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Title: Evolution of the sex-Related Locus and Genomic Features Shared in Microsporidia and Fungi

Journal Article · · PLoS ONE
 [1];  [2];  [2];  [1];  [2];  [1]
  1. Duke University, Durham, NC (United States)
  2. University of British Columbia, Vancouver, BC (Canada)

Microsporidia are obligate intracellular, eukaryotic pathogens that infect a wide range of animals from nematodes to humans, and in some cases, protists. The preponderance of evidence as to the origin of the microsporidia reveals a close relationship with the fungi, either within the kingdom or as a sister group to it. Recent phylogenetic studies and gene order analysis suggest that microsporidia share a particularly close evolutionary relationship with the zygomycetes. Here we expanded this analysis and also examined a putative sex-locus for variability between microsporidian populations. Whole genome inspection reveals a unique syntenic gene pair (RPS9-RPL21) present in the vast majority of fungi and the microsporidians but not in other eukaryotic lineages. Two other unique gene fusions (glutamyl-prolyl tRNA synthetase and ubiquitin-ribosomal subunit S30) that are present in metazoans, choanoflagellates, and filasterean opisthokonts are unfused in the fungi and microsporidians. One locus previously found to be conserved in many microsporidian genomes is similar to the sex locus of zygomycetes in gene order and architecture. Both sex-related and sex loci harbor TPT, HMG, and RNA helicase genes forming a syntenic gene cluster. We sequenced and analyzed the sex-related locus in 11 different Encephalitozoon cuniculi isolates and the sibling species E. intestinalis (3 isolates) and E. hellem (1 isolate). There was no evidence for an idiomorphic sex-related locus in this Encephalitozoon species sample. According to sequence-based phylogenetic analyses, the TPT and RNA helicase genes flanking the HMG genes are paralogous rather than orthologous between zygomycetes and microsporidians. The unique genomic hallmarks between microsporidia and fungi are independent of sequence based phylogenetic comparisons and further contribute to define the borders of the fungal kingdom and support the classification of microsporidia as unusual derived fungi. And the sex/sex-related loci appear to have been subject to frequent gene conversion and translocations in microsporidia and zygomycetes.

Research Organization:
Duke Univ., Durham, NC (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH); Canadian Institute for Health Research; Molecular Mycology Pathogenesis Training Program; Swiss National Science Foundation (SNSF)
Grant/Contract Number:
AC02-05CH11231; AI50113; AI052080; PA00P3_124166
OSTI ID:
1627407
Journal Information:
PLoS ONE, Vol. 5, Issue 5; ISSN 1932-6203
Publisher:
Public Library of ScienceCopyright Statement
Country of Publication:
United States
Language:
English

References (83)

αADα Hybrids of Cryptococcus neoformans: Evidence of Same-Sex Mating in Nature and Hybrid Fitness journal October 2007
The Kingdoms of Organisms journal December 1938
Congruent evidence from α-tubulin and β-tubulin gene phylogenies for a zygomycete origin of microsporidia journal April 2003
Characterization of Encephalitozoon (Septata) intestinalis Isolates Cultured from Nasal Mucosa and Bronchoalveolar Lavage Fluids of Two AIDS Patients journal January 1996
Microsporidia are related to Fungi: Evidence from the largest subunit of RNA polymerase II and other proteins journal January 1999
The GAIT system: a gatekeeper of inflammatory gene expression journal July 2009
Evolution of the MAT locus and its Ho endonuclease in yeast species journal January 2004
Fungal sex genes—searching for the ancestors journal August 2008
Microsporidia: Biology and Evolution of Highly Reduced Intracellular Parasites journal October 2002
Love the one you're with journal August 2009
The Fungi journal September 2009
Genomic Analyses of the Microsporidian Nosema ceranae, an Emergent Pathogen of Honey Bees journal June 2009
Mechanistic Plasticity of Sexual Reproduction and Meiosis in the Candida Pathogenic Species Complex journal June 2009
Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi journal November 2001
The rapid evolution of reproductive proteins journal February 2002
The homeobox genes of Encephalitozoon cuniculi (Microsporidia) reveal a putative mating-type locus journal December 2002
Barrier Activity in Candida albicans Mediates Pheromone Degradation and Promotes Mating journal April 2007
A mitochondrial remnant in the microsporidian Trachipleistophora hominis journal August 2002
Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes journal March 1987
Microsporidia: a journey through radical taxonomical revisions journal February 2009
Phylogenetic Analysis of the Complete Genome Sequence of Encephalitozoon cuniculi Supports the Fungal Origin of Microsporidia and Reveals a High Frequency of Fast-Evolving Genes journal December 2004
Microsporidian polar tube proteins: Highly divergent but closely linked genes encode PTP1 and PTP2 in members of the evolutionarily distant Antonospora and Encephalitozoon groups journal September 2005
Five Questions about Microsporidia journal September 2009
Identification of the MATa mating-type locus of Cryptococcus neoformans reveals a serotype A MATa strain thought to have been extinct journal December 2000
Microsporidian Encephalitozoon cuniculi, a unicellular eukaryote with an unusual chromosomal dispersion of ribosomal genes and a LSU rRNA reduced to the universal core journal August 1998
Phylogenomic analyses predict sistergroup relationship of nucleariids and Fungi and paraphyly of zygomycetes with significant support journal January 2009
Alpha-tubulin from early-diverging eukaryotic lineages and the evolution of the tubulin family journal December 1996
Opaque cells signal white cells to form biofilms in Candida albicans journal April 2006
Fractionation of Sporogonial Stages of the Microsporidian Encephalitozoon cuniculi by Percoll® Gradients journal July 1999
Fine Structure of a New Human Microsporidian, Encephalitozoon hellem , in Culture journal September 1991
An Expanded Inventory of Conserved Meiotic Genes Provides Evidence for Sex in Trichomonas vaginalis journal August 2008
Homothallic and heterothallic mating in the opportunistic pathogen Candida albicans journal August 2009
Evolution of the Mating-Type Locus: The Basidiomycetes book April 2014
Therapeutic strategies for human microsporidia infections journal June 2005
The kingdoms of organisms journal December 1986
Convergent Evolution of Chromosomal Sex-Determining Regions in the Animal and Fungal Kingdoms journal November 2004
Assessing the microsporidia-fungi relationship: Combined phylogenetic analysis of eight genes journal June 2006
Sexual reproduction between partners of the same mating type in Cryptococcus neoformans journal April 2005
The signature of balancing selection: Fungal mating compatibility gene evolution journal August 1999
Genomic analyses of the microsporidian Nosema ceranae, an emergent pathogen of honey bees text January 2009
WHEP Domains Direct Noncanonical Function of Glutamyl-Prolyl tRNA Synthetase in Translational Control of Gene Expression journal March 2008
Evolution of pathogenicity and sexual reproduction in eight Candida genomes journal May 2009
Love the one you're with journal December 2016
Karyogamy and meiosis in an Amblyospora sp. (Microspora) in the mosquito Culex salinarius journal July 1984
The Saccharomyces cerevisiae BAR1 gene encodes an exported protein with homology to pepsin. journal January 1988
Sexual reproduction and dimorphism in the pathogenic basidiomycetes journal March 2009
Reconstructing the early evolution of Fungi using a six-gene phylogeny journal October 2006
Sex-Specific Homeodomain Proteins Sxi1α and Sxi2a Coordinately Regulate Sexual Development in Cryptococcus neoformans journal March 2005
Draft genome sequence of the Daphnia pathogen Octosporea bayeri: insights into the gene content of a large microsporidian genome and a model for host-parasite interactions text January 2009
Multiple losses of sex within a single genus of Microsporidia journal January 2007
Genomic Survey of the Non-Cultivatable Opportunistic Human Pathogen, Enterocytozoon bieneusi journal January 2009
Life cycle of Amblyospora dyxenoides sp. nov. in the mosquito Culex annulirostris and the copepod Mesocyclops albicans journal January 1988
Microsporidia Are Natural Intracellular Parasites of the Nematode Caenorhabditis elegans journal December 2008
Phylogenetic Analysis of β-Tubulin Sequences from Amitochondrial Protozoa journal April 1996
Multigene Phylogeny of Choanozoa and the Origin of Animals journal May 2008
Love the One You're With journal August 2003
Evolutionary Biology: Genomic Clues to Original Sex in Fungi journal March 2008
Identification of the sex genes in an early diverged fungus journal January 2008
The Ashbya gossypii Genome as a Tool for Mapping the Ancient Saccharomyces cerevisiae Genome journal April 2004
Using a meiosis detection toolkit to investigate ancient asexual “scandals” and the evolution of sex journal January 2008
Evidence from Beta-Tubulin Phylogeny that Microsporidia Evolved from Within the Fungi journal January 2000
Evolutionary Biology: Microsporidia Sex — A Missing Link to Fungi journal November 2008
The divergence-homogenization duality in the evolution of the b1 mating type gene of Coprinus cinereus journal July 1999
Draft genome sequence of the Daphnia pathogen Octosporea bayeri: insights into the gene content of a large microsporidian genome and a model for host-parasite interactions journal January 2009
Diploids in the Cryptococcus neoformans Serotype A Population Homozygous for the α Mating Type Originate via Unisexual Mating journal January 2009
The amelogenin loci span an ancient pseudoautosomal boundary in diverse mammalian species journal April 2003
Microsporidia Evolved from Ancestral Sexual Fungi journal November 2008
Evidence for balancing selection operating at the het-c heterokaryon incompatibility locus in a group of filamentous fungi journal October 1998
A Simple, Fast, and Accurate Algorithm to Estimate Large Phylogenies by Maximum Likelihood journal October 2003
Signs of sex: what we know and how we know it journal April 2009
The microsporidian polar tube: A highly specialised invasion organelle journal August 2005
Sex: Deviant Mating in Yeast journal July 2009
Not Just Because It Is There: Aminoacyl-tRNA Synthetases Gain Control of the Cell journal April 2008
A gene fusion event in the evolution of aminoacyl-tRNA synthetases journal March 2000
Identification and characterization of three Encephalitozoon cuniculi strains journal November 1995
A slippery boundary journal April 2003
Fungal Sex and Pathogenesis journal January 2010
Evolution of the Mating Type Locus: Insights Gained from the Dimorphic Primary Fungal Pathogens Histoplasma capsulatum, Coccidioides immitis, and Coccidioides posadasii journal March 2007
Mating-Type Locus of Cryptococcus neoformans: a Step in the Evolution of Sex Chromosomes journal October 2002
Identification of a New Spore Wall Protein from Encephalitozoon cuniculi journal January 2006
Genotyping Encephalitozoon cuniculi by Multilocus Analyses of Genes with Repetitive Sequences journal June 2001
Correction: An Expanded Inventory of Conserved Meiotic Genes Provides Evidence for Sex in Trichomonas vaginalis journal September 2008
Detecting changes in real-world objects: The relationship between visual long-term memory and change blindness journal January 2009

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