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Molecular and Genetic Evidence for a Tetrapolar Mating System in the Basidiomycetous Yeast Kwoniella mangrovensis and Two Novel Sibling Species

Identifieur interne : 000133 ( Pmc/Checkpoint ); précédent : 000132; suivant : 000134

Molecular and Genetic Evidence for a Tetrapolar Mating System in the Basidiomycetous Yeast Kwoniella mangrovensis and Two Novel Sibling Species

Auteurs : Marco A. Guerreiro ; Deborah J. Springer ; Joana A. Rodrigues ; Laura N. Rusche ; Keisha Findley ; Joseph Heitman ; Álvaro Fonseca

Source :

RBID : PMC:3647770

Abstract

Kwoniella mangrovensis has been described as a sexual species with a bipolar mating system. Phylogenetic analysis of multiple genes places this species together with Kwoniella heveanensis in the Kwoniella clade, a sister clade to that containing two pathogenic species of global importance, Cryptococcus neoformans and Cryptococcus gattii, within the Tremellales. Recent studies defining the mating type loci (MAT) of species in these clades showed that, with the exception of C. neoformans and C. gattii, which are bipolar with a single biallelic multigene MAT locus, several other species feature a tetrapolar mating system with two unlinked loci (homeodomain [HD] and pheromone/receptor [P/R] loci). We characterized several strains from the original study describing K. mangrovensis; two MAT regions were amplified and sequenced: the STE20 gene (P/R locus) and the divergently transcribed SXI1 and SXI2 genes (HD locus). We identified five different mating types with different STE20/SXI allele combinations that together with results of mating experiments demonstrate that K. mangrovensis is not bipolar but instead has a tetrapolar mating system. Sequence and gene analysis for a 43-kb segment of the K. mangrovensis type strain MAT locus revealed remarkable synteny with the homologous K. heveanensisMAT P/R region, providing new insights into slower evolution of MAT loci in the Kwoniella compared to the Cryptococcus clade of the Tremellales. The study of additional isolates from plant substrates in Europe and Botswana using a combination of multilocus sequencing with MAT gene analysis revealed two novel sibling species that we name Kwoniella europaea and Kwoniella botswanensis and which appear to also have tetrapolar mating systems.


Url:
DOI: 10.1128/EC.00065-13
PubMed: 23524993
PubMed Central: 3647770


Affiliations:


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PMC:3647770

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<named-content content-type="genus-species">Kwoniella mangrovensis</named-content>
has been described as a sexual species with a bipolar mating system. Phylogenetic analysis of multiple genes places this species together with
<named-content content-type="genus-species">Kwoniella heveanensis</named-content>
in the
<named-content content-type="genus-species">Kwoniella</named-content>
clade, a sister clade to that containing two pathogenic species of global importance,
<named-content content-type="genus-species">Cryptococcus neoformans</named-content>
and
<named-content content-type="genus-species">Cryptococcus gattii</named-content>
, within the Tremellales. Recent studies defining the mating type loci (
<italic>MAT</italic>
) of species in these clades showed that, with the exception of
<named-content content-type="genus-species">C. neoformans</named-content>
and
<named-content content-type="genus-species">C. gattii</named-content>
, which are bipolar with a single biallelic multigene
<italic>MAT</italic>
locus, several other species feature a tetrapolar mating system with two unlinked loci (homeodomain [HD] and pheromone/receptor [P/R] loci). We characterized several strains from the original study describing
<named-content content-type="genus-species">K. mangrovensis</named-content>
; two
<italic>MAT</italic>
regions were amplified and sequenced: the
<italic>STE20</italic>
gene (P/R locus) and the divergently transcribed
<italic>SXI1</italic>
and
<italic>SXI2</italic>
genes (HD locus). We identified five different mating types with different
<italic>STE20</italic>
/
<italic>SXI</italic>
allele combinations that together with results of mating experiments demonstrate that
<named-content content-type="genus-species">K. mangrovensis</named-content>
is not bipolar but instead has a tetrapolar mating system. Sequence and gene analysis for a 43-kb segment of the
<named-content content-type="genus-species">K. mangrovensis</named-content>
type strain
<italic>MAT</italic>
locus revealed remarkable synteny with the homologous
<named-content content-type="genus-species">K. heveanensis</named-content>
<italic>MAT</italic>
P/R region, providing new insights into slower evolution of
<italic>MAT</italic>
loci in the
<named-content content-type="genus-species">Kwoniella</named-content>
compared to the
<named-content content-type="genus-species">Cryptococcus</named-content>
clade of the Tremellales. The study of additional isolates from plant substrates in Europe and Botswana using a combination of multilocus sequencing with
<italic>MAT</italic>
gene analysis revealed two novel sibling species that we name
<named-content content-type="genus-species">Kwoniella europaea</named-content>
and
<named-content content-type="genus-species">Kwoniella botswanensis</named-content>
and which appear to also have tetrapolar mating systems.</p>
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<article-title>Molecular and Genetic Evidence for a Tetrapolar Mating System in the Basidiomycetous Yeast
<named-content content-type="genus-species">Kwoniella mangrovensis</named-content>
and Two Novel Sibling Species</article-title>
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<name>
<surname>Guerreiro</surname>
<given-names>Marco A.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
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<surname>Springer</surname>
<given-names>Deborah J.</given-names>
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<xref ref-type="aff" rid="aff2">
<sup>b</sup>
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<name>
<surname>Rodrigues</surname>
<given-names>Joana A.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
<xref ref-type="author-notes" rid="FN1">*</xref>
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<contrib contrib-type="author">
<name>
<surname>Rusche</surname>
<given-names>Laura N.</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
<xref ref-type="author-notes" rid="FN1">*</xref>
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<contrib contrib-type="author">
<name>
<surname>Findley</surname>
<given-names>Keisha</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
<xref ref-type="author-notes" rid="FN1">*</xref>
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<name>
<surname>Heitman</surname>
<given-names>Joseph</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
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<sup>a</sup>
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<aff id="aff1">Centro de Recursos Microbiológicos (CREM), Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Caparica, Portugal
<label>a</label>
</aff>
<aff id="aff2">Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina, USA
<label>b</label>
</aff>
</contrib-group>
<author-notes>
<corresp>Address correspondence to Álvaro Fonseca,
<email>amrf@fct.unl.pt</email>
.</corresp>
<fn id="FN1" fn-type="present-address">
<label>*</label>
<p>Present address: Joana A. Rodrigues, Departamento das Ciências e Tecnologia da Biomassa, FCT/UNL, Caparica, Portugal; Laura N. Rusche, Department of Biological Sciences, University at Buffalo, SUNY, Buffalo, New York, USA; Keisha Findley, National Human Genome Research Institute, Bethesda, Maryland, USA.</p>
</fn>
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<month>5</month>
<year>2013</year>
</pub-date>
<volume>12</volume>
<issue>5</issue>
<fpage>746</fpage>
<lpage>760</lpage>
<history>
<date date-type="received">
<day>9</day>
<month>3</month>
<year>2013</year>
</date>
<date date-type="accepted">
<day>15</day>
<month>3</month>
<year>2013</year>
</date>
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<permissions>
<copyright-statement>Copyright © 2013, American Society for Microbiology. All Rights Reserved.</copyright-statement>
<copyright-year>2013</copyright-year>
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<abstract>
<p>
<named-content content-type="genus-species">Kwoniella mangrovensis</named-content>
has been described as a sexual species with a bipolar mating system. Phylogenetic analysis of multiple genes places this species together with
<named-content content-type="genus-species">Kwoniella heveanensis</named-content>
in the
<named-content content-type="genus-species">Kwoniella</named-content>
clade, a sister clade to that containing two pathogenic species of global importance,
<named-content content-type="genus-species">Cryptococcus neoformans</named-content>
and
<named-content content-type="genus-species">Cryptococcus gattii</named-content>
, within the Tremellales. Recent studies defining the mating type loci (
<italic>MAT</italic>
) of species in these clades showed that, with the exception of
<named-content content-type="genus-species">C. neoformans</named-content>
and
<named-content content-type="genus-species">C. gattii</named-content>
, which are bipolar with a single biallelic multigene
<italic>MAT</italic>
locus, several other species feature a tetrapolar mating system with two unlinked loci (homeodomain [HD] and pheromone/receptor [P/R] loci). We characterized several strains from the original study describing
<named-content content-type="genus-species">K. mangrovensis</named-content>
; two
<italic>MAT</italic>
regions were amplified and sequenced: the
<italic>STE20</italic>
gene (P/R locus) and the divergently transcribed
<italic>SXI1</italic>
and
<italic>SXI2</italic>
genes (HD locus). We identified five different mating types with different
<italic>STE20</italic>
/
<italic>SXI</italic>
allele combinations that together with results of mating experiments demonstrate that
<named-content content-type="genus-species">K. mangrovensis</named-content>
is not bipolar but instead has a tetrapolar mating system. Sequence and gene analysis for a 43-kb segment of the
<named-content content-type="genus-species">K. mangrovensis</named-content>
type strain
<italic>MAT</italic>
locus revealed remarkable synteny with the homologous
<named-content content-type="genus-species">K. heveanensis</named-content>
<italic>MAT</italic>
P/R region, providing new insights into slower evolution of
<italic>MAT</italic>
loci in the
<named-content content-type="genus-species">Kwoniella</named-content>
compared to the
<named-content content-type="genus-species">Cryptococcus</named-content>
clade of the Tremellales. The study of additional isolates from plant substrates in Europe and Botswana using a combination of multilocus sequencing with
<italic>MAT</italic>
gene analysis revealed two novel sibling species that we name
<named-content content-type="genus-species">Kwoniella europaea</named-content>
and
<named-content content-type="genus-species">Kwoniella botswanensis</named-content>
and which appear to also have tetrapolar mating systems.</p>
</abstract>
</article-meta>
</front>
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<name sortKey="Findley, Keisha" sort="Findley, Keisha" uniqKey="Findley K" first="Keisha" last="Findley">Keisha Findley</name>
<name sortKey="Fonseca, Alvaro" sort="Fonseca, Alvaro" uniqKey="Fonseca A" first="Álvaro" last="Fonseca">Álvaro Fonseca</name>
<name sortKey="Guerreiro, Marco A" sort="Guerreiro, Marco A" uniqKey="Guerreiro M" first="Marco A." last="Guerreiro">Marco A. Guerreiro</name>
<name sortKey="Heitman, Joseph" sort="Heitman, Joseph" uniqKey="Heitman J" first="Joseph" last="Heitman">Joseph Heitman</name>
<name sortKey="Rodrigues, Joana A" sort="Rodrigues, Joana A" uniqKey="Rodrigues J" first="Joana A." last="Rodrigues">Joana A. Rodrigues</name>
<name sortKey="Rusche, Laura N" sort="Rusche, Laura N" uniqKey="Rusche L" first="Laura N." last="Rusche">Laura N. Rusche</name>
<name sortKey="Springer, Deborah J" sort="Springer, Deborah J" uniqKey="Springer D" first="Deborah J." last="Springer">Deborah J. Springer</name>
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