The mitochondrial genome of the ethanol-metabolizing, wine cellar mold Zasmidium cellare is the smallest for a filamentous ascomycete

Fungi in the class Dothideomycetes often live in extreme environments or have unusual physiology. One of these, the wine cellar mold Zasmidium cellare, produces thick curtains of mycelia in cellars with high humidity, and its ability to metabolize volatile organic compounds is thought to improve air...

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Published inFungal biology Vol. 120; no. 8; pp. 961 - 974
Main Authors Goodwin, Stephen B., McCorison, Cassandra B., Cavaletto, Jessica R., Culley, David E., LaButti, Kurt, Baker, Scott E., Grigoriev, Igor V.
Format Journal Article
LanguageEnglish
Published Netherlands Elsevier Ltd 01.08.2016
Elsevier
Subjects
air quality
alcohols
amino acids
anaerobic conditions
Ascomycota - genetics
Ascomycota - isolation & purification
BASIC BIOLOGICAL SCIENCES
DNA, Mitochondrial - chemistry
DNA, Mitochondrial - genetics
Environmental Microbiology
essential genes
esters
Ethanol - metabolism
Eurotiomycetes
Filamentous
formaldehyde
fungi
Fungus
Genes, Fungal
Genes, Mitochondrial
Genome, Fungal
Genome, Mitochondrial
humidity
introns
Mitochondrial genome
mycelium
Mycosphaerella graminicola
open reading frames
phylogeny
physiology
ribosomal RNA
sequence analysis
Sequence Analysis, DNA
Smallest
Synteny
terminal repeat sequences
transfer RNA
volatile organic compounds
wines
Zasmidium cellare
Fungus
Filamentous
Zasmidium cellare
Smallest
Mitochondrial genome
Synteny
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Abstract Fungi in the class Dothideomycetes often live in extreme environments or have unusual physiology. One of these, the wine cellar mold Zasmidium cellare, produces thick curtains of mycelia in cellars with high humidity, and its ability to metabolize volatile organic compounds is thought to improve air quality. Whether these abilities have affected its mitochondrial genome is not known. To fill this gap, the circular-mapping mitochondrial genome of Z. cellare was sequenced and, at only 23 743 bp, is the smallest reported for a filamentous fungus. Genes were encoded on both strands with a single change of direction, different from most other fungi but consistent with the Dothideomycetes. Other than its small size, the only unusual feature of the Z. cellare mitochondrial genome was two copies of a 110-bp sequence that were duplicated, inverted and separated by approximately 1 kb. This inverted-repeat sequence confused the assembly program but appears to have no functional significance. The small size of the Z. cellare mitochondrial genome was due to slightly smaller genes, lack of introns and non-essential genes, reduced intergenic spacers and very few ORFs relative to other fungi rather than a loss of essential genes. Whether this reduction facilitates its unusual biology remains unknown. [Display omitted] •The Zasmidium cellare mitochondrial genome is the smallest among filamentous fungi.•Reduced genome size was not due to loss of genes for aerobic respiration.•Gene order in fungal mitochondrial genomes is completely scrambled.•Phylogenetic analysis confirms a likely placement of Z. cellare in the Capnodiales.•Inverted repeats can confuse assembly programs.
AbstractList Fungi in the class Dothideomycetes often live in extreme environments or have unusual physiology. One of these, the wine cellar mold Zasmidium cellare, produces thick curtains of mycelia in cellars with high humidity, and its ability to metabolize volatile organic compounds is thought to improve air quality. Whether these abilities have affected its mitochondrial genome is not known. To fill this gap, the circular-mapping mitochondrial genome of Z. cellare was sequenced and, at only 23 743 bp, is the smallest reported for a filamentous fungus. Genes were encoded on both strands with a single change of direction, different from most other fungi but consistent with the Dothideomycetes. Other than its small size, the only unusual feature of the Z. cellare mitochondrial genome was two copies of a 110-bp sequence that were duplicated, inverted and separated by approximately 1 kb. This inverted-repeat sequence confused the assembly program but appears to have no functional significance. The small size of the Z. cellare mitochondrial genome was due to slightly smaller genes, lack of introns and non-essential genes, reduced intergenic spacers and very few ORFs relative to other fungi rather than a loss of essential genes. Whether this reduction facilitates its unusual biology remains unknown.
Fungi in the class Dothideomycetes often live in extreme environments or have unusual physiology. One of these, the wine cellar mold Zasmidium cellare, produces thick curtains of mycelial growth in cellars with high humidity, and its ability to metabolize volatile organic compounds including alcohols, esters and formaldehyde is thought to improve air quality. It grows slowly but appears to outcompete ordinarily faster-growing species under anaerobic conditions.Whether these abilities have affected its mitochondrial genome is not known.To fill this gap, its mitochondrial genome was assembled as part of a whole- genome shotgun-sequencing project.The circular-mapping mitochondrial genome of Z. cellare, at only 23,743 bp, is the smallest yet reported for a filamentous fungus.It contains the complete set of 14 protein-coding genes seen typically in other filamentous fungi, along with genes for large and small ribosomal RNA subunits, 25 predicted tRNA genes capable of decoding all 20 amino acids, and a single open reading frame potentially coding for a protein of unknown function.The Z. cellare mitochondrial genome had genes encoded on both strands with a single change of direction, different from most other fungi but consistent with the Dothideomycetes. The high synteny among mitochondrial genomes of fungi in the Eurotiomycetes broke down almost completely in the Dothideomycetes.Only a low level of microsynteny was observed among protein-coding and tRNA genes in comparison with Mycosphaerella graminicola (synonym Zymoseptoria tritici), the only other fungus in the order Capnodiales with a sequenced mitochondrial genome, involving the three gene pairs atp8-atp9, nad2-nad3, and nad4L-nad5.However, even this low level of microsynteny did not extend to other fungi in the Dothideomycetes and Eurotiomycetes. Phylogenetic analysis of concatenated protein-coding genes confirmed the relationship between Z. cellare and M. graminicola in the Capnodiales, although conclusions were limited due to low sampling density.Other than its small size, the only unusual feature of the Z. cellare mitochondrial genome was two copies of a 110-bp sequence that were duplicated, inverted and separated by approximately 1 kb. This inverted-repeat sequence confused the assembly program but appears to have no functional significance.The small size of the Z. cellare mitochondrial genome was due to slightly smaller genes, lack of introns and non-essential genes, reduced intergenic spaces and very few ORFs relative to other fungi rather than a loss of essential genes. Whether this reduction facilitates its unusual biology remains unknown.
Fungi in the class Dothideomycetes often live in extreme environments or have unusual physiology. One of these, the wine cellar mold Zasmidium cellare, produces thick curtains of mycelia in cellars with high humidity, and its ability to metabolize volatile organic compounds is thought to improve air quality. Whether these abilities have affected its mitochondrial genome is not known. To fill this gap, the circular-mapping mitochondrial genome of Z. cellare was sequenced and, at only 23 743 bp, is the smallest reported for a filamentous fungus. Genes were encoded on both strands with a single change of direction, different from most other fungi but consistent with the Dothideomycetes. Other than its small size, the only unusual feature of the Z. cellare mitochondrial genome was two copies of a 110-bp sequence that were duplicated, inverted and separated by approximately 1 kb. This inverted-repeat sequence confused the assembly program but appears to have no functional significance. The small size of the Z. cellare mitochondrial genome was due to slightly smaller genes, lack of introns and non-essential genes, reduced intergenic spacers and very few ORFs relative to other fungi rather than a loss of essential genes. Whether this reduction facilitates its unusual biology remains unknown.Fungi in the class Dothideomycetes often live in extreme environments or have unusual physiology. One of these, the wine cellar mold Zasmidium cellare, produces thick curtains of mycelia in cellars with high humidity, and its ability to metabolize volatile organic compounds is thought to improve air quality. Whether these abilities have affected its mitochondrial genome is not known. To fill this gap, the circular-mapping mitochondrial genome of Z. cellare was sequenced and, at only 23 743 bp, is the smallest reported for a filamentous fungus. Genes were encoded on both strands with a single change of direction, different from most other fungi but consistent with the Dothideomycetes. Other than its small size, the only unusual feature of the Z. cellare mitochondrial genome was two copies of a 110-bp sequence that were duplicated, inverted and separated by approximately 1 kb. This inverted-repeat sequence confused the assembly program but appears to have no functional significance. The small size of the Z. cellare mitochondrial genome was due to slightly smaller genes, lack of introns and non-essential genes, reduced intergenic spacers and very few ORFs relative to other fungi rather than a loss of essential genes. Whether this reduction facilitates its unusual biology remains unknown.
Fungi in the class Dothideomycetes often live in extreme environments or have unusual physiology. One of these, the wine cellar mold Zasmidium cellare, produces thick curtains of mycelia in cellars with high humidity, and its ability to metabolize volatile organic compounds is thought to improve air quality. Whether these abilities have affected its mitochondrial genome is not known. To fill this gap, the circular-mapping mitochondrial genome of Z. cellare was sequenced and, at only 23 743 bp, is the smallest reported for a filamentous fungus. Genes were encoded on both strands with a single change of direction, different from most other fungi but consistent with the Dothideomycetes. Other than its small size, the only unusual feature of the Z. cellare mitochondrial genome was two copies of a 110-bp sequence that were duplicated, inverted and separated by approximately 1 kb. This inverted-repeat sequence confused the assembly program but appears to have no functional significance. The small size of the Z. cellare mitochondrial genome was due to slightly smaller genes, lack of introns and non-essential genes, reduced intergenic spacers and very few ORFs relative to other fungi rather than a loss of essential genes. Whether this reduction facilitates its unusual biology remains unknown.
Fungi in the class Dothideomycetes often live in extreme environments or have unusual physiology. One of these, the wine cellar mold Zasmidium cellare, produces thick curtains of mycelia in cellars with high humidity, and its ability to metabolize volatile organic compounds is thought to improve air quality. Whether these abilities have affected its mitochondrial genome is not known. To fill this gap, the circular-mapping mitochondrial genome of Z. cellare was sequenced and, at only 23 743 bp, is the smallest reported for a filamentous fungus. Genes were encoded on both strands with a single change of direction, different from most other fungi but consistent with the Dothideomycetes. Other than its small size, the only unusual feature of the Z. cellare mitochondrial genome was two copies of a 110-bp sequence that were duplicated, inverted and separated by approximately 1 kb. This inverted-repeat sequence confused the assembly program but appears to have no functional significance. The small size of the Z. cellare mitochondrial genome was due to slightly smaller genes, lack of introns and non-essential genes, reduced intergenic spacers and very few ORFs relative to other fungi rather than a loss of essential genes. Whether this reduction facilitates its unusual biology remains unknown. [Display omitted] •The Zasmidium cellare mitochondrial genome is the smallest among filamentous fungi.•Reduced genome size was not due to loss of genes for aerobic respiration.•Gene order in fungal mitochondrial genomes is completely scrambled.•Phylogenetic analysis confirms a likely placement of Z. cellare in the Capnodiales.•Inverted repeats can confuse assembly programs.
Author LaButti, Kurt
Baker, Scott E.
Cavaletto, Jessica R.
Goodwin, Stephen B.
McCorison, Cassandra B.
Culley, David E.
Grigoriev, Igor V.
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Snippet Fungi in the class Dothideomycetes often live in extreme environments or have unusual physiology. One of these, the wine cellar mold Zasmidium cellare,...
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SubjectTerms air quality
alcohols
amino acids
anaerobic conditions
Ascomycota - genetics
Ascomycota - isolation & purification
BASIC BIOLOGICAL SCIENCES
DNA, Mitochondrial - chemistry
DNA, Mitochondrial - genetics
Environmental Microbiology
essential genes
esters
Ethanol - metabolism
Eurotiomycetes
Filamentous
formaldehyde
fungi
Fungus
Genes, Fungal
Genes, Mitochondrial
Genome, Fungal
Genome, Mitochondrial
humidity
introns
Mitochondrial genome
mycelium
Mycosphaerella graminicola
open reading frames
phylogeny
physiology
ribosomal RNA
sequence analysis
Sequence Analysis, DNA
Smallest
Synteny
terminal repeat sequences
transfer RNA
volatile organic compounds
wines
Zasmidium cellare
Title The mitochondrial genome of the ethanol-metabolizing, wine cellar mold Zasmidium cellare is the smallest for a filamentous ascomycete
URI https://dx.doi.org/10.1016/j.funbio.2016.05.003
https://www.ncbi.nlm.nih.gov/pubmed/27521628
https://www.proquest.com/docview/1811559732
https://www.proquest.com/docview/2000193641
https://www.osti.gov/biblio/1332605
Volume 120
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