DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: 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:
 [1];  [2];  [1];  [3];  [4];  [5];  [6];  [7];  [8];  [9];  [5];  [3];  [2]
  1. 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
  2. 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
  3. Vanderbilt Univ., Nashville, TN (United States). Dept. of Biological Sciences
  4. Vanderbilt Univ., Nashville, TN (United States). Dept. of Biological Sciences; South China Agricultural Univ., Guangzhou (China)
  5. US Dept. of Agriculture, Peoria, IL (United States). Mycotoxin Prevention and Applied Microbiology Research Unit, National Center for Agricultural Utilization Research, Agricultural Research Service
  6. 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
  7. Westerdijk Fungal Biodiversity Inst. CT, Utrecht (Netherlands)
  8. Univ. of Wisconsin, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center
  9. 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 = {2019},
month = {2}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 17 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

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
  • DOI: 10.1073/pnas.1517242113

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
  • DOI: 10.1016/S0022-2836(05)80360-2

Bacterial iron homeostasis
journal, June 2003

  • Andrews, Simon C.; Robinson, Andrea K.; Rodríguez-Quiñones, Francisco
  • FEMS Microbiology Reviews, Vol. 27, Issue 2-3
  • DOI: 10.1016/S0168-6445(03)00055-X

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
  • DOI: 10.1093/nar/gkp335

Buried Treasure: Evolutionary Perspectives on Microbial Iron Piracy
journal, November 2015


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
  • DOI: 10.1186/1752-0509-7-46

The Complete Genome Sequence of Escherichia coli K-12
journal, September 1997


Caenorhabditis elegans operons: form and function
journal, February 2003

  • Blumenthal, Thomas; Gleason, Kathy Seggerson
  • Nature Reviews Genetics, Vol. 4, Issue 2
  • DOI: 10.1038/nrg995

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
  • DOI: 10.3852/12-390

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
  • DOI: 10.1093/nar/gkm631

Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction
journal, April 1987


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
  • DOI: 10.1186/1471-2148-13-40

Incorporation of a Horizontally Transferred Gene into an Operon during Cnidarian Evolution
journal, February 2012


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
  • DOI: 10.1073/pnas.0601091103

Genome Diversity and Evolution in the Budding Yeasts (Saccharomycotina)
journal, June 2017


Widespread Lateral Gene Transfer from Intracellular Bacteria to Multicellular Eukaryotes
journal, September 2007


Horizontal gene transfer in fungi
journal, December 2011


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
  • DOI: 10.1038/nature12326

Spliced-Leader RNA trans Splicing in a Chordate, Oikopleura dioica , with a Compact Genome
journal, September 2004


Identification and roles of non-pathogenic microflora associated with honey bees
journal, October 1997


Enterobacteriaceae isolated from foraging worker honey bees, Apis mellifera
journal, January 1974


Massive Horizontal Gene Transfer in Bdelloid Rotifers
journal, May 2008


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
  • DOI: 10.7554/eLife.33034

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
  • DOI: 10.1038/nbt.1883

QUAST: quality assessment tool for genome assemblies
journal, February 2013


Siderophores in Fungal Physiology and Virulence
journal, September 2008


Bacterial conjugative plasmids mobilize DNA transfer between bacteria and yeast
journal, July 1989

  • Heinemann, Jack A.; Sprague, George F.
  • Nature, Vol. 340, Issue 6230
  • DOI: 10.1038/340205a0

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
  • DOI: 10.1038/nature06151

MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects
journal, December 2011


Intron Evolution in Saccharomycetaceae
journal, September 2014

  • Hooks, Katarzyna B.; Delneri, Daniela; Griffiths-Jones, Sam
  • Genome Biology and Evolution, Vol. 6, Issue 9
  • DOI: 10.1093/gbe/evu196

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
  • DOI: 10.1073/pnas.1603910113

Functional horizontal gene transfer from bacteria to eukaryotes
journal, November 2017


Horizontal Gene Transfer from Diverse Bacteria to an Insect Genome Enables a Tripartite Nested Mealybug Symbiosis
journal, June 2013


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
  • DOI: 10.1093/molbev/mst010

Horizontal gene transfer in eukaryotic evolution
journal, August 2008

  • Keeling, Patrick J.; Palmer, Jeffrey D.
  • Nature Reviews Genetics, Vol. 9, Issue 8
  • DOI: 10.1038/nrg2386

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
  • DOI: 10.1038/nrg2776

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
  • DOI: 10.1186/gb-2008-9-1-r18

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
  • DOI: 10.1073/pnas.222228199

ExaML version 3: a tool for phylogenomic analyses on supercomputers
journal, March 2015


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
  • DOI: 10.1073/pnas.1806268115

Biogeography of the yeasts of ephemeral flowers and their insects
journal, April 2001


Selfish Operons: Horizontal Transfer May Drive the Evolution of Gene Clusters
journal, August 1996


An Improved General Amino Acid Replacement Matrix
journal, April 2008


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
  • DOI: 10.1128/JB.00755-07

Use of CAS-agar plate modified to study the effect of different variables on the siderophore production by Aspergillus
journal, March 2003


Acquisition of prokaryotic genes by fungal genomes
journal, January 2010


Genomics and Evolution of Heritable Bacterial Symbionts
journal, December 2008


The intronome of budding yeasts
journal, August 2011

  • Neuvéglise, Cécile; Marck, Christian; Gaillardin, Claude
  • Comptes Rendus Biologies, Vol. 334, Issue 8-9
  • DOI: 10.1016/j.crvi.2011.05.015

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
  • DOI: 10.1093/molbev/msu300

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
  • DOI: 10.1101/gr.7144908

Extensive transcriptional heterogeneity revealed by isoform profiling
journal, April 2013

  • Pelechano, Vicent; Wei, Wu; Steinmetz, Lars M.
  • Nature, Vol. 497, Issue 7447
  • DOI: 10.1038/nature12121

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
  • DOI: 10.1016/j.mimet.2007.03.023

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
  • DOI: 10.1038/nbt.3122

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
  • DOI: 10.1016/j.cub.2006.07.052

Gene transfer into the fungi
journal, July 2011

  • Richards, Thomas A.; Leonard, Guy; Soanes, Darren M.
  • Fungal Biology Reviews, Vol. 25, Issue 2
  • DOI: 10.1016/j.fbr.2011.04.003

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
  • DOI: 10.1073/pnas.1105100108

Yeast communities associated with stingless bees
journal, December 2003


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
  • DOI: 10.1073/pnas.1116168109

Human and Plant Fungal Pathogens: The Role of Secondary Metabolites
journal, January 2014


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
  • DOI: 10.1038/ncomms5910

Iron–sulfur proteins in health and disease
journal, May 2010

  • Sheftel, Alex; Stehling, Oliver; Lill, Roland
  • Trends in Endocrinology & Metabolism, Vol. 21, Issue 5
  • DOI: 10.1016/j.tem.2009.12.006

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
  • DOI: 10.1534/g3.116.034744

Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum
journal, November 2018


BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs
journal, June 2015


The Battle for Iron between Bacterial Pathogens and Their Vertebrate Hosts
journal, August 2010


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
  • DOI: 10.1073/pnas.0914418107

Horizontal Transfer of a Large and Highly Toxic Secondary Metabolic Gene Cluster between Fungi
journal, January 2011


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
  • DOI: 10.1038/nrg3962

A SUF Fe-S Cluster Biogenesis System in the Mitochondrion-Related Organelles of the Anaerobic Protist Pygsuia
journal, June 2014


RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014


Using native and syntenically mapped cDNA alignments to improve de novo gene finding
journal, January 2008


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
  • DOI: 10.1073/pnas.1516453113

Crusade for iron: iron uptake in unicellular eukaryotes and its significance for virulence
journal, June 2008


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
  • DOI: 10.1101/gr.081612.108

Comparative Genomics Reveals What Makes An Enterobacterial Plant Pathogen
journal, September 2006


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
  • DOI: 10.1073/pnas.1116067109

mRNAs that mature through trans-splicing in Caenorhabditis elegans have a trimethylguanosine cap at their 5' termini.
journal, April 1990


mRNA 5'-leader trans-splicing in the chordates
journal, February 2001


Bacterial Iron Sources: From Siderophores to Hemophores
journal, October 2004


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
  • DOI: 10.1006/jipa.1998.4764

Fungal metabolic gene clusters—caravans traveling across genomes and environments
journal, March 2015


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
  • DOI: 10.1093/molbev/msw073

Fast and SNP-tolerant detection of complex variants and splicing in short reads
journal, February 2010


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
  • DOI: 10.1098/rsob.160249

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
  • DOI: 10.1038/s41396-018-0177-y

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
  • DOI: 10.1534/g3.116.034249

Works referencing / citing this record:

Molecular Dating of the Emergence of Anaerobic Rumen Fungi and the Impact of Laterally Acquired Genes
journal, August 2019


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
  • DOI: 10.1073/pnas.1907234116

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
  • DOI: 10.1073/pnas.1909844116

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
  • DOI: 10.1039/c9np00045c

Distinct but Intertwined Evolutionary Histories of Multiple Salmonella enterica Subspecies
journal, January 2020


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
  • DOI: 10.1186/s40659-019-0270-3

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
  • DOI: 10.1039/c9gc00986h