Eukaryotic Acquisition of a Bacterial Operon
Abstract
Operons are a hallmark of bacterial genomes, where they allow concerted expression of functionally related genes as single polycistronic transcripts. They are rare in eukaryotes, where each gene usually drives expression of its own independent messenger RNAs. Here, we report the horizontal operon transfer of a siderophore biosynthesis pathway from relatives of Escherichia coli into a group of budding yeast taxa. We further show that the co-linearly arranged secondary metabolism genes are expressed, exhibit eukaryotic transcriptional features, and enable the sequestration and uptake of iron. After transfer, several genetic changes occurred during subsequent evolution, including the gain of new transcription start sites that were sometimes within protein-coding sequences, acquisition of polyadenylation sites, structural rearrangements, and integration of eukaryotic genes into the cluster. We conclude that the genes were likely acquired as a unit, modified for eukaryotic gene expression, and maintained by selection to adapt to the highly competitive, iron-limited environment.
- Authors:
-
- Univ. of Wisconsin, Madison, WI (United States). Lab. of Genetics, Genome Center of Wisconsin, Wisconsin Energy Inst., J.F. Crow Inst. for the Study of Evolution; Univ. of Wisconsin, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center
- Univ. of Wisconsin, Madison, WI (United States). Lab. of Genetics, Genome Center of Wisconsin, Wisconsin Energy Inst., J.F. Crow Inst. for the Study of Evolution; Univ. of Wisconsin, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center; Univ. of Wisconsin, Madison, WI (United States). Graduate Program in Cellular and Molecular Biology
- Vanderbilt Univ., Nashville, TN (United States). Dept. of Biological Sciences
- Vanderbilt Univ., Nashville, TN (United States). Dept. of Biological Sciences; South China Agricultural Univ., Guangzhou (China)
- US Dept. of Agriculture, Peoria, IL (United States). Mycotoxin Prevention and Applied Microbiology Research Unit, National Center for Agricultural Utilization Research, Agricultural Research Service
- Univ. of Wisconsin, Madison, WI (United States). Lab. of Genetics, Genome Center of Wisconsin, Wisconsin Energy Inst., J.F. Crow Inst. for the Study of Evolution
- Westerdijk Fungal Biodiversity Inst. CT, Utrecht (Netherlands)
- Univ. of Wisconsin, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center
- Univ. of Wisconsin, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center, and Dept. of Biochemistry
- Publication Date:
- Research Org.:
- Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- Contributing Org.:
- Lucigen Corporation (Middleton, WI); University of Wisconsin Biotechnology Center DNA Sequencing Facility; Center for High-Throughput Computing at the University of Wisconsin-Madison
- OSTI Identifier:
- 1547009
- Grant/Contract Number:
- SC0018409
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Cell
- Additional Journal Information:
- Journal Volume: 176; Journal Issue: 6; Journal ID: ISSN 0092-8674
- Publisher:
- Elsevier
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; central dogma of biology; horizontal gene transfer; operon; siderophore; biosynthesis; budding yeasts; Wickerhamiella; Starmerella; Saccharomycotina; enterobactin
Citation Formats
Kominek, Jacek, Doering, Drew T., Opulente, Dana A., Shen, Xing-Xing, Zhou, Xiaofan, DeVirgilio, Jeremy, Hulfachor, Amanda B., Groenewald, Marizeth, Mcgee, Mcsean A., Karlen, Steven D., Kurtzman, Cletus P., Rokas, Antonis, and Hittinger, Chris Todd. Eukaryotic Acquisition of a Bacterial Operon. United States: N. p., 2019.
Web. doi:10.1016/j.cell.2019.01.034.
Kominek, Jacek, Doering, Drew T., Opulente, Dana A., Shen, Xing-Xing, Zhou, Xiaofan, DeVirgilio, Jeremy, Hulfachor, Amanda B., Groenewald, Marizeth, Mcgee, Mcsean A., Karlen, Steven D., Kurtzman, Cletus P., Rokas, Antonis, & Hittinger, Chris Todd. Eukaryotic Acquisition of a Bacterial Operon. United States. https://doi.org/10.1016/j.cell.2019.01.034
Kominek, Jacek, Doering, Drew T., Opulente, Dana A., Shen, Xing-Xing, Zhou, Xiaofan, DeVirgilio, Jeremy, Hulfachor, Amanda B., Groenewald, Marizeth, Mcgee, Mcsean A., Karlen, Steven D., Kurtzman, Cletus P., Rokas, Antonis, and Hittinger, Chris Todd. Thu .
"Eukaryotic Acquisition of a Bacterial Operon". United States. https://doi.org/10.1016/j.cell.2019.01.034. https://www.osti.gov/servlets/purl/1547009.
@article{osti_1547009,
title = {Eukaryotic Acquisition of a Bacterial Operon},
author = {Kominek, Jacek and Doering, Drew T. and Opulente, Dana A. and Shen, Xing-Xing and Zhou, Xiaofan and DeVirgilio, Jeremy and Hulfachor, Amanda B. and Groenewald, Marizeth and Mcgee, Mcsean A. and Karlen, Steven D. and Kurtzman, Cletus P. and Rokas, Antonis and Hittinger, Chris Todd},
abstractNote = {Operons are a hallmark of bacterial genomes, where they allow concerted expression of functionally related genes as single polycistronic transcripts. They are rare in eukaryotes, where each gene usually drives expression of its own independent messenger RNAs. Here, we report the horizontal operon transfer of a siderophore biosynthesis pathway from relatives of Escherichia coli into a group of budding yeast taxa. We further show that the co-linearly arranged secondary metabolism genes are expressed, exhibit eukaryotic transcriptional features, and enable the sequestration and uptake of iron. After transfer, several genetic changes occurred during subsequent evolution, including the gain of new transcription start sites that were sometimes within protein-coding sequences, acquisition of polyadenylation sites, structural rearrangements, and integration of eukaryotic genes into the cluster. We conclude that the genes were likely acquired as a unit, modified for eukaryotic gene expression, and maintained by selection to adapt to the highly competitive, iron-limited environment.},
doi = {10.1016/j.cell.2019.01.034},
journal = {Cell},
number = 6,
volume = 176,
place = {United States},
year = {Thu Feb 21 00:00:00 EST 2019},
month = {Thu Feb 21 00:00:00 EST 2019}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 55 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Genome-based phylogeny and taxonomy of the ‘Enterobacteriales’: proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov.
journal, December 2016
- Adeolu, Mobolaji; Alnajar, Seema; Naushad, Sohail
- International Journal of Systematic and Evolutionary Microbiology, Vol. 66, Issue 12
Horizontally acquired genes in early-diverging pathogenic fungi enable the use of host nucleosides and nucleotides
journal, March 2016
- Alexander, William G.; Wisecaver, Jennifer H.; Rokas, Antonis
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 15
Basic local alignment search tool
journal, October 1990
- Altschul, Stephen F.; Gish, Warren; Miller, Webb
- Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
Bacterial iron homeostasis
journal, June 2003
- Andrews, Simon C.; Robinson, Andrea K.; Rodríguez-Quiñones, Francisco
- FEMS Microbiology Reviews, Vol. 27, Issue 2-3
MEME SUITE: tools for motif discovery and searching
journal, May 2009
- Bailey, T. L.; Boden, M.; Buske, F. A.
- Nucleic Acids Research, Vol. 37, Issue Web Server
Buried Treasure: Evolutionary Perspectives on Microbial Iron Piracy
journal, November 2015
- Barber, Matthew F.; Elde, Nels C.
- Trends in Genetics, Vol. 31, Issue 11
Inferring ancient metabolism using ancestral core metabolic models of enterobacteria
journal, January 2013
- Baumler, David J.; Ma, Bing; Reed, Jennifer L.
- BMC Systems Biology, Vol. 7, Issue 1
The Complete Genome Sequence of Escherichia coli K-12
journal, September 1997
- Blattner, F. R.
- Science, Vol. 277, Issue 5331
Caenorhabditis elegans operons: form and function
journal, February 2003
- Blumenthal, Thomas; Gleason, Kathy Seggerson
- Nature Reviews Genetics, Vol. 4, Issue 2
Repeated loss of an anciently horizontally transferred gene cluster in Botrytis
journal, September 2013
- Campbell, Matthew A.; Staats, Martijn; van Kan, Jan A. L.
- Mycologia, Vol. 105, Issue 5
Discovery of Fur binding site clusters in Escherichia coli by information theory models
journal, October 2007
- Chen, Zehua; Lewis, Karen A.; Shultzaberger, Ryan K.
- Nucleic Acids Research, Vol. 35, Issue 20
Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction
journal, April 1987
- Chomczynski, Piotr; Sacchi, Nicoletta
- Analytical Biochemistry, Vol. 162, Issue 1
Gene make-up: rapid and massive intron gains after horizontal transfer of a bacterial α-amylase gene to Basidiomycetes
journal, January 2013
- Da Lage, Jean-Luc; Binder, Manfred; Hua-Van, Aurélie
- BMC Evolutionary Biology, Vol. 13, Issue 1
Incorporation of a Horizontally Transferred Gene into an Operon during Cnidarian Evolution
journal, February 2012
- Dana, Catherine E.; Glauber, Kristine M.; Chan, Titus A.
- PLoS ONE, Vol. 7, Issue 2
A high-resolution map of transcription in the yeast genome
journal, March 2006
- David, L.; Huber, W.; Granovskaia, M.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 14
Genome Diversity and Evolution in the Budding Yeasts (Saccharomycotina)
journal, June 2017
- Dujon, Bernard A.; Louis, Edward J.
- Genetics, Vol. 206, Issue 2
Widespread Lateral Gene Transfer from Intracellular Bacteria to Multicellular Eukaryotes
journal, September 2007
- Hotopp, J. C. D.; Clark, M. E.; Oliveira, D. C. S. G.
- Science, Vol. 317, Issue 5845
Horizontal gene transfer in fungi
journal, December 2011
- Fitzpatrick, David A.
- FEMS Microbiology Letters, Vol. 329, Issue 1
Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga
journal, July 2013
- Flot, Jean-François; Hespeels, Boris; Li, Xiang
- Nature, Vol. 500, Issue 7463
Spliced-Leader RNA trans Splicing in a Chordate, Oikopleura dioica , with a Compact Genome
journal, September 2004
- Ganot, Philippe; Kallesøe, Torben; Reinhardt, Richard
- Molecular and Cellular Biology, Vol. 24, Issue 17
Identification and roles of non-pathogenic microflora associated with honey bees
journal, October 1997
- Gilliam, M.
- FEMS Microbiology Letters, Vol. 155, Issue 1
Enterobacteriaceae isolated from foraging worker honey bees, Apis mellifera
journal, January 1974
- Gilliam, Martha; Valentine, Diane K.
- Journal of Invertebrate Pathology, Vol. 23, Issue 1
Massive Horizontal Gene Transfer in Bdelloid Rotifers
journal, May 2008
- Gladyshev, E. A.; Meselson, M.; Arkhipova, I. R.
- Science, Vol. 320, Issue 5880
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
Full-length transcriptome assembly from RNA-Seq data without a reference genome
journal, May 2011
- Grabherr, Manfred G.; Haas, Brian J.; Yassour, Moran
- Nature Biotechnology, Vol. 29, Issue 7
QUAST: quality assessment tool for genome assemblies
journal, February 2013
- Gurevich, Alexey; Saveliev, Vladislav; Vyahhi, Nikolay
- Bioinformatics, Vol. 29, Issue 8
Siderophores in Fungal Physiology and Virulence
journal, September 2008
- Haas, Hubertus; Eisendle, Martin; Turgeon, B. Gillian
- Annual Review of Phytopathology, Vol. 46, Issue 1
Bacterial conjugative plasmids mobilize DNA transfer between bacteria and yeast
journal, July 1989
- Heinemann, Jack A.; Sprague, George F.
- Nature, Vol. 340, Issue 6230
Gene duplication and the adaptive evolution of a classic genetic switch
journal, October 2007
- Hittinger, Chris Todd; Carroll, Sean B.
- Nature, Vol. 449, Issue 7163
MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects
journal, December 2011
- Holt, Carson; Yandell, Mark
- BMC Bioinformatics, Vol. 12, Issue 1
Intron Evolution in Saccharomycetaceae
journal, September 2014
- Hooks, Katarzyna B.; Delneri, Daniela; Griffiths-Jones, Sam
- Genome Biology and Evolution, Vol. 6, Issue 9
Repeated replacement of an intrabacterial symbiont in the tripartite nested mealybug symbiosis
journal, August 2016
- Husnik, Filip; McCutcheon, John P.
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 37
Functional horizontal gene transfer from bacteria to eukaryotes
journal, November 2017
- Husnik, Filip; McCutcheon, John P.
- Nature Reviews Microbiology, Vol. 16, Issue 2
Horizontal Gene Transfer from Diverse Bacteria to an Insect Genome Enables a Tripartite Nested Mealybug Symbiosis
journal, June 2013
- Husnik, Filip; Nikoh, Naruo; Koga, Ryuichi
- Cell, Vol. 153, Issue 7
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
Horizontal gene transfer in eukaryotic evolution
journal, August 2008
- Keeling, Patrick J.; Palmer, Jeffrey D.
- Nature Reviews Genetics, Vol. 9, Issue 8
Alternative splicing and evolution: diversification, exon definition and function
journal, April 2010
- Keren, Hadas; Lev-Maor, Galit; Ast, Gil
- Nature Reviews Genetics, Vol. 11, Issue 5
Evidence for horizontal transfer of a secondary metabolite gene cluster between fungi
journal, January 2008
- Khaldi, Nora; Collemare, Jérôme; Lebrun, Marc-Henri
- Genome Biology, Vol. 9, Issue 1
Genome fragment of Wolbachia endosymbiont transferred to X chromosome of host insect
journal, October 2002
- Kondo, N.; Nikoh, N.; Ijichi, N.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 22
ExaML version 3: a tool for phylogenomic analyses on supercomputers
journal, March 2015
- Kozlov, Alexey M.; Aberer, Andre J.; Stamatakis, Alexandros
- Bioinformatics, Vol. 31, Issue 15
Functional and evolutionary characterization of a secondary metabolite gene cluster in budding yeasts
journal, October 2018
- Krause, David J.; Kominek, Jacek; Opulente, Dana A.
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 43
Selfish Operons: Horizontal Transfer May Drive the Evolution of Gene Clusters
journal, August 1996
- Lawrence, Jeffrey G.; Roth, John R.
- Genetics, Vol. 143, Issue 4
An Improved General Amino Acid Replacement Matrix
journal, April 2008
- Le, S. Q.; Gascuel, O.
- Molecular Biology and Evolution, Vol. 25, Issue 7
The Hotdog Thioesterase EntH (YbdB) Plays a Role In Vivo in Optimal Enterobactin Biosynthesis by Interacting with the ArCP Domain of EntB
journal, August 2007
- Leduc, Damien; Battesti, Aurélia; Bouveret, Emmanuelle
- Journal of Bacteriology, Vol. 189, Issue 19
Use of CAS-agar plate modified to study the effect of different variables on the siderophore production by Aspergillus
journal, March 2003
- Machuca, A.; Milagres, A. M. F.
- Letters in Applied Microbiology, Vol. 36, Issue 3
Acquisition of prokaryotic genes by fungal genomes
journal, January 2010
- Marcet-Houben, Marina; Gabaldón, Toni
- Trends in Genetics, Vol. 26, Issue 1
Genomics and Evolution of Heritable Bacterial Symbionts
journal, December 2008
- Moran, Nancy A.; McCutcheon, John P.; Nakabachi, Atsushi
- Annual Review of Genetics, Vol. 42, Issue 1
The intronome of budding yeasts
journal, August 2011
- Neuvéglise, Cécile; Marck, Christian; Gaillardin, Claude
- Comptes Rendus Biologies, Vol. 334, Issue 8-9
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies
journal, November 2014
- Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt
- Molecular Biology and Evolution, Vol. 32, Issue 1
Wolbachia genome integrated in an insect chromosome: Evolution and fate of laterally transferred endosymbiont genes
journal, February 2008
- Nikoh, N.; Tanaka, K.; Shibata, F.
- Genome Research, Vol. 18, Issue 2
Extensive transcriptional heterogeneity revealed by isoform profiling
journal, April 2013
- Pelechano, Vicent; Wei, Wu; Steinmetz, Lars M.
- Nature, Vol. 497, Issue 7447
O-CAS, a fast and universal method for siderophore detection
journal, July 2007
- Pérez-Miranda, S.; Cabirol, N.; George-Téllez, R.
- Journal of Microbiological Methods, Vol. 70, Issue 1
StringTie enables improved reconstruction of a transcriptome from RNA-seq reads
journal, February 2015
- Pertea, Mihaela; Pertea, Geo M.; Antonescu, Corina M.
- Nature Biotechnology, Vol. 33, Issue 3
Evolution of Filamentous Plant Pathogens: Gene Exchange across Eukaryotic Kingdoms
journal, September 2006
- Richards, Thomas A.; Dacks, Joel B.; Jenkinson, Joanna M.
- Current Biology, Vol. 16, Issue 18
Gene transfer into the fungi
journal, July 2011
- Richards, Thomas A.; Leonard, Guy; Soanes, Darren M.
- Fungal Biology Reviews, Vol. 25, Issue 2
Horizontal gene transfer facilitated the evolution of plant parasitic mechanisms in the oomycetes
journal, August 2011
- Richards, T. A.; Soanes, D. M.; Jones, M. D. M.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 37
Yeast communities associated with stingless bees
journal, December 2003
- Rosa, C.; Lachance, M.; Silva, J.
- FEMS Yeast Research, Vol. 4, Issue 3
Host RNAs, including transposons, are encapsidated by a eukaryotic single-stranded RNA virus
journal, January 2012
- Routh, A.; Domitrovic, T.; Johnson, J. E.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 6
Human and Plant Fungal Pathogens: The Role of Secondary Metabolites
journal, January 2014
- Scharf, Daniel H.; Heinekamp, Thorsten; Brakhage, Axel A.
- PLoS Pathogens, Vol. 10, Issue 1
Deciphering Fur transcriptional regulatory network highlights its complex role beyond iron metabolism in Escherichia coli
journal, September 2014
- Seo, Sang Woo; Kim, Donghyuk; Latif, Haythem
- Nature Communications, Vol. 5, Issue 1
Iron–sulfur proteins in health and disease
journal, May 2010
- Sheftel, Alex; Stehling, Oliver; Lill, Roland
- Trends in Endocrinology & Metabolism, Vol. 21, Issue 5
Reconstructing the Backbone of the Saccharomycotina Yeast Phylogeny Using Genome-Scale Data
journal, September 2016
- Shen, Xing-Xing; Zhou, Xiaofan; Kominek, Jacek
- G3: Genes|Genomes|Genetics, Vol. 6, Issue 12
Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum
journal, November 2018
- Shen, Xing-Xing; Opulente, Dana A.; Kominek, Jacek
- Cell, Vol. 175, Issue 6
BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs
journal, June 2015
- Simão, Felipe A.; Waterhouse, Robert M.; Ioannidis, Panagiotis
- Bioinformatics, Vol. 31, Issue 19
The Battle for Iron between Bacterial Pathogens and Their Vertebrate Hosts
journal, August 2010
- Skaar, Eric P.
- PLoS Pathogens, Vol. 6, Issue 8
Multiple GAL pathway gene clusters evolved independently and by different mechanisms in fungi
journal, May 2010
- Slot, J. C.; Rokas, A.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 22
Horizontal Transfer of a Large and Highly Toxic Secondary Metabolic Gene Cluster between Fungi
journal, January 2011
- Slot, Jason C.; Rokas, Antonis
- Current Biology, Vol. 21, Issue 2
Horizontal gene transfer: building the web of life
journal, July 2015
- Soucy, Shannon M.; Huang, Jinling; Gogarten, Johann Peter
- Nature Reviews Genetics, Vol. 16, Issue 8
Operons in C. elegans: Polycistronic mRNA precursors are processed by trans-splicing of SL2 to downstream coding regions
journal, May 1993
- Spieth, John; Brooke, Glenn; Kuersten, Scott
- Cell, Vol. 73, Issue 3
A SUF Fe-S Cluster Biogenesis System in the Mitochondrion-Related Organelles of the Anaerobic Protist Pygsuia
journal, June 2014
- Stairs, Courtney W.; Eme, Laura; Brown, Matthew W.
- Current Biology, Vol. 24, Issue 11
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014
- Stamatakis, Alexandros
- Bioinformatics, Vol. 30, Issue 9
Using native and syntenically mapped cDNA alignments to improve de novo gene finding
journal, January 2008
- Stanke, Mario; Diekhans, Mark; Baertsch, Robert
- Bioinformatics, Vol. 24, Issue 5
Social wasps are a Saccharomyces mating nest
journal, January 2016
- Stefanini, Irene; Dapporto, Leonardo; Berná, Luisa
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 8
Crusade for iron: iron uptake in unicellular eukaryotes and its significance for virulence
journal, June 2008
- Sutak, Robert; Lesuisse, Emmanuel; Tachezy, Jan
- Trends in Microbiology, Vol. 16, Issue 6
Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training
journal, October 2008
- Ter-Hovhannisyan, V.; Lomsadze, A.; Chernoff, Y. O.
- Genome Research, Vol. 18, Issue 12
Comparative Genomics Reveals What Makes An Enterobacterial Plant Pathogen
journal, September 2006
- Toth, Ian K.; Pritchard, Leighton; Birch, Paul R. J.
- Annual Review of Phytopathology, Vol. 44, Issue 1
Evolution of Fe/S cluster biogenesis in the anaerobic parasite Blastocystis
journal, June 2012
- Tsaousis, A. D.; Ollagnier de Choudens, S.; Gentekaki, E.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 26
mRNAs that mature through trans-splicing in Caenorhabditis elegans have a trimethylguanosine cap at their 5' termini.
journal, April 1990
- Van Doren, K.; Hirsh, D.
- Molecular and Cellular Biology, Vol. 10, Issue 4
mRNA 5'-leader trans-splicing in the chordates
journal, February 2001
- Vandenberghe, A. E.
- Genes & Development, Vol. 15, Issue 3
Bacterial Iron Sources: From Siderophores to Hemophores
journal, October 2004
- Wandersman, Cécile; Delepelaire, Philippe
- Annual Review of Microbiology, Vol. 58, Issue 1
Plasmid-Mediated Gene Transfer Between Insect-Resident Bacteria, Enterobacter cloacae , and Plant-Epiphytic Bacteria, Erwinia herbicola , in Guts of Silkworm Larvae
journal, November 1998
- Watanabe, Kenji; Sato, M.
- Current Microbiology, Vol. 37, Issue 5
Evidence for Growth of Strains of the Plant Epiphytic BacteriumErwinia herbicolaand Transconjugation among the Bacterial Strains in Guts of the SilkwormBombyx mori
journal, September 1998
- Watanabe, Kenji; Hara, Wajiro; Sato, Mamoru
- Journal of Invertebrate Pathology, Vol. 72, Issue 2
Fungal metabolic gene clusters—caravans traveling across genomes and environments
journal, March 2015
- Wisecaver, Jennifer H.; Rokas, Antonis
- Frontiers in Microbiology, Vol. 6
Dynamic Evolution of Nitric Oxide Detoxifying Flavohemoglobins, a Family of Single-Protein Metabolic Modules in Bacteria and Eukaryotes
journal, April 2016
- Wisecaver, Jennifer H.; Alexander, William G.; King, Sean B.
- Molecular Biology and Evolution, Vol. 33, Issue 8
Fast and SNP-tolerant detection of complex variants and splicing in short reads
journal, February 2010
- Wu, T. D.; Nacu, S.
- Bioinformatics, Vol. 26, Issue 7, p. 873-881
The plastid genome of some eustigmatophyte algae harbours a bacteria-derived six-gene cluster for biosynthesis of a novel secondary metabolite
journal, November 2016
- Yurchenko, Tatiana; Ševčíková, Tereza; Strnad, Hynek
- Open Biology, Vol. 6, Issue 11
A gene transfer event suggests a long-term partnership between eustigmatophyte algae and a novel lineage of endosymbiotic bacteria
journal, June 2018
- Yurchenko, Tatiana; Ševčíková, Tereza; Přibyl, Pavel
- The ISME Journal, Vol. 12, Issue 9
In Silico Whole Genome Sequencer and Analyzer (iWGS): a Computational Pipeline to Guide the Design and Analysis of de novo Genome Sequencing Studies
journal, September 2016
- Zhou, Xiaofan; Peris, David; Kominek, Jacek
- G3: Genes|Genomes|Genetics, Vol. 6, Issue 11
Works referencing / citing this record:
Reduction-dependent siderophore assimilation in a model pennate diatom
journal, November 2019
- Coale, Tyler H.; Moosburner, Mark; Horák, Aleš
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 47
Multilayered horizontal operon transfers from bacteria reconstruct a thiamine salvage pathway in yeasts
journal, October 2019
- Gonçalves, Carla; Gonçalves, Paula
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 44
Biosynthetic gene clusters and the evolution of fungal chemodiversity
journal, January 2020
- Rokas, Antonis; Mead, Matthew E.; Steenwyk, Jacob L.
- Natural Product Reports, Vol. 37, Issue 7
Distinct but Intertwined Evolutionary Histories of Multiple Salmonella enterica Subspecies
journal, January 2020
- Park, Cooper J.; Andam, Cheryl P.
- mSystems, Vol. 5, Issue 1
Disentangling the genetic bases of Saccharomyces cerevisiae nitrogen consumption and adaptation to low nitrogen environments in wine fermentation
journal, January 2020
- Kessi-Pérez, Eduardo I.; Molinet, Jennifer; Martínez, Claudio
- Biological Research, Vol. 53, Issue 1
Kinetic and mechanistic insights into hydrogenolysis of lignin to monomers in a continuous flow reactor
journal, January 2019
- Li, Yanding; Demir, Benginur; Vázquez Ramos, Leida M.
- Green Chemistry, Vol. 21, Issue 13
Distinct but Intertwined Evolutionary Histories of Multiple Salmonella enterica Subspecies
journal, January 2020
- Park, Cooper J.; Andam, Cheryl P.
- mSystems, Vol. 5, Issue 1
Disentangling the genetic bases of Saccharomyces cerevisiae nitrogen consumption and adaptation to low nitrogen environments in wine fermentation
journal, January 2020
- Kessi-Pérez, Eduardo I.; Molinet, Jennifer; Martínez, Claudio
- Biological Research, Vol. 53, Issue 1
A New Pathway for Mannitol Metabolism in Yeasts Suggests a Link to the Evolution of Alcoholic Fermentation
journal, November 2019
- Gonçalves, Carla; Ferreira, Carolina; Gonçalves, Luís G.
- Frontiers in Microbiology, Vol. 10