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Complete Mitochondrial DNA Sequence of the Mucoralean Fusion Parasite Parasitella parasitica

Authors:
Sabrina Ellenberger at Friedrich Schiller University Jena
Sabrina Ellenberger
Anke Burmester at Friedrich Schiller University Jena
Anke Burmester
Johannes Wostemeyer at Friedrich Schiller University Jena
Johannes Wostemeyer
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Abstract

The complete mitochondrial DNA sequence of the Mucor-related fungus Parasitella parasitica has been sequenced. It has a G+C content of 30% and a total length of 83,361 bp. All protein-coding genes normally found in fungi are present in the sequence. A special feature is the remarkably high number of 27 homing endonucleases.
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Complete Mitochondrial DNA Sequence of the Mucoralean Fusion
Parasite Parasitella parasitica
Sabrina Ellenberger, Anke Burmester, Johannes Wöstemeyer
General Microbiology and Microbe Genetics, Friedrich-Schiller-University Jena, Jena, Germany
The complete mitochondrial DNA sequence of the Mucor-related fungus Parasitella parasitica has been sequenced. It has a GⴙC
content of 30% and a total length of 83,361 bp. All protein-coding genes normally found in fungi are present in the sequence. A
special feature is the remarkably high number of 27 homing endonucleases.
Received 28 August 2014 Accepted 3 October 2014 Published 13 November 2014
Citation Ellenberger S, Burmester A, Wöstemeyer J. 2014. Complete mitochondrial DNA sequence of the mucoralean fusion parasite Parasitella parasitica. Genome Announc.
2(6):e00912-14. doi:10.1128/genomeA.00912-14.
Copyright © 2014 Ellenberger et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 3.0 Unported license.
Address correspondence to Sabrina Ellenberger, sabrina.ellenberger@uni-jena.de.
The mucoralean mold Parasitella parasitica is a facultative par-
asite of many zygomycetes. The parasitic lifestyle is accompa-
nied by the fusion of specialized and spatially limited structures at
the hyphal tips with the hosts (1). Parasitism is thus necessarily
linked with unidirectional transport of organelles from the para-
site to the host. The transfer and expression of genes residing in
nuclei have been verified for antibiotic resistance markers (2) and
several genes involved in amino acid biosynthesis (2,3). In order
to initiate the analysis of mitochondrial information after transfer,
we sequenced the mitochondrial DNA (mtDNA) of Parasitella
parasitica.
The Parasitella chondriome was obtained by Illumina sequenc-
ing (Eurofins Genomics, Ebersberg, Germany). The mitochon-
drial information resides on a single circular molecule with a total
length of 83,361 bp. Compared with others, P. parasitica ranges
among those fungi with larger mtDNA. For other zygomycetes,
the lengths differ, with 54,178 bp in Rhizopus oryzae (4), 58,745 bp
in Mortierella verticillata (4), and 62,082 bp in Phycomyces
blakesleeanus (sequence data available at http://www.jgi.doe
.gov/). The obligate parasitic species Zancudomyces culisetae (for-
merly Smittium culisetae) has a comparable chondriome size of
58,654 bp (4).
The Parasitella chondriome harbors genes for those proteins
that are normally found in fungi, the small and large subunit
rRNAs, and it has 26 tRNA genes. On the whole, 41 protein-
coding genes were identified, some of which are split or duplicated
(atp9,cox1,cox2,cox3,cob,nad1,nad5,nad6,trnM, and trnV).
Both DNA strands are transcribed.
The chondriome harbors 27 genes for endonucleases (12 with
LAGLIDADG domains, 8 with LAGLIDADG/HNH domains, and
7 with GYI-YIG domains). Most of them are intron situated and
thus must be addressed as true homing endonucleases. mtDNAs
of other zygomycetes differ in this respect. Lichtheimia ramosa has
no genes for endonucleases (5), R. oryzae harbors 6, P. blakesleea-
nus 12, M. verticillata 6, and the considerably more distantly re-
lated parasitic harpellalean fungus Zancudomyces culisetae has 13
genes for homing nucleases (4).
The data support the idea that introns, rendered mobile by the
acquisition of homing nuclease genes, develop an evolutionary
tendency for enrichment in an organism acting as gene donor.
The mtDNA sequence of P. parasitica constitutes the starting
point for experimental approaches that follow the fate of mito-
chondria after infection. Experiments along this line have become
especially interesting since it is known that mitochondria are uni-
parentally inherited in the zygomycete P. blakesleeanus (6). The
sequence allows the construction of parasite-specific hybridiza-
tion probes to study postinfection behavior directly at the level of
organelles.
Nucleotide sequence accession number. The mtDNA se-
quence is deposited in GenBank under accession no. KM382275.
ACKNOWLEDGMENTS
The gene transfer studies on P. parasitica were funded by DFG grant
WO323/17-1 and by Friedrich-Schiller-Universität Jena. We personally
financed the Illumina sequencing of P. parasitica DNA.
REFERENCES
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of a stable met-2–1 mutant of the zygomycete Absidia glauca by the corre-
sponding wild type allele of the mycoparasite Parasitella parasitica, trans-
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gki199.
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genome sequence of Lichtheimia ramosa (syn. Lichtheimia hongkongensis).
Genome Announc. 2(4):e00644-14. http://dx.doi.org/10.1128/
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Supplementary resource (1)

Parasitella mtDNA addition 17 11.2014
Data
November 2014
Sabrina Ellenberger · Anke Burmester · Johannes Wostemeyer
... By this technique the genome was found to contain approximately 35% repeated DNA, 10% as foldback DNA and 25% other fast-reassociating repeats. Sequencing the genomes of A. glauca (Ellenberger et al. 2015) and P. parasitica (Ellenberger et al. 2014) provided more detailed information. The general characteristics are provided in Table 1. ...
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... glauca: around 4800 in comparison to below 100 in the nuclear assembly, P. parasitica: up to 2269 in comparison to around 100 in the nuclear assembly) and lower GC content (A. glauca: 28% in comparison to 45% in the nuclear assembly, P. parasitica: 31% in comparison to 39% in the nuclear assembly) (Ellenberger et al. 2014(Ellenberger et al. , 2016. ...
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View
... So far there are no experimental data on recombination events between mitochondria in this system. Analysis of the DNA sequences of the chondriomes from P. parasitica (Ellenberger et al. 2014b) and A. glauca (Ellenberger et al. 2016b) do not provide plain and obvious evidence for horizontal gene transfer between the mitochondria involved in fusion parasitism. The two chondriomes differ in size; the Parasitella sequence is approximately 20 kb larger (83,361 bp instead of 63,080 bp) and harbours an unusually high number of intron-situated homing endonuclease genes. ...
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View
Comparative mitochondrial genomics in zygomycetes: Bacteria-like RNase P RNAs, mobile elements and a close source of the group I intron invasion in angiosperms
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  • NUCLEIC ACIDS RES
To generate data for comparative analyses of zygomycete mitochondrial gene expression, we sequenced mtDNAs of three distantly related zygomycetes, Rhizopus oryzae, Mortierella verticillata and Smittium culisetae. They all contain the standard fungal mitochondrial gene set, plus rnpB, the gene encoding the RNA subunit of the mitochondrial RNase P (mtP-RNA) and rps3, encoding ribosomal protein S3 (the latter lacking in R.oryzae). The mtP-RNAs of R.oryzae and of additional zygomycete relatives have the most eubacteria-like RNA structures among fungi. Precise mapping of the 5′ and 3′ termini of the R.oryzae and M.verticillata mtP-RNAs confirms their expression and processing at the exact sites predicted by secondary structure modeling. The 3′ RNA processing of zygomycete mitochondrial mRNAs, SSU-rRNA and mtP-RNA occurs at the C-rich sequence motifs similar to those identified in fission yeast and basidiomycete mtDNAs. The C-rich motifs are included in the mature transcripts, and are likely generated by exonucleolytic trimming of RNA 3′ termini. Zygomycete mtDNAs feature a variety of insertion elements: (i) mtDNAs of R.oryzae and M.verticillata were subject to invasions by double hairpin elements; (ii) genes of all three species contain numerous mobile group I introns, including one that is closest to an intron that invaded angiosperm mtDNAs; and (iii) at least one additional case of a mobile element, characterized by a homing endonuclease insertion between partially duplicated genes [Paquin,B., Laforest,M.J., Forget,L., Roewer,I., Wang,Z., Longcore,J. and Lang,B.F. (1997) Curr. Genet., 31, 380–395]. The combined mtDNA-encoded proteins contain insufficient phylogenetic signal to demonstrate monophyly of zygomycetes.
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Complete mitochondrial genome sequence of Lichtheimia ramosa (syn. Lichtheimia hongkongensis)
  • Jan 2014
  • e00644-14
  • S-Y Leung
  • Y Huang
  • SKP Lau
  • PCY Woo
Leung S-Y, Huang Y, Lau SKP, Woo PCY. 2014. Complete mitochondrial genome sequence of Lichtheimia ramosa (syn. Lichtheimia hongkongensis).
Comparative mitochondrial genomics in zygomycetes: bacteria-like RNase P RNAs, mobile elements and a close source of the group I intron invasion in angiosperms
  • Jan 2005
  • 734-744
  • E Self
  • J Leigh
  • Y Liu
  • I Roewer
  • L Forget
  • BF Lang
Self E, Leigh J, Liu Y, Roewer I, Forget L, Lang BF. 2005. Comparative mitochondrial genomics in zygomycetes: bacteria-like RNase P RNAs, mobile elements and a close source of the group I intron invasion in angiosperms. Nucleic Acids Res. 33:734-744. http://dx.doi.org/10.1093/nar/ gki199.