Hydrolysis of Untreated Lignocellulosic Feedstock Is Independent of S-Lignin

Total Page:16

File Type:pdf, Size:1020Kb

Hydrolysis of Untreated Lignocellulosic Feedstock Is Independent of S-Lignin Hooker et al. Biotechnol Biofuels (2018) 11:293 https://doi.org/10.1186/s13068-018-1292-8 Biotechnology for Biofuels RESEARCH Open Access Hydrolysis of untreated lignocellulosic feedstock is independent of S‑lignin composition in newly classifed anaerobic fungal isolate, Piromyces sp. UH3‑1 Casey A. Hooker1,2, Ethan T. Hillman1,3, Jonathan C. Overton1,2, Adrian Ortiz‑Velez1, Makayla Schacht4, Abigail Hunnicutt1, Nathan S. Mosier1,2 and Kevin V. Solomon1,2,3* Abstract Background: Plant biomass is an abundant but underused feedstock for bioenergy production due to its complex and variable composition, which resists breakdown into fermentable sugars. These feedstocks, however, are routinely degraded by many uncommercialized microbes such as anaerobic gut fungi. These gut fungi express a broad range of carbohydrate active enzymes and are native to the digestive tracts of ruminants and hindgut fermenters. In this study, we examine gut fungal performance on these substrates as a function of composition, and the ability of this isolate to degrade inhibitory high syringyl lignin-containing forestry residues. Results: We isolated a novel fungal specimen from a donkey in Independence, Indiana, United States. Phylogenetic analysis of the Internal Transcribed Spacer 1 sequence classifed the isolate as a member of the genus Piromyces within the phylum Neocallimastigomycota (Piromyces sp. UH3-1, strain UH3-1). The isolate penetrates the substrate with an extensive rhizomycelial network and secretes many cellulose-binding enzymes, which are active on various components of lignocellulose. These activities enable the fungus to hydrolyze at least 58% of the glucan and 28% of the available xylan in untreated corn stover within 168 h and support growth on crude agricultural residues, food waste, and energy crops. Importantly, UH3-1 hydrolyzes high syringyl lignin-containing poplar that is inhibitory to many fungi with efciencies equal to that of low syringyl lignin-containing poplar with no reduction in fungal growth. This behavior is correlated with slight remodeling of the fungal secretome whose composition adapts with substrate to express an enzyme cocktail optimized to degrade the available biomass. Conclusions: Piromyces sp. UH3-1, a newly isolated anaerobic gut fungus, grows on diverse untreated substrates through production of a broad range of carbohydrate active enzymes that are robust to variations in substrate composition. Additionally, UH3-1 and potentially other anaerobic fungi are resistant to inhibitory lignin composition possibly due to changes in enzyme secretion with substrate. Thus, anaerobic fungi are an attractive platform for the production of enzymes that efciently use mixed feedstocks of variable composition for second generation biofuels. More importantly, our work suggests that the study of anaerobic fungi may reveal naturally evolved strategies to circumvent common hydrolytic inhibitors that hinder biomass usage. Keywords: Anaerobic fungi, Neocallimastigomycota, Lignocellulose, Carbohydrate active enzymes, Lignin, Poplar *Correspondence: [email protected] 1 Department of Agricultural and Biological Engineering, Purdue University, 225 South University Street, West Lafayette, IN 47907‑2093, USA Full list of author information is available at the end of the article © The Author(s) 2018. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat​iveco​mmons​.org/licen​ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creat​iveco​mmons​.org/ publi​cdoma​in/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Hooker et al. Biotechnol Biofuels (2018) 11:293 Page 2 of 14 Background the extent of the cellulosic and xylanosic degradation by Lignocellulosic material is an inexpensive and abundant these enzymes across a range of lignin compositions. source of carbon that remains underexploited for biofuel Given the potential for anaerobic fungi to reduce production due to its complex heteropolymeric structure enzyme production costs, we sought to characterize that hinders release of fermentable sugars by lignocellulo- their enzymatic performance as a function of untreated lytic enzymes [1]. Available plant biomass for bioenergy substrate composition. Here, we report the isolation and is greatly dependent on geographic location and climate taxonomic placement of a recently isolated anaerobic gut variability, leading to large diferences in the types and fungal specimen (Piromyces sp. UH3-1) in the Neocalli- compositions of the potential substrates [2]. More impor- mastigaceae family. We characterize the ability of UH3-1 tantly, the biomass composition strongly afects the per- to degrade and grow on an array of untreated substrates formance of a given enzyme cocktail [3]. As a result, the (e.g., corn stover, switchgrass, orange peel, and sorghum) enzyme cocktails that are used to hydrolyze these feed- under mild conditions. Additionally, we measure the free stocks are optimized for individual substrates and are not sugars released from untreated poplar across a range of suitable for more economically viable feedstock streams lignin compositions to estimate fungal enzyme perfor- whose composition fuctuates greatly with market avail- mance with feedstock composition. Tis work suggests ability [4]. As enzyme cost is a signifcant bottleneck to that anaerobic fungal enzymes are robust for hydrolysis the development of economical biofuels, enzyme systems of diverse untreated lignocellulose and are promising that display superior performance on diverse feedstocks new candidates for lignocellulosic enzyme production. would advance the economic viability of bioenergy [5–7]. Current lignocellulolytic enzymes systems are based on Methods well-known fungi such as Trichoderma reesei and Asper- Isolating a novel species of anaerobic gut fungi gillus spp. due to their oversecretion of many glycoside We suspended fresh donkey feces in Hungate tubes con- hydrolyases (CAZymes), which are active on the glyco- taining sterile anaerobic medium C supplemented with sidic bonds of lignocellulosic materials [8]. However, 15% clarifed rumen fuid (150 ml: Bar Diamond Inc., these species do not naturally express all the enzymes Parma, ID, USA) under 100% CO 2 headspace [16]. Sus- needed to fully hydrolyze the sugars contained in plant pensions of donkey feces were serially diluted 1000-fold biomass [9]. For example, β-glucosidases in T. reesei, an and used as a 10% inoculum in Hungate tubes containing enzyme essential to release the free glucose, form < 1% 9 ml anaerobic medium C, supplemented with switch- of all secreted CAZymes [8]. Tus, enzyme cocktails grass as a carbon source (1% w/v) and chloramphenicol based on T. reesei must be supplemented with enzymes (25 µg/ml; Fisher Scientifc, Waltham, MA, USA). After from other species for sufcient activity [10]. Te need inoculation, the cultures were incubated at 39 °C for for cocktail supplementation with enzymes from various 72–96 h. species greatly increases enzyme production costs due to To obtain axenic cultures, we inoculated roll tubes with capital-intensive parallel enzyme production processes liquid fungal culture and propagated individual colo- [6, 11]. Terefore, a single species enzyme platform nies. Roll tubes were prepared by adding agar (2% w/v), would simplify enzyme production and reduce cost. glucose (0.45% w/v), and chloramphenicol (25 µg/ml) to Degradation of untreated biomass is common in many anaerobic medium C under 100% CO2 headspace [16]. underexplored environments that may harbor efcient We melted solid sterile media at 98 °C in a water bath microbial enzymes for biofuels. One example is the and cooled the media to ~ 45–50 °C prior to the addi- rumen and hindgut of large herbivores where grasses, tion of chloramphenicol and 1 ml of inoculum from a shrubs, and other untreated fber-rich plant biomass are liquid fungal culture in mid-exponential phase. Upon processed daily by a consortium of microbes including inoculation, the tubes were transferred to a benchtop early divergent Neocallimastigomycota (anaerobic fungi) and immediately rolled horizontally creating a uniform [12]. While anaerobic fungi are known to harness pow- agar-inoculum completely coating the walls. Te tubes erful biomass-degrading enzymes, the ability of these were incubated at 39 °C until colonies were visible, typi- enzymes to hydrolyze diverse plant biomass remains cally between 3 and 5 days. Following incubation, we poorly characterized [13]. To date, only fve specimens extracted individual colonies from the agar with a sterile in this phylum have been sequenced and studied in any needle while under CO2 headspace and transferred them detail [14]. Te fungi of Neocallimastigomycota thrive to new Hungate tubes containing 9 ml anaerobic medium under mild conditions (pH ≈ 7, 39 °C) and possess large C, switchgrass, and antibiotics (chloramphenicol [25 µg/ arrays of CAZymes that efciently degrade untreated ml in 40% ethanol], streptomycin [40 µg/ml], penicillin plant biomass [13, 15]. However, there are little data on [50 µg/ml], and kanamycin [25 µg/ml]). After 72–96 h, Hooker et al. Biotechnol Biofuels (2018) 11:293 Page 3 of 14 we used these cultures to inoculate
Recommended publications
  • S41467-021-25308-W.Pdf
    ARTICLE https://doi.org/10.1038/s41467-021-25308-w OPEN Phylogenomics of a new fungal phylum reveals multiple waves of reductive evolution across Holomycota ✉ ✉ Luis Javier Galindo 1 , Purificación López-García 1, Guifré Torruella1, Sergey Karpov2,3 & David Moreira 1 Compared to multicellular fungi and unicellular yeasts, unicellular fungi with free-living fla- gellated stages (zoospores) remain poorly known and their phylogenetic position is often 1234567890():,; unresolved. Recently, rRNA gene phylogenetic analyses of two atypical parasitic fungi with amoeboid zoospores and long kinetosomes, the sanchytrids Amoeboradix gromovi and San- chytrium tribonematis, showed that they formed a monophyletic group without close affinity with known fungal clades. Here, we sequence single-cell genomes for both species to assess their phylogenetic position and evolution. Phylogenomic analyses using different protein datasets and a comprehensive taxon sampling result in an almost fully-resolved fungal tree, with Chytridiomycota as sister to all other fungi, and sanchytrids forming a well-supported, fast-evolving clade sister to Blastocladiomycota. Comparative genomic analyses across fungi and their allies (Holomycota) reveal an atypically reduced metabolic repertoire for sanchy- trids. We infer three main independent flagellum losses from the distribution of over 60 flagellum-specific proteins across Holomycota. Based on sanchytrids’ phylogenetic position and unique traits, we propose the designation of a novel phylum, Sanchytriomycota. In addition, our results indicate that most of the hyphal morphogenesis gene repertoire of multicellular fungi had already evolved in early holomycotan lineages. 1 Ecologie Systématique Evolution, CNRS, Université Paris-Saclay, AgroParisTech, Orsay, France. 2 Zoological Institute, Russian Academy of Sciences, St. ✉ Petersburg, Russia. 3 St.
    [Show full text]
  • University of Groningen Multiple Origins of Hydrogenosomes
    University of Groningen Multiple origins of hydrogenosomes Voncken, F; Boxma, B; Tjaden, J; Akhmanova, A; Huynen, M; Tielens, AGM; Haferkamp, [No Value]; Neuhaus, HE; Vogels, G; Veenhuis, M Published in: Molecular Microbiology DOI: 10.1046/j.1365-2958.2002.02959.x IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 2002 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Voncken, F., Boxma, B., Tjaden, J., Akhmanova, A., Huynen, M., Tielens, AGM., Haferkamp, N. V., Neuhaus, HE., Vogels, G., Veenhuis, M., Hackstein, JHP., Tielens, A. G. M., Haferkamp, I., & Hackstein, J. H. P. (2002). Multiple origins of hydrogenosomes: functional and phylogenetic evidence from the ADP/ATP carrier of the anaerobic chytrid Neocallimastix sp. Molecular Microbiology, 44(6), 1441-1454. https://doi.org/10.1046/j.1365-2958.2002.02959.x Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum.
    [Show full text]
  • UC Santa Barbara Dissertation Template
    UNIVERSITY OF CALIFORNIA Santa Barbara Deciphering the Functions of Natural Products from Anaerobic Fungi for Applications in Biotechnology A dissertation submitted in partial satisfaction of the requirements for the degree Doctor of Philosophy in Chemical Engineering by Candice Lee Swift Committee in charge: Professor Michelle A. O’Malley, Chair Professor Siddharth Dey Professor Song-I-Han Professor David Low December 2020 The dissertation of Candice Lee Swift is approved. ____________________________________________ Siddharth Dey ____________________________________________ Song-I Han ____________________________________________ David Low ____________________________________________ Michelle A. O’Malley, Committee Chair December 2020 ACKNOWLEDGEMENTS I would like to thank my advisor, Michelle O’Malley, for the opportunity to work in her lab and achieve the work described in this dissertation. I would also like to thank all O’Malley lab members, both past and present. I am extremely grateful for the training I received from others in the lab and for the foundation that previous lab members laid in isolating anaerobic fungi and sequencing their genomes and transcriptomes. I also want to thank Nikola Malinov, the diligent undergraduate researcher whose help in lab was invaluable to me and who contributed to the experiments in Chapter five. I would also like to thank our collaborators at the Joint Genome Institute, the Environmental Molecular Sciences Laboratory, and both the Keller lab at the University of Wisconsin-Madison as well as the Solomon lab at Purdue for their experimental contributions and insight. Dr. Jennifer Smith at the Biological Nanostructures Laboratory at UCSB was particularly helpful to me during the library preparation steps of Chapter five. I am grateful to professors Jennifer Reed, Nicholas Abbott, and Betty Chewning for writing letters of recommendation for me when I applied to graduate school after working for five years in industry.
    [Show full text]
  • MICRO-ORGANISMS and RUMINANT DIGESTION: STATE of KNOWLEDGE, TRENDS and FUTURE PROSPECTS Chris Mcsweeney1 and Rod Mackie2
    BACKGROUND STUDY PAPER NO. 61 September 2012 E Organización Food and Organisation des Продовольственная и cельскохозяйственная de las Agriculture Nations Unies Naciones Unidas Organization pour организация para la of the l'alimentation Объединенных Alimentación y la United Nations et l'agriculture Наций Agricultura COMMISSION ON GENETIC RESOURCES FOR FOOD AND AGRICULTURE MICRO-ORGANISMS AND RUMINANT DIGESTION: STATE OF KNOWLEDGE, TRENDS AND FUTURE PROSPECTS Chris McSweeney1 and Rod Mackie2 The content of this document is entirely the responsibility of the authors, and does not necessarily represent the views of the FAO or its Members. 1 Commonwealth Scientific and Industrial Research Organisation, Livestock Industries, 306 Carmody Road, St Lucia Qld 4067, Australia. 2 University of Illinois, Urbana, Illinois, United States of America. This document is printed in limited numbers to minimize the environmental impact of FAO's processes and contribute to climate neutrality. Delegates and observers are kindly requested to bring their copies to meetings and to avoid asking for additional copies. Most FAO meeting documents are available on the Internet at www.fao.org ME992 BACKGROUND STUDY PAPER NO.61 2 Table of Contents Pages I EXECUTIVE SUMMARY .............................................................................................. 5 II INTRODUCTION ............................................................................................................ 7 Scope of the Study ...........................................................................................................
    [Show full text]
  • Effects of Piromyces Sp. CN6 CGMCC 14449 on Fermentation Quality
    Wang et al. AMB Expr (2019) 9:121 https://doi.org/10.1186/s13568-019-0846-x ORIGINAL ARTICLE Open Access Efects of Piromyces sp. CN6 CGMCC 14449 on fermentation quality, nutrient composition and the in vitro degradation rate of whole crop maize silage Dangdang Wang1, Congcong Zhao1, Shimin Liu2, Tao Zhang1, Junhu Yao1 and Yangchun Cao1* Abstract This study investigated the efects of the rumen fungus Piromyces sp. CN6 CGMCC 14449 as a silage additive on the fermentation quality, nutrient composition and in vitro digestibility of whole crop maize silage. Whole crop maize served as the silage material and was vacuum packed in polyethylene bags. Three ensiling treatments were applied: a control (CK), addition of a fungus (FU) at 105 thallus-forming units per gram, and addition of compound enzyme (EN) at 0.033 mg/g (containing cellulase and xylanase at activities of 90 flter paper units and 6000 IU per gram, respec- tively). Compared with the CK, the FU and EN treatments decreased the pH after 30 days fermentation (P <0.05). Both FU and EN treatments increased the lactate, crude protein, and water-soluble carbohydrate contents (P <0.05), whereas reduced the acetate, ADF and NDF contents as well as the ammonia nitrogen to total nitrogen ratio in silage after 30 days of ensilaging (P <0.05), compared with those for the CK, while no changes were found in the dry matter and dry matter recovery (P > 0.05). The fungal inoculant increased the in vitro digestibility of dry matter, NDF and ADF in silage after 30 days fermentation (P <0.05).
    [Show full text]
  • Transcriptomic Characterization of Caecomyces Churrovis: a Novel, Non‑Rhizoid‑Forming Lignocellulolytic Anaerobic Fungus John K
    Henske et al. Biotechnol Biofuels (2017) 10:305 https://doi.org/10.1186/s13068-017-0997-4 Biotechnology for Biofuels RESEARCH Open Access Transcriptomic characterization of Caecomyces churrovis: a novel, non‑rhizoid‑forming lignocellulolytic anaerobic fungus John K. Henske1, Sean P. Gilmore1, Doriv Knop1, Francis J. Cunningham1, Jessica A. Sexton1, Chuck R. Smallwood2, Vaithiyalingam Shutthanandan2, James E. Evans2, Michael K. Theodorou3 and Michelle A. O’Malley1* Abstract Anaerobic gut fungi are the primary colonizers of plant material in the rumen microbiome, but are poorly studied due to a lack of characterized isolates. While most genera of gut fungi form extensive rhizoidal networks, which likely participate in mechanical disruption of plant cell walls, fungi within the Caecomyces genus do not possess these rhizoids. Here, we describe a novel fungal isolate, Caecomyces churrovis, which forms spherical sporangia with a limited rhizoidal network yet secretes a diverse set of carbohydrate active enzymes (CAZymes) for plant cell wall hydrolysis. Despite lacking an extensive rhizoidal system, C. churrovis is capable of growth on fbrous substrates like switchgrass, reed canary grass, and corn stover, although faster growth is observed on soluble sugars. Gut fungi have been shown to use enzyme complexes (fungal cellulosomes) in which CAZymes bind to non-catalytic scafoldins to improve bio- mass degradation efciency. However, transcriptomic analysis and enzyme activity assays reveal that C. churrovis relies more on free enzymes compared to other gut fungal isolates. Only 15% of CAZyme transcripts contain non-catalytic dockerin domains in C. churrovis, compared to 30% in rhizoid-forming fungi. Furthermore, C. churrovis is enriched in GH43 enzymes that provide complementary hemicellulose degrading activities, suggesting that a wider variety of these activities are required to degrade plant biomass in the absence of an extensive fungal rhizoid network.
    [Show full text]
  • A R T IC L E Anaerobic Fungi: Neocallimastigomycota
    View metadata, citation and similar papers at core.ac.uk brought to you by CORE IMA FuNgus · voluMe 1 · No 2: 181–185provided by PubMed Central Anaerobic fungi: Neocallimastigomycota ARTICLE Gareth W Griffith1, Scott Baker2, Kate Fliegerova3, Audra Liggenstoffer4, Mark van der Giezen5, Kerstin Voigt6 and Gordon Beakes7 1IBERS, Aberystwyth University, Aberystwyth SY23 3DD, Wales; corresponding author e-mail: [email protected] 2Chemical and Biological Process Development Group, Energy and Environment Directorate, Pacific Northwest National Laboratory, 902 Battelle Boulevard, P.O. Box 999, MSIN P8-60 Richland, WA 99352 USA 3Institute of Animal Physiology and Genetics, Academy of Sciences of Czech Republic, Videnska 1083, Prague 4 - Krc, 142 20 Czech Republic 4Department of Microbiology and Molecular Genetics, Oklahoma State University, Stillwater, OK, USA 5Centre for Eukaryotic Evolutionary Microbiology, Biosciences, College of Life & Environmental Sciences, University of Exeter, Stocker Road, Exeter EX4 4QD, UK 6Friedrich Schiller University Jena, Institute of Microbiology, Department of Microbiology and Molecular Biology, Jena Microbial Research Collection, Neugasse 25, 07743 Jena, Germany 7School of Biology, Newcastle University, Newcastle upon Tyne NE1 7RU, UK Abstract: This contribution is based on the six oral presentations given at the Special Interest Group Key words: session on anaerobic fungi held during IMC9. These fungi, recently elevated to the status of a separate chytrid phylum (Neocallimastigomycota), distinct from the chytrid
    [Show full text]
  • Cytosolic Enzymes with a Mitochondrial Ancestry from the Anaerobic Chytrid Piromyces Sp
    Molecular Microbiology (1998) 30(5), 1017–1027 Cytosolic enzymes with a mitochondrial ancestry from the anaerobic chytrid Piromyces sp. E2 Anna Akhmanova,†‡* Frank G. J. Voncken,‡ Harry zoospore stages and a vegetative phase in which a com- Harhangi, Ken M. Hosea, Godfried D. Vogels and plex rhizomycelial system is formed. The hyphae of the Johannes H. P. Hackstein rhizomycelial system attach to plant-derived particles of Department of Microbiology and Evolutionary Biology, the digesta, and the intestinal chytrids contribute signifi- Faculty of Science, University of Nijmegen, Toernooiveld, cantly to the digestion of plant polymers by the production NL-6525 ED Nijmegen, The Netherlands. and excretion of a broad spectrum of (cellulolytic and other) enzymes (Teunissen et al., 1991; Orpin, 1994). Summary These highly specialized anaerobic chytrids evolved from mitochondria-bearing aerobic ancestors, as phylo- The anaerobic chytrid Piromyces sp. E2 lacks mito- genetic analysis of their rRNA genes has shown unequivo- chondria, but contains hydrogen-producing organ- cally that yeasts and fungi belong to a ‘crown group’ of elles, the hydrogenosomes. We are interested in how eukaryotic microorganisms that includes the aerobic and the adaptation to anaerobiosis influenced enzyme com- anaerobic chytrids (Sogin, 1991; Knoll, 1992). DNA sequ- partmentalization in this organism. Random sequenc- ence analysis reveals a clustering of both aerobic and ing of a cDNA library from Piromyces sp. E2 resulted anaerobic chytrids (Dore and Stahl, 1991; Bowman et in the isolation of cDNAs encoding malate dehydro- al., 1992; Li and Heath, 1992). Also, an analysis of bio- genase, aconitase and acetohydroxyacid reductoiso- chemical (Ragan and Chapman, 1978) and morphological merase.
    [Show full text]
  • 487215V1.Full.Pdf
    bioRxiv preprint doi: https://doi.org/10.1101/487215; this version posted December 4, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Horizontal gene transfer as an indispensible driver for Neocallimastigomycota 2 evolution into a distinct gut-dwelling fungal lineage 3 4 Chelsea L. Murphy1¶, Noha H. Youssef1¶, Radwa A. Hanafy1, MB Couger2, Jason E. 5 Stajich3, Y. Wang3, Kristina Baker1, Sumit S. Dagar4, Gareth W. Griffith5, Ibrahim F. 6 Farag1, TM Callaghan6, and Mostafa S. Elshahed1* 7 1Department of Microbiology and Molecular Genetics and 2 High Performance Computing Center, 8 Oklahoma State University, Stillwater, OK. 3Department of Microbiology and Plant Pathology, Institute 9 for Integrative Genome Biology, University of California-Riverside, Riverside, CA. Bioenergy group, 10 Agharkar Research Institute, Pune, India. 5Institute of Biological, Environmental, and Rural Sciences 11 (IBERS) Aberystwyth University, Aberystwyth, Wales, UK. 6Department for Quality Assurance and 12 Analytics, Bavarian State Research Center for Agriculture, Freising, Germany. 13 14 15 Running Title: HGT in the Neocallimastigomycota 16 17 *Corresponding author: Mailing address: Oklahoma State University, Department of 18 Microbiology and Molecular Genetics, 1110 S Innovation Way, Stillwater, OK 74074. Phone: 19 (405) 744-3005, Fax: (405) 744-1112. Email: [email protected]. 20 21 ¶ Both authors contributed equally to this work. 22 1 bioRxiv preprint doi: https://doi.org/10.1101/487215; this version posted December 4, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.
    [Show full text]
  • High-Level Classification of the Fungi and a Tool for Evolutionary Ecological Analyses
    Fungal Diversity (2018) 90:135–159 https://doi.org/10.1007/s13225-018-0401-0 (0123456789().,-volV)(0123456789().,-volV) High-level classification of the Fungi and a tool for evolutionary ecological analyses 1,2,3 4 1,2 3,5 Leho Tedersoo • Santiago Sa´nchez-Ramı´rez • Urmas Ko˜ ljalg • Mohammad Bahram • 6 6,7 8 5 1 Markus Do¨ ring • Dmitry Schigel • Tom May • Martin Ryberg • Kessy Abarenkov Received: 22 February 2018 / Accepted: 1 May 2018 / Published online: 16 May 2018 Ó The Author(s) 2018 Abstract High-throughput sequencing studies generate vast amounts of taxonomic data. Evolutionary ecological hypotheses of the recovered taxa and Species Hypotheses are difficult to test due to problems with alignments and the lack of a phylogenetic backbone. We propose an updated phylum- and class-level fungal classification accounting for monophyly and divergence time so that the main taxonomic ranks are more informative. Based on phylogenies and divergence time estimates, we adopt phylum rank to Aphelidiomycota, Basidiobolomycota, Calcarisporiellomycota, Glomeromycota, Entomoph- thoromycota, Entorrhizomycota, Kickxellomycota, Monoblepharomycota, Mortierellomycota and Olpidiomycota. We accept nine subkingdoms to accommodate these 18 phyla. We consider the kingdom Nucleariae (phyla Nuclearida and Fonticulida) as a sister group to the Fungi. We also introduce a perl script and a newick-formatted classification backbone for assigning Species Hypotheses into a hierarchical taxonomic framework, using this or any other classification system. We provide an example
    [Show full text]
  • The Anaerobic Fungi: Challenges and Opportunities for Industrial Lignocellulosic Biofuel Production
    microorganisms Review The Anaerobic Fungi: Challenges and Opportunities for Industrial Lignocellulosic Biofuel Production Luke M. G. Saye 1,2, Tejas A. Navaratna 3 , James P. J. Chong 1 , Michelle A. O’Malley 3 , Michael K. Theodorou 2,* and Matthew Reilly 1,* 1 Department of Biology, University of York, York YO10 5DD, UK; [email protected] (L.M.G.S.); [email protected] (J.P.J.C.) 2 Department of Agriculture and the Environment, Harper Adams University, Newport TF10 8NB, UK 3 Department of Chemical Engineering, University of California, Santa Barbara, CA 93106, USA; [email protected] (T.A.N.); [email protected] (M.A.O.) * Correspondence: [email protected] (M.K.T.); [email protected] (M.R.) Abstract: Lignocellulose is a promising feedstock for biofuel production as a renewable, carbohydrate- rich and globally abundant source of biomass. However, challenges faced include environmental and/or financial costs associated with typical lignocellulose pretreatments needed to overcome the natural recalcitrance of the material before conversion to biofuel. Anaerobic fungi are a group of underexplored microorganisms belonging to the early diverging phylum Neocallimastigomycota and are native to the intricately evolved digestive system of mammalian herbivores. Anaerobic fungi have promising potential for application in biofuel production processes due to the combination of Citation: Saye, L.M.G.; Navaratna, their highly effective ability to hydrolyse lignocellulose and capability to convert this substrate to H2 T.A.; Chong, J.P.J.; O’Malley, M.A.; and ethanol. Furthermore, they can produce volatile fatty acid precursors for subsequent biological Theodorou, M.K.; Reilly, M.
    [Show full text]
  • UC Santa Barbara Dissertation Template
    UNIVERSITY OF CALIFORNIA Santa Barbara Developing a systems biology framework to engineer anaerobic gut fungi A dissertation submitted in partial satisfaction of the requirements for the degree Doctor of Philosophy in Chemical Engineering by St. Elmo Wilken Committee in charge: Professor Michelle A. O’Malley, Co-chair Professor Linda R. Petzold, Co-chair Professor M. Scott Shell Professor Elizabeth G. Wilbanks September 2020 The dissertation of St. Elmo Wilken is approved. ____________________________________________ Elizabeth G. Wilbanks ____________________________________________ M. Scott Shell ____________________________________________ Linda R. Petzold, Committee co-chair ____________________________________________ Michelle A. O’Malley, Committee co-chair September 2020 Developing a systems biology framework to engineer anaerobic gut fungi Copyright © 2020 by St. Emo Wilken iii ACKNOWLEDGEMENTS First, I would like to acknowledge and thank God for giving me the opportunity and ability to pursue my Ph. D. at UCSB. Next, I would like to thank my advisors, Michelle O’Malley and Linda Petzold for their guidance, support and encouragement in completing the work that went into this thesis. They always supported me in my desire to explore new avenues of inquiry and were patient when things did not work out as expected. The Dow Discovery Fellowship was also instrumental in the research freedom I had, and I gratefully acknowledge its support. I would also like to acknowledge the entire O’Malley lab, but specifically Susanna Seppälä and Tom Lankiewicz for their many insightful discussions about biology and their patience in explaining it to an engineer. I would also like to thank Jon Monk for guiding me through the process of developing the first genome-scale model of a decidedly non-model anaerobic gut fungus.
    [Show full text]