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Title: PCR and Omics Based Techniques to Study the Diversity, Ecology and Biology of Anaerobic Fungi: Insights, Challenges and Opportunities

Abstract

Anaerobic fungi (phylum Neocallimastigomycota) are common inhabitants of the digestive tract of mammalian herbivores, and in the rumen, can account for up to 20% of the microbial biomass. Anaerobic fungi play a primary role in the degradation of lignocellulosic plant material. They also have a syntrophic interaction with methanogenic archaea, which increases their fiber degradation activity. To date, nine anaerobic fungal genera have been described, with further novel taxonomic groupings known to exist based on culture-independent molecular surveys. However, the true extent of their diversity may be even more extensively underestimated as anaerobic fungi continue being discovered in yet unexplored gut and non-gut environments. Additionally many studies are now known to have used primers that provide incomplete coverage of the Neocallimastigomycota. For ecological studies the internal transcribed spacer 1 region (ITS1) has been the taxonomic marker of choice, but due to various limitations the large subunit rRNA (LSU) is now being increasingly used. How the continued expansion of our knowledge regarding anaerobic fungal diversity will impact on our understanding of their biology and ecological role remains unclear; particularly as it is becoming apparent that anaerobic fungi display niche differentiation. As a consequence, there is a need to move beyond themore » broad generalization of anaerobic fungi as fiber-degraders, and explore the fundamental differences that underpin their ability to exist in distinct ecological niches. Application of genomics, transcriptomics, proteomics and metabolomics to their study in pure/mixed cultures and environmental samples will be invaluable in this process. To date the genomes and transcriptomes of several characterized anaerobic fungal isolates have been successfully generated. In contrast, the application of proteomics and metabolomics to anaerobic fungal analysis is still in its infancy. A central problem for all analyses, however, is the limited functional annotation of anaerobic fungal sequence data. There is therefore an urgent need to expand information held within publicly available reference databases. Finally, once this challenge is overcome, along with improved sample collection and extraction, the application of these techniques will be key in furthering our understanding of the ecological role and impact of anaerobic fungi in the wide range of environments they inhabit.« less

Authors:
 [1];  [2];  [3];  [3];  [4];  [5];  [6];  [7];  [8];  [9];  [10];  [10];  [10];  [11];  [1]
  1. Wageningen Univ. & Research, Wageningen (Netherlands). Lab. of Microbiology
  2. Agriculture and Agri-Food Canada, Lethbridge, AB (Canada). Lethbridge Research and Development Centre
  3. Bavarian State Research Center for Agriculture, Freising (Germany). Dept. for Quality Assurance and Analytics
  4. Agharkar Research Inst., Pune (India). Bioenergy Group
  5. Nanjing Agricultural Univ., Nanjing (China). Lab. of Gastrointestinal Microbiology
  6. Korea National Open Univ., Seoul (South Korea). Dept. of Agricultural Science
  7. AgResearch Ltd., Palmerston North (New Zealand). Grasslands Research Centre
  8. Czech Academy of Sciences, Prague (Czechia). Inst. of Animal Physiology and Genetics
  9. Guru Angad Dev Veterinary and Animal Sciences Univ., Ludhiana (India). College of Dairy Science and Technology; CAR-National Dairy Research Inst., Karnal (India). Dairy Microbiology Division
  10. Univ. of California, Santa Barbara, CA (United States). Dept. of Chemical Engineering
  11. Aberystwyth Univ., Aberystwyth (United Kingdom). Inst. of Biological Environmental and Rural Sciences
Publication Date:
Research Org.:
Univ. of California, Santa Barbara, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); European Union (EU); National Science Foundation (NSF)
OSTI Identifier:
1424614
Grant/Contract Number:  
SC0010352; AC02-05CH11231; AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 8; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; anerobic fungi; Neocallimastigomycota; rumen; phylogeny; genomics; (meta) transcriptomics; proteomics; metabolomics

Citation Formats

Edwards, Joan E., Forster, Robert J., Callaghan, Tony M., Dollhofer, Veronika, Dagar, Sumit S., Cheng, Yanfen, Chang, Jongsoo, Kittelmann, Sandra, Fliegerova, Katerina, Puniya, Anil K., Henske, John K., Gilmore, Sean P., O'Malley, Michelle A., Griffith, Gareth W., and Smidt, Hauke. PCR and Omics Based Techniques to Study the Diversity, Ecology and Biology of Anaerobic Fungi: Insights, Challenges and Opportunities. United States: N. p., 2017. Web. doi:10.3389/fmicb.2017.01657.
Edwards, Joan E., Forster, Robert J., Callaghan, Tony M., Dollhofer, Veronika, Dagar, Sumit S., Cheng, Yanfen, Chang, Jongsoo, Kittelmann, Sandra, Fliegerova, Katerina, Puniya, Anil K., Henske, John K., Gilmore, Sean P., O'Malley, Michelle A., Griffith, Gareth W., & Smidt, Hauke. PCR and Omics Based Techniques to Study the Diversity, Ecology and Biology of Anaerobic Fungi: Insights, Challenges and Opportunities. United States. doi:10.3389/fmicb.2017.01657.
Edwards, Joan E., Forster, Robert J., Callaghan, Tony M., Dollhofer, Veronika, Dagar, Sumit S., Cheng, Yanfen, Chang, Jongsoo, Kittelmann, Sandra, Fliegerova, Katerina, Puniya, Anil K., Henske, John K., Gilmore, Sean P., O'Malley, Michelle A., Griffith, Gareth W., and Smidt, Hauke. Mon . "PCR and Omics Based Techniques to Study the Diversity, Ecology and Biology of Anaerobic Fungi: Insights, Challenges and Opportunities". United States. doi:10.3389/fmicb.2017.01657. https://www.osti.gov/servlets/purl/1424614.
@article{osti_1424614,
title = {PCR and Omics Based Techniques to Study the Diversity, Ecology and Biology of Anaerobic Fungi: Insights, Challenges and Opportunities},
author = {Edwards, Joan E. and Forster, Robert J. and Callaghan, Tony M. and Dollhofer, Veronika and Dagar, Sumit S. and Cheng, Yanfen and Chang, Jongsoo and Kittelmann, Sandra and Fliegerova, Katerina and Puniya, Anil K. and Henske, John K. and Gilmore, Sean P. and O'Malley, Michelle A. and Griffith, Gareth W. and Smidt, Hauke},
abstractNote = {Anaerobic fungi (phylum Neocallimastigomycota) are common inhabitants of the digestive tract of mammalian herbivores, and in the rumen, can account for up to 20% of the microbial biomass. Anaerobic fungi play a primary role in the degradation of lignocellulosic plant material. They also have a syntrophic interaction with methanogenic archaea, which increases their fiber degradation activity. To date, nine anaerobic fungal genera have been described, with further novel taxonomic groupings known to exist based on culture-independent molecular surveys. However, the true extent of their diversity may be even more extensively underestimated as anaerobic fungi continue being discovered in yet unexplored gut and non-gut environments. Additionally many studies are now known to have used primers that provide incomplete coverage of the Neocallimastigomycota. For ecological studies the internal transcribed spacer 1 region (ITS1) has been the taxonomic marker of choice, but due to various limitations the large subunit rRNA (LSU) is now being increasingly used. How the continued expansion of our knowledge regarding anaerobic fungal diversity will impact on our understanding of their biology and ecological role remains unclear; particularly as it is becoming apparent that anaerobic fungi display niche differentiation. As a consequence, there is a need to move beyond the broad generalization of anaerobic fungi as fiber-degraders, and explore the fundamental differences that underpin their ability to exist in distinct ecological niches. Application of genomics, transcriptomics, proteomics and metabolomics to their study in pure/mixed cultures and environmental samples will be invaluable in this process. To date the genomes and transcriptomes of several characterized anaerobic fungal isolates have been successfully generated. In contrast, the application of proteomics and metabolomics to anaerobic fungal analysis is still in its infancy. A central problem for all analyses, however, is the limited functional annotation of anaerobic fungal sequence data. There is therefore an urgent need to expand information held within publicly available reference databases. Finally, once this challenge is overcome, along with improved sample collection and extraction, the application of these techniques will be key in furthering our understanding of the ecological role and impact of anaerobic fungi in the wide range of environments they inhabit.},
doi = {10.3389/fmicb.2017.01657},
journal = {Frontiers in Microbiology},
number = ,
volume = 8,
place = {United States},
year = {2017},
month = {9}
}

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Molecular analysis of the anaerobic rumen fungus Orpinomyces - insights into an AT-rich genome
journal, January 2005


Neocallimastix patriciarum sp.nov., a new member of the Neocallimasticaceae inhabiting the rumen of sheep
journal, January 1986


Metatranscriptomics Reveals the Active Bacterial and Eukaryotic Fibrolytic Communities in the Rumen of Dairy Cow Fed a Mixed Diet
journal, January 2017

  • Comtet-Marre, Sophie; Parisot, Nicolas; Lepercq, Pascale
  • Frontiers in Microbiology, Vol. 8
  • DOI: 10.3389/fmicb.2017.00067

Detection and monitoring of anaerobic rumen fungi using an ARISA method
journal, December 2008


Fungal diversity notes 111–252—taxonomic and phylogenetic contributions to fungal taxa
journal, November 2015

  • Ariyawansa, Hiran A.; Hyde, Kevin D.; Jayasiri, Subashini C.
  • Fungal Diversity, Vol. 75, Issue 1
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Pecoramyces ruminantium , gen. nov., sp. nov., an anaerobic gut fungus from the feces of cattle and sheep
journal, March 2017


Metagenomics of the Svalbard Reindeer Rumen Microbiome Reveals Abundance of Polysaccharide Utilization Loci
journal, June 2012


The UNITE database for molecular identification of fungi - recent updates and future perspectives: Letters
journal, March 2010


Effect of administration of rumen fungi on production performance of lactating buffaloes
journal, June 2010

  • Saxena, S.; Sehgal, J.; Puniya, A.
  • Beneficial Microbes, Vol. 1, Issue 2
  • DOI: 10.3920/BM2009.0018

Development of three specific PCR-based tools to determine quantity, cellulolytic transcriptional activity and phylogeny of anaerobic fungi
journal, August 2016

  • Dollhofer, Veronika; Callaghan, Tony Martin; Dorn-In, Samart
  • Journal of Microbiological Methods, Vol. 127
  • DOI: 10.1016/j.mimet.2016.05.017

A fast and reliable procedure for spore collection from anaerobic fungi: Application for RNA uptake and long-term storage of isolates
journal, August 2016


Large-scale protein identification using mass spectrometry
journal, March 2003

  • Lin, Dayin; Tabb, David L.; Yates, John R.
  • Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1646, Issue 1-2
  • DOI: 10.1016/S1570-9639(02)00546-0

Real-Time PCR Assays for Monitoring Anaerobic Fungal Biomass and Population Size in the Rumen
journal, December 2010

  • Lwin, Khin Ohnmar; Hayakawa, Mika; Ban-Tokuda, Tomomi
  • Current Microbiology, Vol. 62, Issue 4
  • DOI: 10.1007/s00284-010-9843-7

A cyclophilin from the polycentric anaerobic rumen fungus Orpinomyces sp. strain PC-2 is highly homologous to vertebrate cyclophilin B.
journal, March 1995

  • Chen, H.; Li, X. L.; Ljungdahl, L. G.
  • Proceedings of the National Academy of Sciences, Vol. 92, Issue 7
  • DOI: 10.1073/pnas.92.7.2587

Diversity of anaerobic gut fungal populations analysed using ribosomal ITS1 sequences in faeces of wild and domesticated herbivores
journal, April 2010


Efficient production of cellulolytic and xylanolytic enzymes by the rumen anaerobic fungus, Neocallimastix frontalis, in a repeated batch culture
journal, January 2001

  • Srinivasan, Karthikeyan; Murakami, Makoto; Nakashimada, Yutaka
  • Journal of Bioscience and Bioengineering, Vol. 91, Issue 2
  • DOI: 10.1016/S1389-1723(01)80058-X

Classical and molecular approaches as a powerful tool for the characterization of rumen polycentric fungi
journal, March 2004

  • Fliegerová, K.; Hodrová, B.; Voigt, K.
  • Folia Microbiologica, Vol. 49, Issue 2
  • DOI: 10.1007/BF02931392

Biochemical and Microbiological Evidence for Fermentative Digestion in Free‐Living Land Iguanas ( Conolophus pallidus ) and Marine Iguanas ( Amblyrhynchus cristatus ) on the Galápagos Archipelago
journal, January 2004

  • Mackie, Roderick I.; Rycyk, Mathew; Ruemmler, Rebecca L.
  • Physiological and Biochemical Zoology, Vol. 77, Issue 1
  • DOI: 10.1086/383498

Phylogeny of Oedogoniales, Chaetophorales and Chaetopeltidales (Chlorophyceae): inferences from sequence-structure analysis of ITS2
journal, October 2011

  • Buchheim, Mark A.; Sutherland, Danica M.; Schleicher, Tina
  • Annals of Botany, Vol. 109, Issue 1
  • DOI: 10.1093/aob/mcr275

Presence and transcriptional activity of anaerobic fungi in agricultural biogas plants
journal, July 2017


Anaerobic Fungi: A Potential Source of Biological H2 in the Oceanic Crust
journal, May 2016


Coastal marine habitats harbor novel early-diverging fungal diversity
journal, February 2017


FinisherSC: a repeat-aware tool for upgrading de novo assembly using long reads
journal, June 2015


Sugar and polysaccharide fermentation by rumen anaerobic fungi from Australia, Britain and New Zealand
journal, January 1988


Metatranscriptomic Profiling Reveals Linkages between the Active Rumen Microbiome and Feed Efficiency in Beef Cattle
journal, February 2017

  • Li, Fuyong; Guan, Le Luo
  • Applied and Environmental Microbiology, Vol. 83, Issue 9
  • DOI: 10.1128/AEM.00061-17

D1/D2 Domain of Large-Subunit Ribosomal DNA for Differentiation of Orpinomyces spp.
journal, July 2011

  • Dagar, Sumit S.; Kumar, Sanjay; Mudgil, Priti
  • Applied and Environmental Microbiology, Vol. 77, Issue 18
  • DOI: 10.1128/AEM.05441-11

Glucose metabolic pathways in the anaerobic rumen fungus Neocallimastix frontalis EB188
journal, March 1991

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  • Biochemical Journal, Vol. 274, Issue 2
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Transcriptomic analysis of lignocellulosic biomass degradation by the anaerobic fungal isolate Orpinomyces sp. strain C1A
journal, December 2015

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  • Biotechnology for Biofuels, Vol. 8, Issue 1
  • DOI: 10.1186/s13068-015-0390-0

Metabolomics technology and bioinformatics
journal, March 2006


Special Properties of Polycentric Anaerobic Fungus Anaeromyces mucronatus
journal, January 2002

  • Fliegerová, K.; Pažoutová, S.; Mrázek, J.
  • Acta Veterinaria Brno, Vol. 71, Issue 4
  • DOI: 10.2754/avb200271040441

Enhanced biogas yield from energy crops with rumen anaerobic fungi: Increase of biogas yield by rumen fungi
journal, June 2012

  • Procházka, Jindřich; Mrázek, Jakub; Štrosová, Lenka
  • Engineering in Life Sciences, Vol. 12, Issue 3
  • DOI: 10.1002/elsc.201100076

Analysis of Functional Genes in Carbohydrate Metabolic Pathway of Anaerobic Rumen Fungus Neocallimastix frontalis PMA02
journal, October 2009

  • Kwon, Mi; Song, Jaeyong; Ha, Jong K.
  • Asian-Australasian Journal of Animal Sciences, Vol. 22, Issue 11
  • DOI: 10.5713/ajas.2009.80371

Modification of a xylanase cDNA isolated from an anaerobic fungus Neocallimastix patriciarum for high-level expression in Escherichia coli
journal, January 1995


Metatranscriptomic Analyses of Plant Cell Wall Polysaccharide Degradation by Microorganisms in the Cow Rumen
journal, December 2014

  • Dai, Xin; Tian, Yan; Li, Jinting
  • Applied and Environmental Microbiology, Vol. 81, Issue 4
  • DOI: 10.1128/AEM.03682-14

Proteomic Challenges: Sample Preparation Techniques for Microgram-Quantity Protein Analysis from Biological Samples
journal, February 2015

  • Feist, Peter; Hummon, Amanda
  • International Journal of Molecular Sciences, Vol. 16, Issue 2
  • DOI: 10.3390/ijms16023537

ProfDistS: (profile-) distance based phylogeny on sequence--structure alignments
journal, August 2008


Widespread adenine N6-methylation of active genes in fungi
journal, May 2017

  • Mondo, Stephen J.; Dannebaum, Richard O.; Kuo, Rita C.
  • Nature Genetics, Vol. 49, Issue 6
  • DOI: 10.1038/ng.3859

Metagenomic Discovery of Biomass-Degrading Genes and Genomes from Cow Rumen
journal, January 2011


Microbial communities for bioprocessing: lessons learned from nature
journal, November 2016

  • Peng, Xuefeng “Nick”; Gilmore, Sean P.; O’Malley, Michelle A.
  • Current Opinion in Chemical Engineering, Vol. 14
  • DOI: 10.1016/j.coche.2016.09.003

Snapshot of the Eukaryotic Gene Expression in Muskoxen Rumen—A Metatranscriptomic Approach
journal, May 2011


Identification and characterization of anaerobic gut fungi using molecular methodologies based on ribosomal ITS1 and 18S rRNA
journal, February 2000