža Čadež
Nicolas Bellora
Ricardo Ulloa
Miha Tome
Hrvoje Petković
Marizeth Groenewald
Chris Todd Hittinger
Diego Libkind
Hanseniaspora smithiae sp. nov., a Novel Apiculate Yeast Species From Patagonian Forests That Lacks the Typical Genomic Domestication Signatures for Fermentative Environments
Frontiers in Microbiology
apiculate yeast
new species
phylogenomics
OGRI
gene loss
speciation
title Hanseniaspora smithiae sp. nov., a Novel Apiculate Yeast Species From Patagonian Forests That Lacks the Typical Genomic Domestication Signatures for Fermentative Environments
title_full Hanseniaspora smithiae sp. nov., a Novel Apiculate Yeast Species From Patagonian Forests That Lacks the Typical Genomic Domestication Signatures for Fermentative Environments
title_fullStr Hanseniaspora smithiae sp. nov., a Novel Apiculate Yeast Species From Patagonian Forests That Lacks the Typical Genomic Domestication Signatures for Fermentative Environments
title_full_unstemmed Hanseniaspora smithiae sp. nov., a Novel Apiculate Yeast Species From Patagonian Forests That Lacks the Typical Genomic Domestication Signatures for Fermentative Environments
title_short Hanseniaspora smithiae sp. nov., a Novel Apiculate Yeast Species From Patagonian Forests That Lacks the Typical Genomic Domestication Signatures for Fermentative Environments
title_sort hanseniaspora smithiae sp nov a novel apiculate yeast species from patagonian forests that lacks the typical genomic domestication signatures for fermentative environments
topic apiculate yeast
new species
phylogenomics
OGRI
gene loss
speciation
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.679894/full
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