Horizontally acquired genes in early-diverging pathogenic fungi enable the use of host nucleosides and nucleotides
Abstract
Horizontal gene transfer (HGT) among bacteria, archaea, and viruses is widespread, but the extent of transfers from these lineages into eukaryotic organisms is contentious. In this work, we systematically identify hundreds of genes that were likely acquired horizontally from a variety of sources by the early-diverging fungal phyla Microsporidia and Cryptomycota. Interestingly, the Microsporidia have acquired via HGT several genes involved in nucleic acid synthesis and salvage, such as those encoding thymidine kinase (TK), cytidylate kinase, and purine nucleotide phosphorylase. We show that these HGT-derived nucleic acid synthesis genes tend to function at the interface between the metabolic networks of the host and pathogen. Thus, these genes likely play vital roles in diversifying the useable nucleic acid components available to the intracellular parasite, often through the direct capture of resources from the host. Using an in vivo viability assay, we also demonstrate that one of these genes, TK, encodes an enzyme that is capable of activating known prodrugs to their active form, which suggests a possible treatment route for microsporidiosis. We further argue that interfacial genes with well-understood activities, especially those horizontally transferred from bacteria or viruses, could provide medical treatments for microsporidian infections.
- Authors:
-
[2];
- Univ. of Wisconsin, Madison, WI (United States). Great Lakes Bioenergy Research Center (GLBRC), Wisconsin Energy Inst., Genome Center of Wisconsin, J.F. Crow Inst. for the Study of Evolution and Lab. of Genetics
- Vanderbilt Univ., Nashville, TN (United States). Dept. of Biological Sciences
- Publication Date:
- Research Org.:
- Univ. of Wisconsin, Madison, WI (United States)
- Sponsoring Org.:
- USDOE; USDA; National Science Foundation (NSF); Alexander von Humboldt Foundation; Pew Charitable Trusts
- OSTI Identifier:
- 1469103
- Grant/Contract Number:
- FC02-07ER64494; IOS-1401682; DEB-1442113; DEB-1253634; DEB-1442148; 1003258
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Volume: 113; Journal Issue: 15; Journal ID: ISSN 0027-8424
- Publisher:
- National Academy of Sciences, Washington, DC (United States)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; horizontal gene transfer; Microsporidia; Cryptomycota; thymidine kinase; metabolic networks
Citation Formats
Alexander, William G., Wisecaver, Jennifer H., Rokas, Antonis, and Hittinger, Chris Todd. Horizontally acquired genes in early-diverging pathogenic fungi enable the use of host nucleosides and nucleotides. United States: N. p., 2016.
Web. doi:10.1073/pnas.1517242113.
Alexander, William G., Wisecaver, Jennifer H., Rokas, Antonis, & Hittinger, Chris Todd. Horizontally acquired genes in early-diverging pathogenic fungi enable the use of host nucleosides and nucleotides. United States. https://doi.org/10.1073/pnas.1517242113
Alexander, William G., Wisecaver, Jennifer H., Rokas, Antonis, and Hittinger, Chris Todd. Tue .
"Horizontally acquired genes in early-diverging pathogenic fungi enable the use of host nucleosides and nucleotides". United States. https://doi.org/10.1073/pnas.1517242113. https://www.osti.gov/servlets/purl/1469103.
@article{osti_1469103,
title = {Horizontally acquired genes in early-diverging pathogenic fungi enable the use of host nucleosides and nucleotides},
author = {Alexander, William G. and Wisecaver, Jennifer H. and Rokas, Antonis and Hittinger, Chris Todd},
abstractNote = {Horizontal gene transfer (HGT) among bacteria, archaea, and viruses is widespread, but the extent of transfers from these lineages into eukaryotic organisms is contentious. In this work, we systematically identify hundreds of genes that were likely acquired horizontally from a variety of sources by the early-diverging fungal phyla Microsporidia and Cryptomycota. Interestingly, the Microsporidia have acquired via HGT several genes involved in nucleic acid synthesis and salvage, such as those encoding thymidine kinase (TK), cytidylate kinase, and purine nucleotide phosphorylase. We show that these HGT-derived nucleic acid synthesis genes tend to function at the interface between the metabolic networks of the host and pathogen. Thus, these genes likely play vital roles in diversifying the useable nucleic acid components available to the intracellular parasite, often through the direct capture of resources from the host. Using an in vivo viability assay, we also demonstrate that one of these genes, TK, encodes an enzyme that is capable of activating known prodrugs to their active form, which suggests a possible treatment route for microsporidiosis. We further argue that interfacial genes with well-understood activities, especially those horizontally transferred from bacteria or viruses, could provide medical treatments for microsporidian infections.},
doi = {10.1073/pnas.1517242113},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 15,
volume = 113,
place = {United States},
year = {Tue Mar 29 00:00:00 EDT 2016},
month = {Tue Mar 29 00:00:00 EDT 2016}
}
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Works referenced in this record:
Structures of Escherichia coli CMP kinase alone and in complex with CDP: a new fold of the nucleoside monophosphate binding domain and insights into cytosine nucleotide specificity
journal, December 1998
- Briozzo, Pierre; Golinelli-Pimpaneau, Béatrice; Gilles, Anne-Marie
- Structure, Vol. 6, Issue 12
The Role of Herpes Simplex Virus Type 1 Thymidine Kinase in Pathogenesis
journal, April 1989
- Efstathiou, S.; Kemp, S.; Darby, G.
- Journal of General Virology, Vol. 70, Issue 4
The Genome of the Obligate Intracellular Parasite Trachipleistophora hominis: New Insights into Microsporidian Genome Dynamics and Reductive Evolution
journal, October 2012
- Heinz, Eva; Williams, Tom A.; Nakjang, Sirintra
- PLoS Pathogens, Vol. 8, Issue 10
5-Fluorouracil: mechanisms of action and clinical strategies
journal, May 2003
- Longley, Daniel B.; Harkin, D. Paul; Johnston, Patrick G.
- Nature Reviews Cancer, Vol. 3, Issue 5
Rediscovery of Nucleophaga amoebae, a novel member of the Rozellomycota
journal, September 2014
- Corsaro, Daniele; Walochnik, Julia; Venditti, Danielle
- Parasitology Research, Vol. 113, Issue 12
Identification of transcriptional signals in Encephalitozoon cuniculi widespread among Microsporidia phylum: support for accurate structural genome annotation
journal, January 2009
- Peyretaillade, Eric; Gonçalves, Olivier; Terrat, Sébastien
- BMC Genomics, Vol. 10, Issue 1
Horizontal gene acquisitions by eukaryotes as drivers of adaptive evolution: Insights & Perspectives
journal, November 2013
- Schönknecht, Gerald; Weber, Andreas P. M.; Lercher, Martin J.
- BioEssays, Vol. 36, Issue 1
Genomic analyses of the microsporidian Nosema ceranae, an emergent pathogen of honey bees
text, January 2009
- Cornman, R. Scott; Chen, Yan Ping; Schatz, Michael C.
- Columbia University
Morphological, Molecular, and Phylogenetic Characterization of Nosema ceranae , a Microsporidian Parasite Isolated from the European Honey Bee, Apis mellifera
journal, March 2009
- Chen, Yanping P.; Evans, Jay D.; Murphy, Charles
- Journal of Eukaryotic Microbiology, Vol. 56, Issue 2
Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences
journal, May 2006
- Li, W.; Godzik, A.
- Bioinformatics, Vol. 22, Issue 13
Clinical Manifestations and Treatment Considerations of Herpes Simplex Virus Infection
journal, October 2002
- Simmons, Anthony
- The Journal of Infectious Diseases, Vol. 186, Issue s1
Horizontal gene transfer in eukaryotic evolution
journal, August 2008
- Keeling, Patrick J.; Palmer, Jeffrey D.
- Nature Reviews Genetics, Vol. 9, Issue 8
Microsporidian genome analysis reveals evolutionary strategies for obligate intracellular growth
journal, July 2012
- Cuomo, C. A.; Desjardins, C. A.; Bakowski, M. A.
- Genome Research, Vol. 22, Issue 12
Probing the Mechanistic Consequences of 5-Fluorine Substitution on Cytidine Nucleotide Analogue Incorporation by HIV-1 Reverse Transcriptase
journal, June 2003
- Ray, Adrian S.; Schinazi, Raymond F.; Murakami, Eisuke
- Antiviral Chemistry and Chemotherapy, Vol. 14, Issue 3
Whole genome evaluation of horizontal transfers in the pathogenic fungus Aspergillus fumigatus
journal, January 2010
- Mallet, Ludovic V.; Becq, Jennifer; Deschavanne, Patrick
- BMC Genomics, Vol. 11, Issue 1
Microsporidia: Biology and Evolution of Highly Reduced Intracellular Parasites
journal, October 2002
- Keeling, Patrick J.; Fast, Naomi M.
- Annual Review of Microbiology, Vol. 56, Issue 1
PCR Mutagenesis and Gap Repair in Yeast
book, January 2014
- Weir, Mark; Keeney, Jill B.
- Methods in Molecular Biology
Invasion and intracellular survival by protozoan parasites: Parasite invasion strategies
journal, February 2011
- David Sibley, L.
- Immunological Reviews, Vol. 240, Issue 1
Human thymidine kinase 1. Regulation in normal and malignant cells
journal, January 1995
- Munch-Petersen, B.; Cloos, L.; Jensen, H. K.
- Advances in Enzyme Regulation, Vol. 35
Evolution and Variation of the Yeast (Saccharomyces) Genome
journal, April 2000
- Mortimer, R. K.
- Genome Research, Vol. 10, Issue 4
Genome-scale model reconstruction of the methylotrophic yeast Ogataea polymorpha
text, January 2021
- Liebal, Ulf Winfried; Fabry, Brigida A.; Ravikrishnan, Aarthi
- RWTH Aachen University
Characterization of Herpes Simplex Virus type 1 thymidine kinase mutants engineered for improved ganciclovir or acyclovir activity
journal, September 2002
- Kokoris, Mark S.; Black, Margaret E.
- Protein Science, Vol. 11, Issue 9
Genomic Analyses of the Microsporidian Nosema ceranae, an Emergent Pathogen of Honey Bees
journal, June 2009
- Cornman, R. Scott; Chen, Yan Ping; Schatz, Michael C.
- PLoS Pathogens, Vol. 5, Issue 6
Gain and loss of multiple functionally related, horizontally transferred genes in the reduced genomes of two microsporidian parasites
journal, July 2012
- Pombert, J. -F.; Selman, M.; Burki, F.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 31
Reduction and Expansion in Microsporidian Genome Evolution: New Insights from Comparative Genomics
journal, November 2013
- Nakjang, Sirintra; Williams, Tom A.; Heinz, Eva
- Genome Biology and Evolution, Vol. 5, Issue 12
Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi
journal, November 2001
- Katinka, Michaël D.; Duprat, Simone; Cornillot, Emmanuel
- Nature, Vol. 414, Issue 6862
The role of floxuridine in metastatic liver disease
journal, April 2009
- Power, D. G.; Kemeny, N. E.
- Molecular Cancer Therapeutics, Vol. 8, Issue 5
Multiple Comparisons of Log-Likelihoods with Applications to Phylogenetic Inference
journal, August 1999
- Shimodaira, H.; Hasegawa, M.
- Molecular Biology and Evolution, Vol. 16, Issue 8
Horizontal Transfer and Death of a Fungal Secondary Metabolic Gene Cluster
journal, January 2012
- Campbell, Matthew A.; Rokas, Antonis; Slot, Jason C.
- Genome Biology and Evolution, Vol. 4, Issue 3
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models
journal, August 2006
- Stamatakis, Alexandros
- Bioinformatics, Vol. 22, Issue 21
Adaptive evolution of bacterial metabolic networks by horizontal gene transfer
journal, November 2005
- Pál, Csaba; Papp, Balázs; Lercher, Martin J.
- Nature Genetics, Vol. 37, Issue 12
The Evolution of Fungal Metabolic Pathways
journal, December 2014
- Wisecaver, Jennifer H.; Slot, Jason C.; Rokas, Antonis
- PLoS Genetics, Vol. 10, Issue 12
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability
journal, January 2013
- Katoh, K.; Standley, D. M.
- Molecular Biology and Evolution, Vol. 30, Issue 4
Transcriptome analysis of the parasite Encephalitozoon cuniculi: an in-depth examination of pre-mRNA splicing in a reduced eukaryote
text, January 2013
- Grisdale, Cameron J.; Bowers, Lisa C.; Didier, Elizabeth S.
- BioMed Central
Patterns of prokaryotic lateral gene transfers affecting parasitic microbial eukaryotes
journal, January 2013
- Alsmark, Cecilia; Foster, Peter G.; Sicheritz-Ponten, Thomas
- Genome Biology, Vol. 14, Issue 2
Microsporidiosis: Enterocytozoon bieneusi in domesticated and wild animals
journal, June 2011
- Santín, Mónica; Fayer, Ronald
- Research in Veterinary Science, Vol. 90, Issue 3
Novel basal, fungal lineages from freshwater phytoplankton and lake samples: Novel fungal lineages in lakes
journal, March 2015
- Ishida, Seiji; Nozaki, Daiki; Grossart, Hans-Peter
- Environmental Microbiology Reports, Vol. 7, Issue 3
Acquisition of prokaryotic genes by fungal genomes
journal, January 2010
- Marcet-Houben, Marina; Gabaldón, Toni
- Trends in Genetics, Vol. 26, Issue 1
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses
journal, June 2009
- Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T.
- Bioinformatics, Vol. 25, Issue 15
The Genome of Spraguea lophii and the Basis of Host-Microsporidian Interactions
journal, August 2013
- Campbell, Scott E.; Williams, Tom A.; Yousuf, Asim
- PLoS Genetics, Vol. 9, Issue 8
Horizontal Transfer, Not Duplication, Drives the Expansion of Protein Families in Prokaryotes
journal, January 2011
- Treangen, Todd J.; Rocha, Eduardo P. C.
- PLoS Genetics, Vol. 7, Issue 1
Phosphorylation of Cytidine, Deoxycytidine, and Their Analog Monophosphates by Human UMP/CMP Kinase Is Differentially Regulated by ATP and Magnesium
journal, November 2004
- Hsu, Chih-Hung; Liou, Jieh-Yuan; Dutschman, Ginger E.
- Molecular Pharmacology, Vol. 67, Issue 3
Ten reasons to exclude viruses from the tree of life
journal, March 2009
- Moreira, David; López-García, Purificación
- Nature Reviews Microbiology, Vol. 7, Issue 4
Microsporidiosis: An emerging and opportunistic infection in humans and animals
journal, April 2005
- Didier, Elizabeth S.
- Acta Tropica, Vol. 94, Issue 1
A novel route for ATP acquisition by the remnant mitochondria of Encephalitozoon cuniculi
journal, April 2008
- Tsaousis, Anastasios D.; Kunji, Edmund R. S.; Goldberg, Alina V.
- Nature, Vol. 453, Issue 7194
Systematic discovery of pseudomonad genetic factors involved in sensitivity to tailocins
journal, March 2021
- Carim, Sean; Azadeh, Ashley L.; Kazakov, Alexey E.
- The ISME Journal, Vol. 15, Issue 8
Fungal metabolic gene clusters—caravans traveling across genomes and environments
journal, March 2015
- Wisecaver, Jennifer H.; Rokas, Antonis
- Frontiers in Microbiology, Vol. 6
Acquisition of an animal gene by microsporidian intracellular parasites
journal, August 2011
- Selman, Mohammed; Pombert, Jean-François; Solter, Leellen
- Current Biology, Vol. 21, Issue 15
Gene transfer in the evolution of parasite nucleotide biosynthesis
journal, February 2004
- Striepen, B.; Pruijssers, A. J. P.; Huang, J.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 9
Ubiquitin-Mediated Response to Microsporidia and Virus Infection in C. elegans
journal, June 2014
- Bakowski, Malina A.; Desjardins, Christopher A.; Smelkinson, Margery G.
- PLoS Pathogens, Vol. 10, Issue 6
MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004
- Edgar, R. C.
- Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
Shared Signatures of Parasitism and Phylogenomics Unite Cryptomycota and Microsporidia
journal, August 2013
- James, Timothy Y.; Pelin, Adrian; Bonen, Linda
- Current Biology, Vol. 23, Issue 16
High-Efficiency Genome Editing and Allele Replacement in Prototrophic and Wild Strains of Saccharomyces
journal, September 2014
- Alexander, W. G.; Doering, D. T.; Hittinger, C. T.
- Genetics, Vol. 198, Issue 3, p. 859-866
Python for Scientific Computing
journal, January 2007
- Oliphant, Travis E.
- Computing in Science & Engineering, Vol. 9, Issue 3
MycoCosm portal: gearing up for 1000 fungal genomes
journal, December 2013
- Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet
- Nucleic Acids Research, Vol. 42, Issue D1
Massive Horizontal Gene Transfer in Bdelloid Rotifers
journal, May 2008
- Gladyshev, E. A.; Meselson, M.; Arkhipova, I. R.
- Science, Vol. 320, Issue 5880
Transcriptome analysis of the parasite Encephalitozoon cuniculi: an in-depth examination of pre-mRNA splicing in a reduced eukaryote
journal, January 2013
- Grisdale, Cameron J.; Bowers, Lisa C.; Didier, Elizabeth S.
- BMC Genomics, Vol. 14, Issue 1
Codon Optimality Is a Major Determinant of mRNA Stability
journal, March 2015
- Presnyak, Vladimir; Alhusaini, Najwa; Chen, Ying-Hsin
- Cell, Vol. 160, Issue 6
Horizontal gene transfer in eukaryotes: The weak‐link model
journal, August 2013
- Huang, Jinling
- BioEssays, Vol. 35, Issue 10
Works referencing / citing this record:
Genome wide analysis of the transition to pathogenic lifestyles in Magnaporthales fungi
journal, April 2018
- Zhang, Ning; Cai, Guohong; Price, Dana C.
- Scientific Reports, Vol. 8, Issue 1
Evolutionary Genomics of Metchnikovella incurvata (Metchnikovellidae): An Early Branching Microsporidium
journal, September 2018
- Galindo, Luis Javier; Torruella, Guifré; Moreira, David
- Genome Biology and Evolution, Vol. 10, Issue 10
Resurrection of Ancestral Malate Dehydrogenases Reveals the Evolutionary History of Halobacterial Proteins: Deciphering Gene Trajectories and Changes in Biochemical Properties
journal, May 2021
- Blanquart, Samuel; Groussin, Mathieu; Le Roy, Aline
- Molecular Biology and Evolution, Vol. 38, Issue 9
New genome assemblies reveal patterns of domestication and adaptation across Brettanomyces (Dekkera) species
journal, March 2020
- Roach, Michael J.; Borneman, Anthony R.
- BMC Genomics, Vol. 21, Issue 1
Environment-dependent fitness gains can be driven by horizontal gene transfer of transporter-encoding genes
journal, March 2019
- Milner, David S.; Attah, Victoria; Cook, Emily
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 12
Eukaryotic Acquisition of a Bacterial Operon
journal, August 2018
- Kominek, Jacek; Doering, Drew T.; Opulente, Dana A.
- Cell
Evidence for loss and reacquisition of alcoholic fermentation in a fructophilic yeast lineage
journal, April 2018
- Gonçalves, Carla; Wisecaver, Jennifer H.; Kominek, Jacek
- eLife, Vol. 7
Clarifying the Relationships between Microsporidia and Cryptomycota
journal, April 2018
- Bass, David; Czech, Lucas; Williams, Bryony A. P.
- Journal of Eukaryotic Microbiology, Vol. 65, Issue 6
Functional horizontal gene transfer from bacteria to eukaryotes
journal, November 2017
- Husnik, Filip; McCutcheon, John P.
- Nature Reviews Microbiology, Vol. 16, Issue 2
Environment-dependent fitness gains can be driven by horizontal gene transfer of transporter-encoding genes
journal, March 2019
- Milner, David S.; Attah, Victoria; Cook, Emily
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 12
Quantitative Proteomic Analysis of Germination of Nosema bombycis Spores under Extremely Alkaline Conditions
journal, September 2016
- Liu, Han; Chen, Bosheng; Hu, Sirui
- Frontiers in Microbiology, Vol. 7
Clarifying the Relationships between Microsporidia and Cryptomycota
journal, April 2018
- Bass, David; Czech, Lucas; Williams, Bryony A. P.
- Journal of Eukaryotic Microbiology, Vol. 65, Issue 6
Adaptive divergence in wine yeasts and their wild relatives suggests a prominent role for introgressions and rapid evolution at noncoding sites
journal, March 2017
- Almeida, Pedro; Barbosa, Raquel; Bensasson, Douda
- Molecular Ecology, Vol. 26, Issue 7
Ancestral Function and Diversification of a Horizontally Acquired Oomycete Carboxylic Acid Transporter
journal, April 2018
- Savory, Fiona R.; Milner, David S.; Miles, Daniel C.
- Molecular Biology and Evolution, Vol. 35, Issue 8
Microsporidia: Why Make Nucleotides if You Can Steal Them?
journal, November 2016
- Dean, Paul; Hirt, Robert P.; Embley, T. Martin
- PLOS Pathogens, Vol. 12, Issue 11
Evolutionary Genomics of Metchnikovella incurvata (Metchnikovellidae): An Early Branching Microsporidium
journal, September 2018
- Galindo, Luis Javier; Torruella, Guifré; Moreira, David
- Genome Biology and Evolution, Vol. 10, Issue 10
Genome wide analysis of the transition to pathogenic lifestyles in Magnaporthales fungi
journal, April 2018
- Zhang, Ning; Cai, Guohong; Price, Dana C.
- Scientific Reports, Vol. 8, Issue 1
Fungal evolution: diversity, taxonomy and phylogeny of the Fungi
journal, October 2019
- Naranjo‐Ortiz, Miguel A.; Gabaldón, Toni
- Biological Reviews, Vol. 94, Issue 6
Horizontal gene transfer in the human and skin commensal Malassezia : a bacterially-derived flavohemoglobin is required for NO resistance and host interaction
journal, April 2020
- Ianiri, Giuseppe; Coelho, Marco A.; Ruchti, Fiorella
- Proceedings of the National Academy of Sciences
Quantitative Proteomic Analysis of Germination of Nosema bombycis Spores under Extremely Alkaline Conditions
journal, September 2016
- Liu, Han; Chen, Bosheng; Hu, Sirui
- Frontiers in Microbiology, Vol. 7
Host–symbiont–pathogen interactions in blood-feeding parasites: nutrition, immune cross-talk and gene exchange
journal, April 2018
- Husnik, Filip
- Parasitology, Vol. 145, Issue 10
A new chromosomal rearrangement improves the adaptation of wine yeasts to sulfite
journal, March 2019
- García‐Ríos, Estéfani; Nuévalos, Marcos; Barrio, Eladio
- Environmental Microbiology, Vol. 21, Issue 5
The Genome of the Fungal Pathogen Verticillium dahliae Reveals Extensive Bacterial to Fungal Gene Transfer
journal, February 2019
- Shi-Kunne, Xiaoqian; van Kooten, Mathijs; Depotter, Jasper R. L.
- Genome Biology and Evolution, Vol. 11, Issue 3
The genome of the fungal pathogen Verticillium dahliae reveals extensive bacterial to fungal gene transfer
journal, December 2018
- Shi-Kunne, Xiaoqian; van Kooten, Mathijs; Depotter, Jasper R. L.
- Genome Biology and Evolution