Publications by authors named "Asaf Salamov"

89 Publications

Genome-scale phylogenetic analyses confirm Olpidium as the closest living zoosporic fungus to the non-flagellated, terrestrial fungi.

Sci Rep 2021 Feb 5;11(1):3217. Epub 2021 Feb 5.

Department of Botany and Plant Pathology, College of Agricultural Sciences, Oregon State University, Oregon, USA.

The zoosporic obligate endoparasites, Olpidium, hold a pivotal position to the reconstruction of the flagellum loss in fungi, one of the key morphological transitions associated with the colonization of land by the early fungi. We generated genome and transcriptome data from non-axenic zoospores of Olpidium bornovanus and used a metagenome approach to extract phylogenetically informative fungal markers. Our phylogenetic reconstruction strongly supported Olpidium as the closest zoosporic relative of the non-flagellated terrestrial fungi. Super-alignment analyses resolved Olpidium as sister to the non-flagellated terrestrial fungi, whereas a super-tree approach recovered different placements of Olpidium, but without strong support. Further investigations detected little conflicting signal among the sampled markers but revealed a potential polytomy in early fungal evolution associated with the branching order among Olpidium, Zoopagomycota and Mucoromycota. The branches defining the evolutionary relationships of these lineages were characterized by short branch lengths and low phylogenetic content and received equivocal support for alternative phylogenetic hypotheses from individual markers. These nodes were marked by important morphological innovations, including the transition to hyphal growth and the loss of flagellum, which enabled early fungi to explore new niches and resulted in rapid and temporally concurrent Precambrian diversifications of the ancestors of several phyla of fungi.
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http://dx.doi.org/10.1038/s41598-021-82607-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7865070PMC
February 2021

Genomic and functional analyses of fungal and bacterial consortia that enable lignocellulose breakdown in goat gut microbiomes.

Nat Microbiol 2021 Apr 1;6(4):499-511. Epub 2021 Feb 1.

Department of Chemical Engineering, University of California, Santa Barbara, CA, USA.

The herbivore digestive tract is home to a complex community of anaerobic microbes that work together to break down lignocellulose. These microbiota are an untapped resource of strains, pathways and enzymes that could be applied to convert plant waste into sugar substrates for green biotechnology. We carried out more than 400 parallel enrichment experiments from goat faeces to determine how substrate and antibiotic selection influence membership, activity, stability and chemical productivity of herbivore gut communities. We assembled 719 high-quality metagenome-assembled genomes (MAGs) that are unique at the species level. More than 90% of these MAGs are from previously unidentified herbivore gut microorganisms. Microbial consortia dominated by anaerobic fungi outperformed bacterially dominated consortia in terms of both methane production and extent of cellulose degradation, which indicates that fungi have an important role in methane release. Metabolic pathway reconstructions from MAGs of 737 bacteria, archaea and fungi suggest that cross-domain partnerships between fungi and methanogens enabled production of acetate, formate and methane, whereas bacterially dominated consortia mainly produced short-chain fatty acids, including propionate and butyrate. Analyses of carbohydrate-active enzyme domains present in each anaerobic consortium suggest that anaerobic bacteria and fungi employ mostly complementary hydrolytic strategies. The division of labour among herbivore anaerobes to degrade plant biomass could be harnessed for industrial bioprocessing.
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http://dx.doi.org/10.1038/s41564-020-00861-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8007473PMC
April 2021

PhycoCosm, a comparative algal genomics resource.

Nucleic Acids Res 2021 01;49(D1):D1004-D1011

US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.

Algae are a diverse, polyphyletic group of photosynthetic eukaryotes spanning nearly all eukaryotic lineages of life and collectively responsible for ∼50% of photosynthesis on Earth. Sequenced algal genomes, critical to understanding their complex biology, are growing in number and require efficient tools for analysis. PhycoCosm (https://phycocosm.jgi.doe.gov) is an algal multi-omics portal, developed by the US Department of Energy Joint Genome Institute to support analysis and distribution of algal genome sequences and other 'omics' data. PhycoCosm provides integration of genome sequence and annotation for >100 algal genomes with available multi-omics data and interactive web-based tools to enable algal research in bioenergy and the environment, encouraging community engagement and data exchange, and fostering new sequencing projects that will further these research goals.
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http://dx.doi.org/10.1093/nar/gkaa898DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7779022PMC
January 2021

Phylogenomic Analyses of Non-Dikarya Fungi Supports Horizontal Gene Transfer Driving Diversification of Secondary Metabolism in the Amphibian Gastrointestinal Symbiont, .

G3 (Bethesda) 2020 09 2;10(9):3417-3433. Epub 2020 Sep 2.

Department of Botany and Plant Pathology, College of Agricultural Sciences, Oregon State University, Corvallis.

Research into secondary metabolism (SM) production by fungi has resulted in the discovery of diverse, biologically active compounds with significant medicinal applications. The fungi rich in SM production are taxonomically concentrated in the subkingdom Dikarya, which comprises the phyla Ascomycota and Basidiomycota. Here, we explore the potential for SM production in Mucoromycota and Zoopagomycota, two phyla of nonflagellated fungi that are not members of Dikarya, by predicting and identifying core genes and gene clusters involved in SM. The majority of non-Dikarya have few genes and gene clusters involved in SM production except for the amphibian gut symbionts in the genus genomes exhibit an enrichment of SM genes involved in siderophore, surfactin-like, and terpene cyclase production, all these with evidence of constitutive gene expression. Gene expression and chemical assays also confirm that has significant siderophore activity. The expansion of SMs in are partially due to horizontal gene transfer from bacteria, likely as a consequence of its ecology as an amphibian gut endosymbiont.
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http://dx.doi.org/10.1534/g3.120.401516DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7466969PMC
September 2020

Genome Sequence of the Chestnut Blight Fungus EP155: A Fundamental Resource for an Archetypical Invasive Plant Pathogen.

Phytopathology 2020 Jun 17;110(6):1180-1188. Epub 2020 Apr 17.

Institute for Bioscience and Biotechnology Research, University of Maryland, Rockville, MD, U.S.A.

is the causal agent of chestnut blight, a fungal disease that almost entirely eliminated mature American chestnut from North America over a 50-year period. Here, we formally report the genome of EP155 using a Sanger shotgun sequencing approach. After finishing and integration with simple-sequence repeat markers, the assembly was 43.8 Mb in 26 scaffolds (L = 5; N = 4.0Mb). Eight chromosomes are predicted: five scaffolds have two telomeres and six scaffolds have one telomere sequence. In total, 11,609 gene models were predicted, of which 85% show similarities to other proteins. This genome resource has already increased the utility of a fundamental plant pathogen experimental system through new understanding of the fungal vegetative incompatibility system, with significant implications for enhancing mycovirus-based biological control.
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http://dx.doi.org/10.1094/PHYTO-12-19-0478-ADOI Listing
June 2020

A comparative genomics study of 23 Aspergillus species from section Flavi.

Nat Commun 2020 02 27;11(1):1106. Epub 2020 Feb 27.

Department of Biotechnology and Bioengineering, Technical University of Denmark, Søltoft Plads 223, 2800, Kongens Lyngby, Denmark.

Section Flavi encompasses both harmful and beneficial Aspergillus species, such as Aspergillus oryzae, used in food fermentation and enzyme production, and Aspergillus flavus, food spoiler and mycotoxin producer. Here, we sequence 19 genomes spanning section Flavi and compare 31 fungal genomes including 23 Flavi species. We reassess their phylogenetic relationships and show that the closest relative of A. oryzae is not A. flavus, but A. minisclerotigenes or A. aflatoxiformans and identify high genome diversity, especially in sub-telomeric regions. We predict abundant CAZymes (598 per species) and prolific secondary metabolite gene clusters (73 per species) in section Flavi. However, the observed phenotypes (growth characteristics, polysaccharide degradation) do not necessarily correlate with inferences made from the predicted CAZyme content. Our work, including genomic analyses, phenotypic assays, and identification of secondary metabolites, highlights the genetic and metabolic diversity within section Flavi.
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http://dx.doi.org/10.1038/s41467-019-14051-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7046712PMC
February 2020

Genomic and proteomic biases inform metabolic engineering strategies for anaerobic fungi.

Metab Eng Commun 2020 Jun 15;10:e00107. Epub 2019 Nov 15.

Department of Chemical Engineering, University of California, Santa Barbara, CA, 93106, USA.

Anaerobic fungi (Neocallimastigomycota) are emerging non-model hosts for biotechnology due to their wealth of biomass-degrading enzymes, yet tools to engineer these fungi have not yet been established. Here, we show that the anaerobic gut fungi have the most GC depleted genomes among 443 sequenced organisms in the fungal kingdom, which has ramifications for heterologous expression of genes as well as for emerging CRISPR-based genome engineering approaches. Comparative genomic analyses suggest that anaerobic fungi may contain cellular machinery to aid in sexual reproduction, yet a complete mating pathway was not identified. Predicted proteomes of the anaerobic fungi also contain an unusually large fraction of proteins with homopolymeric amino acid runs consisting of five or more identical consecutive amino acids. In particular, threonine runs are especially enriched in anaerobic fungal carbohydrate active enzymes (CAZymes) and this, together with a high abundance of predicted N-glycosylation motifs, suggests that gut fungal CAZymes are heavily glycosylated, which may impact heterologous production of these biotechnologically useful enzymes. Finally, we present a codon optimization strategy to aid in the development of genetic engineering tools tailored to these early-branching anaerobic fungi.
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http://dx.doi.org/10.1016/j.mec.2019.e00107DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6883316PMC
June 2020

Uncovering secondary metabolite evolution and biosynthesis using gene cluster networks and genetic dereplication.

Sci Rep 2018 12 18;8(1):17957. Epub 2018 Dec 18.

Department of Biotechnology and Biomedicine, Technical University of Denmark, DK-2800, Kongens Lyngby, Denmark.

The increased interest in secondary metabolites (SMs) has driven a number of genome sequencing projects to elucidate their biosynthetic pathways. As a result, studies revealed that the number of secondary metabolite gene clusters (SMGCs) greatly outnumbers detected compounds, challenging current methods to dereplicate and categorize this amount of gene clusters on a larger scale. Here, we present an automated workflow for the genetic dereplication and analysis of secondary metabolism genes in fungi. Focusing on the secondary metabolite rich genus Aspergillus, we categorize SMGCs across genomes into SMGC families using network analysis. Our method elucidates the diversity and dynamics of secondary metabolism in section Nigri, showing that SMGC diversity within the section has the same magnitude as within the genus. Using our genome analysis we were able to predict the gene cluster responsible for biosynthesis of malformin, a potentiator of anti-cancer drugs, in 18 strains. To proof the general validity of our predictions, we developed genetic engineering tools in Aspergillus brasiliensis and subsequently verified the genes for biosynthesis of malformin.
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http://dx.doi.org/10.1038/s41598-018-36561-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6298953PMC
December 2018

Investigation of inter- and intraspecies variation through genome sequencing of Aspergillus section Nigri.

Nat Genet 2018 12 22;50(12):1688-1695. Epub 2018 Oct 22.

Department of Biotechnology and Bioengineering, Technical University of Denmark, Kongens Lyngby, Denmark.

Aspergillus section Nigri comprises filamentous fungi relevant to biomedicine, bioenergy, health, and biotechnology. To learn more about what genetically sets these species apart, as well as about potential applications in biotechnology and biomedicine, we sequenced 23 genomes de novo, forming a full genome compendium for the section (26 species), as well as 6 Aspergillus niger isolates. This allowed us to quantify both inter- and intraspecies genomic variation. We further predicted 17,903 carbohydrate-active enzymes and 2,717 secondary metabolite gene clusters, which we condensed into 455 distinct families corresponding to compound classes, 49% of which are only found in single species. We performed metabolomics and genetic engineering to correlate genotypes to phenotypes, as demonstrated for the metabolite aurasperone, and by heterologous transfer of citrate production to Aspergillus nidulans. Experimental and computational analyses showed that both secondary metabolism and regulation are key factors that are significant in the delineation of Aspergillus species.
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http://dx.doi.org/10.1038/s41588-018-0246-1DOI Listing
December 2018

Leveraging single-cell genomics to expand the fungal tree of life.

Nat Microbiol 2018 12 8;3(12):1417-1428. Epub 2018 Oct 8.

US Department of Energy Joint Genome Institute, Walnut Creek, CA, USA.

Environmental DNA surveys reveal that most fungal diversity represents uncultured species. We sequenced the genomes of eight uncultured species across the fungal tree of life using a new single-cell genomics pipeline. We show that, despite a large variation in genome and gene space recovery from each single amplified genome (SAG), ≥90% can be recovered by combining multiple SAGs. SAGs provide robust placement for early-diverging lineages and infer a diploid ancestor of fungi. Early-diverging fungi share metabolic deficiencies and show unique gene expansions correlated with parasitism and unculturability. Single-cell genomics holds great promise in exploring fungal diversity, life cycles and metabolic potential.
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http://dx.doi.org/10.1038/s41564-018-0261-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6784888PMC
December 2018

Fungal Genome Annotation.

Methods Mol Biol 2018 ;1775:171-184

United States Department of Energy Joint Genome Institute, Walnut Creek, CA, USA.

The term "genome annotation" includes identification of protein-coding and noncoding sequences (e.g., repeats, rDNA, and ncRNA) in genome assemblies and attaching functional information (metadata) to these annotated features. Here, we describe the basic outline of fungal nuclear and mitochondrial genome annotation as performed at the US Department of Energy Joint Genome Institute (JGI).
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http://dx.doi.org/10.1007/978-1-4939-7804-5_15DOI Listing
February 2019

Massive lateral transfer of genes encoding plant cell wall-degrading enzymes to the mycoparasitic fungus Trichoderma from its plant-associated hosts.

PLoS Genet 2018 04 9;14(4):e1007322. Epub 2018 Apr 9.

Microbiology and Applied Genomics Group, Research Area Biochemical Technology, Institute of Chemical, Environmental & Bioscience Engineering, TU Wien, Vienna, Austria.

Unlike most other fungi, molds of the genus Trichoderma (Hypocreales, Ascomycota) are aggressive parasites of other fungi and efficient decomposers of plant biomass. Although nutritional shifts are common among hypocrealean fungi, there are no examples of such broad substrate versatility as that observed in Trichoderma. A phylogenomic analysis of 23 hypocrealean fungi (including nine Trichoderma spp. and the related Escovopsis weberi) revealed that the genus Trichoderma has evolved from an ancestor with limited cellulolytic capability that fed on either fungi or arthropods. The evolutionary analysis of Trichoderma genes encoding plant cell wall-degrading carbohydrate-active enzymes and auxiliary proteins (pcwdCAZome, 122 gene families) based on a gene tree / species tree reconciliation demonstrated that the formation of the genus was accompanied by an unprecedented extent of lateral gene transfer (LGT). Nearly one-half of the genes in Trichoderma pcwdCAZome (41%) were obtained via LGT from plant-associated filamentous fungi belonging to different classes of Ascomycota, while no LGT was observed from other potential donors. In addition to the ability to feed on unrelated fungi (such as Basidiomycota), we also showed that Trichoderma is capable of endoparasitism on a broad range of Ascomycota, including extant LGT donors. This phenomenon was not observed in E. weberi and rarely in other mycoparasitic hypocrealean fungi. Thus, our study suggests that LGT is linked to the ability of Trichoderma to parasitize taxonomically related fungi (up to adelphoparasitism in strict sense). This may have allowed primarily mycotrophic Trichoderma fungi to evolve into decomposers of plant biomass.
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http://dx.doi.org/10.1371/journal.pgen.1007322DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5908196PMC
April 2018

Linking secondary metabolites to gene clusters through genome sequencing of six diverse species.

Proc Natl Acad Sci U S A 2018 01 9;115(4):E753-E761. Epub 2018 Jan 9.

Department of Biotechnology and Biomedicine, Technical University of Denmark, 2800 Lyngby, Denmark;

The fungal genus of is highly interesting, containing everything from industrial cell factories, model organisms, and human pathogens. In particular, this group has a prolific production of bioactive secondary metabolites (SMs). In this work, four diverse species (, , , and ) have been whole-genome PacBio sequenced to provide genetic references in three sections. and also were sequenced for SM elucidation. Thirteen genomes were analyzed with comparative genomics to determine phylogeny and genetic diversity, showing that each presented genome contains 15-27% genes not found in other sequenced Aspergilli. In particular, was compared with the pathogenic species This suggests that can produce most of the same allergens, virulence, and pathogenicity factors as , suggesting that could be as pathogenic as Furthermore, SMs were linked to gene clusters based on biological and chemical knowledge and analysis, genome sequences, and predictive algorithms. We thus identify putative SM clusters for aflatoxin, chlorflavonin, and ochrindol in , , and , respectively, and novofumigatonin, -cycloechinulin, and -aszonalenins in Our study delivers six fungal genomes, showing the large diversity found in the genus; highlights the potential for discovery of beneficial or harmful SMs; and supports reports of pathogenicity. It also shows how biological, biochemical, and genomic information can be combined to identify genes involved in the biosynthesis of specific SMs.
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http://dx.doi.org/10.1073/pnas.1715954115DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5789934PMC
January 2018

Conserved genomic collinearity as a source of broadly applicable, fast evolving, markers to resolve species complexes: A case study using the lichen-forming genus Peltigera section Polydactylon.

Mol Phylogenet Evol 2017 12 30;117:10-29. Epub 2017 Aug 30.

Department of Biology, Duke University, Durham, NC 27708, United States.

Synteny can be maintained for certain genomic regions across broad phylogenetic groups. In these homologous genomic regions, sites that are under relaxed purifying selection, such as intergenic regions, could be used broadly as markers for population genetic and phylogenetic studies on species complexes. To explore the potential of this approach, we found 125 Collinear Orthologous Regions (COR) ranging from 1 to >10kb across nine genomes representing the Lecanoromycetes and Eurotiomycetes (Pezizomycotina, Ascomycota). Twenty-six of these COR were found in all 24 eurotiomycete genomes surveyed for this study. Given the high abundance and availability of fungal genomes we believe this approach could be adopted for other large groups of fungi outside the Pezizomycotina. Asa proof of concept, we selected three Collinear Orthologous Regions (COR1b, COR3, and COR16), based on synteny analyses of several genomes representing three classes of Ascomycota: Eurotiomycetes, Lecanoromycetes, and Lichinomycetes. COR16, for example, was found across these three classes of fungi. Here we compare the resolving power of these three new markers with five loci commonly used in phylogenetic studies of fungi, using section Polydactylon of the cyanolichen-forming genus Peltigera (Lecanoromycetes) - a clade with several challenging species complexes. Sequence data were subjected to three species discovery and two validating methods. COR markers substantially increased phylogenetic resolution and confidence, and highly contributed to species delimitation. The level of phylogenetic signal provided by each of the COR markers was higher than the commonly used fungal barcode ITS. High cryptic diversity was revealed by all methods. As redefined here, most species represent lineages that have relatively narrower, and more homogeneous biogeographical ranges than previously understood. The scabrosoid clade consists of ten species, seven of which are new. For the dolichorhizoid clade, twenty-two new species were discovered for a total of twenty-nine species in this clade.
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http://dx.doi.org/10.1016/j.ympev.2017.08.013DOI Listing
December 2017

The transcription factor PDR-1 is a multi-functional regulator and key component of pectin deconstruction and catabolism in .

Biotechnol Biofuels 2017 12;10:149. Epub 2017 Jun 12.

HFM, TUM School of Life Sciences Weihenstephan, Technical University of Munich, Freising, Germany.

Background: Pectin is an abundant component in many fruit and vegetable wastes and could therefore be an excellent resource for biorefinery, but is currently underutilized. Fungal pectinases already play a crucial role for industrial purposes, such as for foodstuff processing. However, the regulation of pectinase gene expression is still poorly understood. For an optimal utilization of plant biomass for biorefinery and biofuel production, a detailed analysis of the underlying regulatory mechanisms is warranted. In this study, we applied the genetic resources of the filamentous ascomycete species to screen for transcription factors that play a major role in pectinase induction.

Results: The pectin degradation regulator-1 (PDR-1) was identified through a transcription factor mutant screen in . The Δ- mutant exhibited a severe growth defect on pectin and all tested pectin-related poly- and monosaccharides. Biochemical as well as transcriptional analyses of WT and the Δ- mutant revealed that while PDR-1-mediated gene induction was dependent on the presence of l-rhamnose, it also strongly affected the degradation of the homogalacturonan backbone. The expression of the endo-polygalacturonase - was greatly reduced in the Δ- mutant, while the expression levels of all pectate lyase genes increased. Moreover, a - overexpression strain displayed substantially increased pectinase production. Promoter analysis of the PDR-1 regulon allowed refinement of the putative PDR-1 DNA-binding motif.

Conclusions: PDR-1 is highly conserved in filamentous ascomycete fungi and is present in many pathogenic and industrially important fungi. Our data demonstrate that the function of PDR-1 in combines features of two recently described transcription factors in (RhaR) and (GaaR). The results presented in this study contribute to a broader understanding of how pectin degradation is orchestrated in filamentous fungi and how it could be manipulated for optimized pectinase production.
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http://dx.doi.org/10.1186/s13068-017-0807-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5469009PMC
June 2017

A parts list for fungal cellulosomes revealed by comparative genomics.

Nat Microbiol 2017 May 30;2:17087. Epub 2017 May 30.

Department of Chemical Engineering, University of California, Santa Barbara, California 93106, USA.

Cellulosomes are large, multiprotein complexes that tether plant biomass-degrading enzymes together for improved hydrolysis. These complexes were first described in anaerobic bacteria, where species-specific dockerin domains mediate the assembly of enzymes onto cohesin motifs interspersed within protein scaffolds. The versatile protein assembly mechanism conferred by the bacterial cohesin-dockerin interaction is now a standard design principle for synthetic biology. For decades, analogous structures have been reported in anaerobic fungi, which are known to assemble by sequence-divergent non-catalytic dockerin domains (NCDDs). However, the components, modular assembly mechanism and functional role of fungal cellulosomes remain unknown. Here, we describe a comprehensive set of proteins critical to fungal cellulosome assembly, including conserved scaffolding proteins unique to the Neocallimastigomycota. High-quality genomes of the anaerobic fungi Anaeromyces robustus, Neocallimastix californiae and Piromyces finnis were assembled with long-read, single-molecule technology. Genomic analysis coupled with proteomic validation revealed an average of 312 NCDD-containing proteins per fungal strain, which were overwhelmingly carbohydrate active enzymes (CAZymes), with 95 large fungal scaffoldins identified across four genera that bind to NCDDs. Fungal dockerin and scaffoldin domains have no similarity to their bacterial counterparts, yet several catalytic domains originated via horizontal gene transfer with gut bacteria. However, the biocatalytic activity of anaerobic fungal cellulosomes is expanded by the inclusion of GH3, GH6 and GH45 enzymes. These findings suggest that the fungal cellulosome is an evolutionarily chimaeric structure-an independently evolved fungal complex that co-opted useful activities from bacterial neighbours within the gut microbiome.
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http://dx.doi.org/10.1038/nmicrobiol.2017.87DOI Listing
May 2017

Widespread adenine N6-methylation of active genes in fungi.

Nat Genet 2017 Jun 8;49(6):964-968. Epub 2017 May 8.

US Department of Energy Joint Genome Institute, Walnut Creek, California, USA.

N6-methyldeoxyadenine (6mA) is a noncanonical DNA base modification present at low levels in plant and animal genomes, but its prevalence and association with genome function in other eukaryotic lineages remains poorly understood. Here we report that abundant 6mA is associated with transcriptionally active genes in early-diverging fungal lineages. Using single-molecule long-read sequencing of 16 diverse fungal genomes, we observed that up to 2.8% of all adenines were methylated in early-diverging fungi, far exceeding levels observed in other eukaryotes and more derived fungi. 6mA occurred symmetrically at ApT dinucleotides and was concentrated in dense methylated adenine clusters surrounding the transcriptional start sites of expressed genes; its distribution was inversely correlated with that of 5-methylcytosine. Our results show a striking contrast in the genomic distributions of 6mA and 5-methylcytosine and reinforce a distinct role for 6mA as a gene-expression-associated epigenomic mark in eukaryotes.
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http://dx.doi.org/10.1038/ng.3859DOI Listing
June 2017

Comparative genomics reveals high biological diversity and specific adaptations in the industrially and medically important fungal genus Aspergillus.

Authors:
Ronald P de Vries Robert Riley Ad Wiebenga Guillermo Aguilar-Osorio Sotiris Amillis Cristiane Akemi Uchima Gregor Anderluh Mojtaba Asadollahi Marion Askin Kerrie Barry Evy Battaglia Özgür Bayram Tiziano Benocci Susanna A Braus-Stromeyer Camila Caldana David Cánovas Gustavo C Cerqueira Fusheng Chen Wanping Chen Cindy Choi Alicia Clum Renato Augusto Corrêa Dos Santos André Ricardo de Lima Damásio George Diallinas Tamás Emri Erzsébet Fekete Michel Flipphi Susanne Freyberg Antonia Gallo Christos Gournas Rob Habgood Matthieu Hainaut María Laura Harispe Bernard Henrissat Kristiina S Hildén Ryan Hope Abeer Hossain Eugenia Karabika Levente Karaffa Zsolt Karányi Nada Kraševec Alan Kuo Harald Kusch Kurt LaButti Ellen L Lagendijk Alla Lapidus Anthony Levasseur Erika Lindquist Anna Lipzen Antonio F Logrieco Andrew MacCabe Miia R Mäkelä Iran Malavazi Petter Melin Vera Meyer Natalia Mielnichuk Márton Miskei Ákos P Molnár Giuseppina Mulé Chew Yee Ngan Margarita Orejas Erzsébet Orosz Jean Paul Ouedraogo Karin M Overkamp Hee-Soo Park Giancarlo Perrone Francois Piumi Peter J Punt Arthur F J Ram Ana Ramón Stefan Rauscher Eric Record Diego Mauricio Riaño-Pachón Vincent Robert Julian Röhrig Roberto Ruller Asaf Salamov Nadhira S Salih Rob A Samson Erzsébet Sándor Manuel Sanguinetti Tabea Schütze Kristina Sepčić Ekaterina Shelest Gavin Sherlock Vicky Sophianopoulou Fabio M Squina Hui Sun Antonia Susca Richard B Todd Adrian Tsang Shiela E Unkles Nathalie van de Wiele Diana van Rossen-Uffink Juliana Velasco de Castro Oliveira Tammi C Vesth Jaap Visser Jae-Hyuk Yu Miaomiao Zhou Mikael R Andersen David B Archer Scott E Baker Isabelle Benoit Axel A Brakhage Gerhard H Braus Reinhard Fischer Jens C Frisvad Gustavo H Goldman Jos Houbraken Berl Oakley István Pócsi Claudio Scazzocchio Bernhard Seiboth Patricia A vanKuyk Jennifer Wortman Paul S Dyer Igor V Grigoriev

Genome Biol 2017 02 14;18(1):28. Epub 2017 Feb 14.

US Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA, 94598, USA.

Background: The fungal genus Aspergillus is of critical importance to humankind. Species include those with industrial applications, important pathogens of humans, animals and crops, a source of potent carcinogenic contaminants of food, and an important genetic model. The genome sequences of eight aspergilli have already been explored to investigate aspects of fungal biology, raising questions about evolution and specialization within this genus.

Results: We have generated genome sequences for ten novel, highly diverse Aspergillus species and compared these in detail to sister and more distant genera. Comparative studies of key aspects of fungal biology, including primary and secondary metabolism, stress response, biomass degradation, and signal transduction, revealed both conservation and diversity among the species. Observed genomic differences were validated with experimental studies. This revealed several highlights, such as the potential for sex in asexual species, organic acid production genes being a key feature of black aspergilli, alternative approaches for degrading plant biomass, and indications for the genetic basis of stress response. A genome-wide phylogenetic analysis demonstrated in detail the relationship of the newly genome sequenced species with other aspergilli.

Conclusions: Many aspects of biological differences between fungal species cannot be explained by current knowledge obtained from genome sequences. The comparative genomics and experimental study, presented here, allows for the first time a genus-wide view of the biological diversity of the aspergilli and in many, but not all, cases linked genome differences to phenotype. Insights gained could be exploited for biotechnological and medical applications of fungi.
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http://dx.doi.org/10.1186/s13059-017-1151-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5307856PMC
February 2017

Evolutionary genomics of the cold-adapted diatom Fragilariopsis cylindrus.

Nature 2017 01 16;541(7638):536-540. Epub 2017 Jan 16.

Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, California 94598, USA.

The Southern Ocean houses a diverse and productive community of organisms. Unicellular eukaryotic diatoms are the main primary producers in this environment, where photosynthesis is limited by low concentrations of dissolved iron and large seasonal fluctuations in light, temperature and the extent of sea ice. How diatoms have adapted to this extreme environment is largely unknown. Here we present insights into the genome evolution of a cold-adapted diatom from the Southern Ocean, Fragilariopsis cylindrus, based on a comparison with temperate diatoms. We find that approximately 24.7 per cent of the diploid F. cylindrus genome consists of genetic loci with alleles that are highly divergent (15.1 megabases of the total genome size of 61.1 megabases). These divergent alleles were differentially expressed across environmental conditions, including darkness, low iron, freezing, elevated temperature and increased CO. Alleles with the largest ratio of non-synonymous to synonymous nucleotide substitutions also show the most pronounced condition-dependent expression, suggesting a correlation between diversifying selection and allelic differentiation. Divergent alleles may be involved in adaptation to environmental fluctuations in the Southern Ocean.
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http://dx.doi.org/10.1038/nature20803DOI Listing
January 2017

An expanded evaluation of protein function prediction methods shows an improvement in accuracy.

Authors:
Yuxiang Jiang Tal Ronnen Oron Wyatt T Clark Asma R Bankapur Daniel D'Andrea Rosalba Lepore Christopher S Funk Indika Kahanda Karin M Verspoor Asa Ben-Hur Da Chen Emily Koo Duncan Penfold-Brown Dennis Shasha Noah Youngs Richard Bonneau Alexandra Lin Sayed M E Sahraeian Pier Luigi Martelli Giuseppe Profiti Rita Casadio Renzhi Cao Zhaolong Zhong Jianlin Cheng Adrian Altenhoff Nives Skunca Christophe Dessimoz Tunca Dogan Kai Hakala Suwisa Kaewphan Farrokh Mehryary Tapio Salakoski Filip Ginter Hai Fang Ben Smithers Matt Oates Julian Gough Petri Törönen Patrik Koskinen Liisa Holm Ching-Tai Chen Wen-Lian Hsu Kevin Bryson Domenico Cozzetto Federico Minneci David T Jones Samuel Chapman Dukka Bkc Ishita K Khan Daisuke Kihara Dan Ofer Nadav Rappoport Amos Stern Elena Cibrian-Uhalte Paul Denny Rebecca E Foulger Reija Hieta Duncan Legge Ruth C Lovering Michele Magrane Anna N Melidoni Prudence Mutowo-Meullenet Klemens Pichler Aleksandra Shypitsyna Biao Li Pooya Zakeri Sarah ElShal Léon-Charles Tranchevent Sayoni Das Natalie L Dawson David Lee Jonathan G Lees Ian Sillitoe Prajwal Bhat Tamás Nepusz Alfonso E Romero Rajkumar Sasidharan Haixuan Yang Alberto Paccanaro Jesse Gillis Adriana E Sedeño-Cortés Paul Pavlidis Shou Feng Juan M Cejuela Tatyana Goldberg Tobias Hamp Lothar Richter Asaf Salamov Toni Gabaldon Marina Marcet-Houben Fran Supek Qingtian Gong Wei Ning Yuanpeng Zhou Weidong Tian Marco Falda Paolo Fontana Enrico Lavezzo Stefano Toppo Carlo Ferrari Manuel Giollo Damiano Piovesan Silvio C E Tosatto Angela Del Pozo José M Fernández Paolo Maietta Alfonso Valencia Michael L Tress Alfredo Benso Stefano Di Carlo Gianfranco Politano Alessandro Savino Hafeez Ur Rehman Matteo Re Marco Mesiti Giorgio Valentini Joachim W Bargsten Aalt D J van Dijk Branislava Gemovic Sanja Glisic Vladmir Perovic Veljko Veljkovic Nevena Veljkovic Danillo C Almeida-E-Silva Ricardo Z N Vencio Malvika Sharan Jörg Vogel Lakesh Kansakar Shanshan Zhang Slobodan Vucetic Zheng Wang Michael J E Sternberg Mark N Wass Rachael P Huntley Maria J Martin Claire O'Donovan Peter N Robinson Yves Moreau Anna Tramontano Patricia C Babbitt Steven E Brenner Michal Linial Christine A Orengo Burkhard Rost Casey S Greene Sean D Mooney Iddo Friedberg Predrag Radivojac

Genome Biol 2016 09 7;17(1):184. Epub 2016 Sep 7.

Department of Computer Science and Informatics, Indiana University, Bloomington, IN, USA.

Background: A major bottleneck in our understanding of the molecular underpinnings of life is the assignment of function to proteins. While molecular experiments provide the most reliable annotation of proteins, their relatively low throughput and restricted purview have led to an increasing role for computational function prediction. However, assessing methods for protein function prediction and tracking progress in the field remain challenging.

Results: We conducted the second critical assessment of functional annotation (CAFA), a timed challenge to assess computational methods that automatically assign protein function. We evaluated 126 methods from 56 research groups for their ability to predict biological functions using Gene Ontology and gene-disease associations using Human Phenotype Ontology on a set of 3681 proteins from 18 species. CAFA2 featured expanded analysis compared with CAFA1, with regards to data set size, variety, and assessment metrics. To review progress in the field, the analysis compared the best methods from CAFA1 to those of CAFA2.

Conclusions: The top-performing methods in CAFA2 outperformed those from CAFA1. This increased accuracy can be attributed to a combination of the growing number of experimental annotations and improved methods for function prediction. The assessment also revealed that the definition of top-performing algorithms is ontology specific, that different performance metrics can be used to probe the nature of accurate predictions, and the relative diversity of predictions in the biological process and human phenotype ontologies. While there was methodological improvement between CAFA1 and CAFA2, the interpretation of results and usefulness of individual methods remain context-dependent.
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http://dx.doi.org/10.1186/s13059-016-1037-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5015320PMC
September 2016

Comparative genomics of biotechnologically important yeasts.

Proc Natl Acad Sci U S A 2016 08 17;113(35):9882-7. Epub 2016 Aug 17.

Department of Bacteriology, University of Wisconsin-Madison, Madison, WI 53706;

Ascomycete yeasts are metabolically diverse, with great potential for biotechnology. Here, we report the comparative genome analysis of 29 taxonomically and biotechnologically important yeasts, including 16 newly sequenced. We identify a genetic code change, CUG-Ala, in Pachysolen tannophilus in the clade sister to the known CUG-Ser clade. Our well-resolved yeast phylogeny shows that some traits, such as methylotrophy, are restricted to single clades, whereas others, such as l-rhamnose utilization, have patchy phylogenetic distributions. Gene clusters, with variable organization and distribution, encode many pathways of interest. Genomics can predict some biochemical traits precisely, but the genomic basis of others, such as xylose utilization, remains unresolved. Our data also provide insight into early evolution of ascomycetes. We document the loss of H3K9me2/3 heterochromatin, the origin of ascomycete mating-type switching, and panascomycete synteny at the MAT locus. These data and analyses will facilitate the engineering of efficient biosynthetic and degradative pathways and gateways for genomic manipulation.
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http://dx.doi.org/10.1073/pnas.1603941113DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5024638PMC
August 2016

Expansion of Signal Transduction Pathways in Fungi by Extensive Genome Duplication.

Curr Biol 2016 06 26;26(12):1577-1584. Epub 2016 May 26.

US Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA 94598, USA.

Plants and fungi use light and other signals to regulate development, growth, and metabolism. The fruiting bodies of the fungus Phycomyces blakesleeanus are single cells that react to environmental cues, including light, but the mechanisms are largely unknown [1]. The related fungus Mucor circinelloides is an opportunistic human pathogen that changes its mode of growth upon receipt of signals from the environment to facilitate pathogenesis [2]. Understanding how these organisms respond to environmental cues should provide insights into the mechanisms of sensory perception and signal transduction by a single eukaryotic cell, and their role in pathogenesis. We sequenced the genomes of P. blakesleeanus and M. circinelloides and show that they have been shaped by an extensive genome duplication or, most likely, a whole-genome duplication (WGD), which is rarely observed in fungi [3-6]. We show that the genome duplication has expanded gene families, including those involved in signal transduction, and that duplicated genes have specialized, as evidenced by differences in their regulation by light. The transcriptional response to light varies with the developmental stage and is still observed in a photoreceptor mutant of P. blakesleeanus. A phototropic mutant of P. blakesleeanus with a heterozygous mutation in the photoreceptor gene madA demonstrates that photosensor dosage is important for the magnitude of signal transduction. We conclude that the genome duplication provided the means to improve signal transduction for enhanced perception of environmental signals. Our results will help to understand the role of genome dynamics in the evolution of sensory perception in eukaryotes.
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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5089372PMC
http://dx.doi.org/10.1016/j.cub.2016.04.038DOI Listing
June 2016

Widespread Polycistronic Transcripts in Fungi Revealed by Single-Molecule mRNA Sequencing.

PLoS One 2015 15;10(7):e0132628. Epub 2015 Jul 15.

Department of Energy Joint Genome Institute, Walnut Creek, California, United States of America; School of Natural Sciences, University of California at Merced, Merced, California, United States of America.

Genes in prokaryotic genomes are often arranged into clusters and co-transcribed into polycistronic RNAs. Isolated examples of polycistronic RNAs were also reported in some higher eukaryotes but their presence was generally considered rare. Here we developed a long-read sequencing strategy to identify polycistronic transcripts in several mushroom forming fungal species including Plicaturopsis crispa, Phanerochaete chrysosporium, Trametes versicolor, and Gloeophyllum trabeum. We found genome-wide prevalence of polycistronic transcription in these Agaricomycetes, involving up to 8% of the transcribed genes. Unlike polycistronic mRNAs in prokaryotes, these co-transcribed genes are also independently transcribed. We show that polycistronic transcription may interfere with expression of the downstream tandem gene. Further comparative genomic analysis indicates that polycistronic transcription is conserved among a wide range of mushroom forming fungi. In summary, our study revealed, for the first time, the genome prevalence of polycistronic transcription in a phylogenetic range of higher fungi. Furthermore, we systematically show that our long-read sequencing approach and combined bioinformatics pipeline is a generic powerful tool for precise characterization of complex transcriptomes that enables identification of mRNA isoforms not recovered via short-read assembly.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0132628PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4503453PMC
May 2016

Phylogenomic Analyses Indicate that Early Fungi Evolved Digesting Cell Walls of Algal Ancestors of Land Plants.

Genome Biol Evol 2015 May 14;7(6):1590-601. Epub 2015 May 14.

Department of Botany, University of British Columbia, Vancouver, British Columbia.

As decomposers, fungi are key players in recycling plant material in global carbon cycles. We hypothesized that genomes of early diverging fungi may have inherited pectinases from an ancestral species that had been able to extract nutrients from pectin-containing land plants and their algal allies (Streptophytes). We aimed to infer, based on pectinase gene expansions and on the organismal phylogeny, the geological timing of the plant-fungus association. We analyzed 40 fungal genomes, three of which, including Gonapodya prolifera, were sequenced for this study. In the organismal phylogeny from 136 housekeeping loci, Rozella diverged first from all other fungi. Gonapodya prolifera was included among the flagellated, predominantly aquatic fungal species in Chytridiomycota. Sister to Chytridiomycota were the predominantly terrestrial fungi including zygomycota I and zygomycota II, along with the ascomycetes and basidiomycetes that comprise Dikarya. The Gonapodya genome has 27 genes representing five of the seven classes of pectin-specific enzymes known from fungi. Most of these share a common ancestry with pectinases from Dikarya. Indicating functional and sequence similarity, Gonapodya, like many Dikarya, can use pectin as a carbon source for growth in pure culture. Shared pectinases of Dikarya and Gonapodya provide evidence that even ancient aquatic fungi had adapted to extract nutrients from the plants in the green lineage. This implies that 750 million years, the estimated maximum age of origin of the pectin-containing streptophytes represents a maximum age for the divergence of Chytridiomycota from the lineage including Dikarya.
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http://dx.doi.org/10.1093/gbe/evv090DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4494064PMC
May 2015

Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists.

Nat Genet 2015 Apr 23;47(4):410-5. Epub 2015 Feb 23.

1] Institut National de la Recherche Agronomique (INRA), Laboratory of Excellence Advanced Research on the Biology of Tree and Forest Ecosystems (ARBRE), UMR 1136, Champenoux, France. [2] University of Lorraine, Laboratory of Excellence ARBRE, UMR 1136, Champenoux, France.

To elucidate the genetic bases of mycorrhizal lifestyle evolution, we sequenced new fungal genomes, including 13 ectomycorrhizal (ECM), orchid (ORM) and ericoid (ERM) species, and five saprotrophs, which we analyzed along with other fungal genomes. Ectomycorrhizal fungi have a reduced complement of genes encoding plant cell wall-degrading enzymes (PCWDEs), as compared to their ancestral wood decayers. Nevertheless, they have retained a unique array of PCWDEs, thus suggesting that they possess diverse abilities to decompose lignocellulose. Similar functional categories of nonorthologous genes are induced in symbiosis. Of induced genes, 7-38% are orphan genes, including genes that encode secreted effector-like proteins. Convergent evolution of the mycorrhizal habit in fungi occurred via the repeated evolution of a 'symbiosis toolkit', with reduced numbers of PCWDEs and lineage-specific suites of mycorrhiza-induced genes.
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http://dx.doi.org/10.1038/ng.3223DOI Listing
April 2015

Alternative splicing acting as a bridge in evolution.

Stem Cell Investig 2015 30;2:19. Epub 2015 Oct 30.

1 US Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA 94598, USA ; 2 Roche Molecular Diagnostics, 4300 Hacienda Drive, Pleasanton, CA 94588, USA ; 3 Department of Clinical Medicine, Kunming University of Science and Technology, Kunming 650031, China.

Background: Alternative splicing (AS) regulates diverse cellular and developmental functions through alternative protein structures of different isoforms. Alternative exons dominate AS in vertebrates; however, very little is known about the extent and function of AS in lower eukaryotes. To understand the role of introns in gene evolution, we examined AS from a green algal and five fungal genomes using a novel EST-based gene-modeling algorithm (COMBEST).

Methods: AS from each genome was classified with COMBEST that maps EST sequences to genomes to build gene models. Various aspects of AS were analyzed through statistical methods. The interplay of intron 3n length, phase, coding property, and intron retention (RI) were examined with Chi-square testing.

Results: With 3 to 834 times EST coverage, we identified up to 73% of AS in intron-containing genes and found preponderance of RI among 11 types of AS. The number of exons, expression level, and maximum intron length correlated with number of AS per gene (NAG), and intron-rich genes suppressed AS. Genes with AS were more ancient, and AS was conserved among fungal genomes. Among stopless introns, non-retained introns (NRI) avoided, but major RI preferred 3n length. In contrast, stop-containing introns showed uniform distribution among 3n, 3n+1, and 3n+2 lengths. We found a clue to the intron phase enigma: it was the coding function of introns involved in AS that dictates the intron phase bias.

Conclusions: Majority of AS is non-functional, and the extent of AS is suppressed for intron-rich genes. RI through 3n length, stop codon, and phase bias bridges the transition from functionless to functional alternative isoforms.
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http://dx.doi.org/10.3978/j.issn.2306-9759.2015.10.01DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4923640PMC
June 2016

Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi.

Proc Natl Acad Sci U S A 2014 Jul 23;111(27):9923-8. Epub 2014 Jun 23.

US Department of Energy (DOE) Joint Genome Institute, Walnut Creek, CA 94598;

Basidiomycota (basidiomycetes) make up 32% of the described fungi and include most wood-decaying species, as well as pathogens and mutualistic symbionts. Wood-decaying basidiomycetes have typically been classified as either white rot or brown rot, based on the ability (in white rot only) to degrade lignin along with cellulose and hemicellulose. Prior genomic comparisons suggested that the two decay modes can be distinguished based on the presence or absence of ligninolytic class II peroxidases (PODs), as well as the abundance of enzymes acting directly on crystalline cellulose (reduced in brown rot). To assess the generality of the white-rot/brown-rot classification paradigm, we compared the genomes of 33 basidiomycetes, including four newly sequenced wood decayers, and performed phylogenetically informed principal-components analysis (PCA) of a broad range of gene families encoding plant biomass-degrading enzymes. The newly sequenced Botryobasidium botryosum and Jaapia argillacea genomes lack PODs but possess diverse enzymes acting on crystalline cellulose, and they group close to the model white-rot species Phanerochaete chrysosporium in the PCA. Furthermore, laboratory assays showed that both B. botryosum and J. argillacea can degrade all polymeric components of woody plant cell walls, a characteristic of white rot. We also found expansions in reducing polyketide synthase genes specific to the brown-rot fungi. Our results suggest a continuum rather than a dichotomy between the white-rot and brown-rot modes of wood decay. A more nuanced categorization of rot types is needed, based on an improved understanding of the genomics and biochemistry of wood decay.
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http://dx.doi.org/10.1073/pnas.1400592111DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4103376PMC
July 2014

Genomics of wood-degrading fungi.

Fungal Genet Biol 2014 Nov 20;72:82-90. Epub 2014 May 20.

US Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA 94598, United States. Electronic address:

Woody plants convert the energy of the sun into lignocellulosic biomass, which is an abundant substrate for bioenergy production. Fungi, especially wood decayers from the class Agaricomycetes, have evolved ways to degrade lignocellulose into its monomeric constituents, and understanding this process may facilitate the development of biofuels. Over the past decade genomics has become a powerful tool to study the Agaricomycetes. In 2004 the first sequenced genome of the white rot fungus Phanerochaete chrysosporium revealed a rich catalog of lignocellulolytic enzymes. In the decade that followed the number of genomes of Agaricomycetes grew to more than 75 and revealed a diversity of wood-decaying strategies. New technologies for high-throughput functional genomics are now needed to further study these organisms.
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http://dx.doi.org/10.1016/j.fgb.2014.05.001DOI Listing
November 2014