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Title: Fungi contribute critical but spatially varying roles in nitrogen and carbon cycling in acid mine drainage

Abstract

© 2016 Mosier, Miller, Frischkorn, Ohm, Li, LaButti, Lapidus, Lipzen, Chen, Johnson, Lindquist, Pan, Hettich, Grigoriev, Singer and Banfield. The ecosystem roles of fungi have been extensively studied by targeting one organism and/or biological process at a time, but the full metabolic potential of fungi has rarely been captured in an environmental context. We hypothesized that fungal genome sequences could be assembled directly from the environment using metagenomics and that transcriptomics and proteomics could simultaneously reveal metabolic differentiation across habitats. We reconstructed the near-complete 27 Mbp genome of a filamentous fungus, Acidomyces richmondensis, and evaluated transcript and protein expression in floating and streamer biofilms from an acid mine drainage (AMD) system. A. richmondensis transcripts involved in denitrification and in the degradation of complex carbon sources (including cellulose) were up-regulated in floating biofilms, whereas central carbon metabolism and stress-related transcripts were significantly up-regulated in streamer biofilms. These findings suggest that the biofilm niches are distinguished by distinct carbon and nitrogen resource utilization, oxygen availability, and environmental challenges. An isolated A. richmondensis strain from this environment was used to validate the metagenomics-derived genome and confirm nitrous oxide production at pH 1. Overall, our analyses defined mechanisms of fungal adaptation and identified amore » functional shift related to different roles in carbon and nitrogen turnover for the same species of fungi growing in closely located but distinct biofilm niches.« less

Authors:
 [1];  [1];  [1];  [2];  [3];  [2];  [2];  [2];  [2];  [2];  [2];  [3];  [3];  [2];  [4];  [1]
  1. Univ. of California, Berkeley, CA (United States)
  2. US Dept. of Energy Joint Genome Institute, Walnut Creek, CA (United States)
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  4. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1257271
Alternate Identifier(s):
OSTI ID: 1326500; OSTI ID: 1379136
Grant/Contract Number:  
FG02-10ER64996; SC0004918; AC02-05CH11231; AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; fungi; metagenomics; transcriptomics; proteomics; carbon; nitrogen; biofilm

Citation Formats

Mosier, Annika C., Miller, Christopher S., Frischkorn, Kyle R., Ohm, Robin A., Li, Zhou, LaButti, Kurt, Lapidus, Alla, Lipzen, Anna, Chen, Cindy, Johnson, Jenifer, Lindquist, Erika A., Pan, Chongle, Hettich, Robert L., Grigoriev, Igor V., Singer, Steven W., and Banfield, Jillian F. Fungi contribute critical but spatially varying roles in nitrogen and carbon cycling in acid mine drainage. United States: N. p., 2016. Web. doi:10.3389/fmicb.2016.00238.
Mosier, Annika C., Miller, Christopher S., Frischkorn, Kyle R., Ohm, Robin A., Li, Zhou, LaButti, Kurt, Lapidus, Alla, Lipzen, Anna, Chen, Cindy, Johnson, Jenifer, Lindquist, Erika A., Pan, Chongle, Hettich, Robert L., Grigoriev, Igor V., Singer, Steven W., & Banfield, Jillian F. Fungi contribute critical but spatially varying roles in nitrogen and carbon cycling in acid mine drainage. United States. https://doi.org/10.3389/fmicb.2016.00238
Mosier, Annika C., Miller, Christopher S., Frischkorn, Kyle R., Ohm, Robin A., Li, Zhou, LaButti, Kurt, Lapidus, Alla, Lipzen, Anna, Chen, Cindy, Johnson, Jenifer, Lindquist, Erika A., Pan, Chongle, Hettich, Robert L., Grigoriev, Igor V., Singer, Steven W., and Banfield, Jillian F. Thu . "Fungi contribute critical but spatially varying roles in nitrogen and carbon cycling in acid mine drainage". United States. https://doi.org/10.3389/fmicb.2016.00238. https://www.osti.gov/servlets/purl/1257271.
@article{osti_1257271,
title = {Fungi contribute critical but spatially varying roles in nitrogen and carbon cycling in acid mine drainage},
author = {Mosier, Annika C. and Miller, Christopher S. and Frischkorn, Kyle R. and Ohm, Robin A. and Li, Zhou and LaButti, Kurt and Lapidus, Alla and Lipzen, Anna and Chen, Cindy and Johnson, Jenifer and Lindquist, Erika A. and Pan, Chongle and Hettich, Robert L. and Grigoriev, Igor V. and Singer, Steven W. and Banfield, Jillian F.},
abstractNote = {© 2016 Mosier, Miller, Frischkorn, Ohm, Li, LaButti, Lapidus, Lipzen, Chen, Johnson, Lindquist, Pan, Hettich, Grigoriev, Singer and Banfield. The ecosystem roles of fungi have been extensively studied by targeting one organism and/or biological process at a time, but the full metabolic potential of fungi has rarely been captured in an environmental context. We hypothesized that fungal genome sequences could be assembled directly from the environment using metagenomics and that transcriptomics and proteomics could simultaneously reveal metabolic differentiation across habitats. We reconstructed the near-complete 27 Mbp genome of a filamentous fungus, Acidomyces richmondensis, and evaluated transcript and protein expression in floating and streamer biofilms from an acid mine drainage (AMD) system. A. richmondensis transcripts involved in denitrification and in the degradation of complex carbon sources (including cellulose) were up-regulated in floating biofilms, whereas central carbon metabolism and stress-related transcripts were significantly up-regulated in streamer biofilms. These findings suggest that the biofilm niches are distinguished by distinct carbon and nitrogen resource utilization, oxygen availability, and environmental challenges. An isolated A. richmondensis strain from this environment was used to validate the metagenomics-derived genome and confirm nitrous oxide production at pH 1. Overall, our analyses defined mechanisms of fungal adaptation and identified a functional shift related to different roles in carbon and nitrogen turnover for the same species of fungi growing in closely located but distinct biofilm niches.},
doi = {10.3389/fmicb.2016.00238},
journal = {Frontiers in Microbiology},
number = ,
volume = 7,
place = {United States},
year = {Thu Mar 03 00:00:00 EST 2016},
month = {Thu Mar 03 00:00:00 EST 2016}
}

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Works referenced in this record:

Dual isotope and isotopomer signatures of nitrous oxide from fungal denitrification - a pure culture study: Isotopomer signatures of N
journal, August 2014

  • Rohe, Lena; Anderson, Traute-Heidi; Braker, Gesche
  • Rapid Communications in Mass Spectrometry, Vol. 28, Issue 17
  • DOI: 10.1002/rcm.6975

Aerobic denitrification: a controversy revived
journal, November 1984

  • Robertson, Lesley A.; Kuenen, J. Gijs
  • Archives of Microbiology, Vol. 139, Issue 4
  • DOI: 10.1007/BF00408378

Exhaustive database searching for amino acid mutations in proteomes
journal, May 2012


Quantitative Proteomic Analysis of the Heat Stress Response in Clostridium difficile Strain 630
journal, September 2011

  • Jain, Shailesh; Graham, Ciaren; Graham, Robert L. J.
  • Journal of Proteome Research, Vol. 10, Issue 9
  • DOI: 10.1021/pr200327t

Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization
journal, August 2012

  • Sharon, I.; Morowitz, M. J.; Thomas, B. C.
  • Genome Research, Vol. 23, Issue 1
  • DOI: 10.1101/gr.142315.112

A new acidophilic fungus Teratosphaeria acidotherma (Capnodiales, Ascomycota) from a hot spring
journal, November 2010


Fast and accurate short read alignment with Burrows-Wheeler transform
journal, May 2009


Arsenic toxicity in mammals and aquatic animals: A comparative biochemical approach
journal, March 2011

  • Ventura-Lima, Juliane; Bogo, Maurício Reis; Monserrat, José M.
  • Ecotoxicology and Environmental Safety, Vol. 74, Issue 3
  • DOI: 10.1016/j.ecoenv.2010.11.002

Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla
journal, September 2012


Ultrafast and memory-efficient alignment of short DNA sequences to the human genome
journal, January 2009


Comparison of environmental and isolate Sulfobacillus genomes reveals diverse carbon, sulfur, nitrogen, and hydrogen metabolisms
journal, January 2014


Community-wide analysis of microbial genome sequence signatures
journal, January 2009

  • Dick, Gregory J.; Andersson, Anders F.; Baker, Brett J.
  • Genome Biology, Vol. 10, Issue 8
  • DOI: 10.1186/gb-2009-10-8-r85

Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
journal, September 1997

  • Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A.
  • Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402
  • DOI: 10.1093/nar/25.17.3389

Diversity of fungal communities in saline and acidic soils in the Soos National Natural Reserve, Czech Republic
journal, September 2009

  • Hujslová, Martina; Kubátová, Alena; Chudíčková, Milada
  • Mycological Progress, Vol. 9, Issue 1
  • DOI: 10.1007/s11557-009-0611-7

FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010


Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments
journal, August 2004


InterPro: the integrative protein signature database
journal, January 2009

  • Hunter, S.; Apweiler, R.; Attwood, T. K.
  • Nucleic Acids Research, Vol. 37, Issue Database
  • DOI: 10.1093/nar/gkn785

Improvement of Phylogenies after Removing Divergent and Ambiguously Aligned Blocks from Protein Sequence Alignments
journal, August 2007


The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics
journal, January 2009

  • Cantarel, B. L.; Coutinho, P. M.; Rancurel, C.
  • Nucleic Acids Research, Vol. 37, Issue Database
  • DOI: 10.1093/nar/gkn663

ProRata:  A Quantitative Proteomics Program for Accurate Protein Abundance Ratio Estimation with Confidence Interval Evaluation
journal, October 2006

  • Pan, Chongle; Kora, Guruprasad; McDonald, W. Hayes
  • Analytical Chemistry, Vol. 78, Issue 20
  • DOI: 10.1021/ac060654b

MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability
journal, January 2013

  • Katoh, K.; Standley, D. M.
  • Molecular Biology and Evolution, Vol. 30, Issue 4
  • DOI: 10.1093/molbev/mst010

TM4: A Free, Open-Source System for Microarray Data Management and Analysis
journal, February 2003

  • Saeed, A. I.; Sharov, V.; White, J.
  • BioTechniques, Vol. 34, Issue 2
  • DOI: 10.2144/03342mt01

Interactions of Sodium Selenite, Glutathione, Arsenic Species, and Omega Class Human Glutathione Transferase
journal, August 2005

  • Zakharyan, Robert A.; Tsaprailis, George; Chowdhury, Uttam K.
  • Chemical Research in Toxicology, Vol. 18, Issue 8
  • DOI: 10.1021/tx0500530

Single-Cell Genomics Reveals Organismal Interactions in Uncultivated Marine Protists
journal, May 2011


Universal sample preparation method for proteome analysis
journal, April 2009

  • Wiśniewski, Jacek R.; Zougman, Alexandre; Nagaraj, Nagarjuna
  • Nature Methods, Vol. 6, Issue 5
  • DOI: 10.1038/nmeth.1322

The carbohydrate-active enzymes database (CAZy) in 2013
journal, November 2013

  • Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1178

Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes
journal, May 2013

  • Albertsen, Mads; Hugenholtz, Philip; Skarshewski, Adam
  • Nature Biotechnology, Vol. 31, Issue 6
  • DOI: 10.1038/nbt.2579

Untangling Genomes from Metagenomes: Revealing an Uncultured Class of Marine Euryarchaeota
journal, February 2012


Microbial communities in acid mine drainage
journal, May 2003


Large-scale analysis of the yeast proteome by multidimensional protein identification technology
journal, March 2001

  • Washburn, Michael P.; Wolters, Dirk; Yates, John R.
  • Nature Biotechnology, Vol. 19, Issue 3
  • DOI: 10.1038/85686

Drought meets acid: three new genera in a dothidealean clade of extremotolerant fungi
journal, January 2008


Basic local alignment search tool
journal, October 1990

  • Altschul, Stephen F.; Gish, Warren; Miller, Webb
  • Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
  • DOI: 10.1016/S0022-2836(05)80360-2

Ammonia Fermentation, a Novel Anoxic Metabolism of Nitrate by Fungi
journal, November 2001

  • Zhou, Zhemin; Takaya, Naoki; Nakamura, Akira
  • Journal of Biological Chemistry, Vol. 277, Issue 3
  • DOI: 10.1074/jbc.M109096200

Acidiella bohemica gen. et sp. nov. and Acidomyces spp. (Teratosphaeriaceae), the indigenous inhabitants of extremely acidic soils in Europe
journal, October 2012

  • Hujslová, Martina; Kubátová, Alena; Kostovčík, Martin
  • Fungal Diversity, Vol. 58, Issue 1
  • DOI: 10.1007/s13225-012-0176-7

Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi
journal, March 2012

  • Schoch, C. L.; Seifert, K. A.; Huhndorf, S.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 16
  • DOI: 10.1073/pnas.1117018109

Associating Growth-Phase-Related Changes in the Proteome of Acinetobacter baumannii with Increased Resistance to Oxidative Stress
journal, April 2010

  • Soares, Nelson C.; Cabral, Maria P.; Gayoso, Carmen
  • Journal of Proteome Research, Vol. 9, Issue 4
  • DOI: 10.1021/pr901116r

The Pfam protein families database
journal, November 2011

  • Punta, M.; Coggill, P. C.; Eberhardt, R. Y.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr1065

An efficient algorithm for large-scale detection of protein families
journal, April 2002


ABA-Regulated G Protein Signaling in Arabidopsis Guard Cells: A Proteomic Perspective
journal, April 2010

  • Zhao, Zhixin; Stanley, Bruce A.; Zhang, Wei
  • Journal of Proteome Research, Vol. 9, Issue 4
  • DOI: 10.1021/pr901011h

Exoproteome of Staphylococcus aureus Reveals Putative Determinants of Nasal Carriage
journal, April 2011

  • Muthukrishnan, Gowrishankar; Quinn, Gerry A.; Lamers, Ryan P.
  • Journal of Proteome Research, Vol. 10, Issue 4
  • DOI: 10.1021/pr200029r

A Genomic Perspective on Protein Families
journal, October 1997


MycoCosm portal: gearing up for 1000 fungal genomes
journal, December 2013

  • Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1183

Denitrifier abundance and activity across the San Francisco Bay estuary: Estuarine denitrifier abundance and activity
journal, April 2010


Extraordinary phylogenetic diversity and metabolic versatility in aquifer sediment
journal, August 2013

  • Castelle, Cindy J.; Hug, Laura A.; Wrighton, Kelly C.
  • Nature Communications, Vol. 4, Issue 1
  • DOI: 10.1038/ncomms3120

AMD biofilms: using model communities to study microbial evolution and ecological complexity in nature
journal, February 2010

  • Denef, Vincent J.; Mueller, Ryan S.; Banfield, Jillian F.
  • The ISME Journal, Vol. 4, Issue 5
  • DOI: 10.1038/ismej.2009.158

Metabolically Active Eukaryotic Communities in Extremely Acidic Mine Drainage
journal, October 2004


One Bacterial Cell, One Complete Genome
journal, April 2010


Watershed-Scale Fungal Community Characterization along a pH Gradient in a Subsurface Environment Cocontaminated with Uranium and Nitrate
journal, January 2014

  • Jasrotia, Puja; Green, Stefan J.; Canion, Andy
  • Applied and Environmental Microbiology, Vol. 80, Issue 6
  • DOI: 10.1128/AEM.03423-13

Quantitative proteomic analyses of the response of acidophilic microbial communities to different pH conditions
journal, January 2011

  • Belnap, Christopher P.; Pan, Chongle; Denef, Vincent J.
  • The ISME Journal, Vol. 5, Issue 7
  • DOI: 10.1038/ismej.2010.200

Diauxic Growth of Fusarium oxysporum during Aerobic Culture in the Presence of Nitrate/Nitrite
journal, January 1992

  • Tanimoto, Tatsuo; Nakahara, Kazuhiko; Shoun, Hirofumi
  • Bioscience, Biotechnology, and Biochemistry, Vol. 56, Issue 12
  • DOI: 10.1271/bbb.56.2058

KEGG for linking genomes to life and the environment
journal, December 2007

  • Kanehisa, M.; Araki, M.; Goto, S.
  • Nucleic Acids Research, Vol. 36, Issue Database
  • DOI: 10.1093/nar/gkm882

Sipros/ProRata: a versatile informatics system for quantitative community proteomics
journal, June 2013


A novel highly acidic β-mannanase from the acidophilic fungus Bispora sp. MEY-1: gene cloning and overexpression in Pichia pastoris
journal, November 2008

  • Luo, Huiying; Wang, Yaru; Wang, Hui
  • Applied Microbiology and Biotechnology, Vol. 82, Issue 3
  • DOI: 10.1007/s00253-008-1766-x

Quantitative Proteomics Analysis Demonstrates Post-transcriptional Regulation of Embryonic Stem Cell Differentiation to Hematopoiesis
journal, November 2007

  • Williamson, Andrew J. K.; Smith, Duncan L.; Blinco, David
  • Molecular & Cellular Proteomics, Vol. 7, Issue 3
  • DOI: 10.1074/mcp.M700370-MCP200

Ecological distribution and population physiology defined by proteomics in a natural microbial community
journal, January 2010

  • Mueller, Ryan S.; Denef, Vincent J.; Kalnejais, Linda H.
  • Molecular Systems Biology, Vol. 6, Issue 1
  • DOI: 10.1038/msb.2010.30

Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles
journal, September 2005

  • Subramanian, A.; Tamayo, P.; Mootha, V. K.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 43, p. 15545-15550
  • DOI: 10.1073/pnas.0506580102

Gene Ontology: tool for the unification of biology
journal, May 2000

  • Ashburner, Michael; Ball, Catherine A.; Blake, Judith A.
  • Nature Genetics, Vol. 25, Issue 1
  • DOI: 10.1038/75556

Targeted metagenomics and ecology of globally important uncultured eukaryotic phytoplankton
journal, July 2010

  • Cuvelier, M. L.; Allen, A. E.; Monier, A.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 33
  • DOI: 10.1073/pnas.1001665107

The Genome Portal of the Department of Energy Joint Genome Institute
journal, November 2011

  • Grigoriev, I. V.; Nordberg, H.; Shabalov, I.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr947

Detection of Differential Proteomes Associated with the Development of Type 2 Diabetes in the Zucker Rat Model Using the iTRAQ Technique
journal, February 2011

  • Han, Dohyun; Moon, Sungyoon; Kim, Hyunsoo
  • Journal of Proteome Research, Vol. 10, Issue 2
  • DOI: 10.1021/pr100759a

Elevated temperature alters proteomic responses of individual organisms within a biofilm community
journal, July 2014


Acid mine drainage biogeochemistry at Iron Mountain, California
journal, June 2004

  • Druschel, Gregory K.; Baker, Brett J.; Gihring, Thomas M.
  • Geochemical Transactions, Vol. 5, Issue 2
  • DOI: 10.1186/1467-4866-5-13

Direct Cellular Lysis/Protein Extraction Protocol for Soil Metaproteomics
journal, December 2010

  • Chourey, Karuna; Jansson, Janet; VerBerkmoes, Nathan
  • Journal of Proteome Research, Vol. 9, Issue 12
  • DOI: 10.1021/pr100787q

Velvet: Algorithms for de novo short read assembly using de Bruijn graphs
journal, February 2008


Oxygen requirement for denitrification by the fungus Fusarium oxysporum
journal, January 2001

  • Zhou, Zhemin; Takaya, Naoki; Sakairi, Maria Antonina C.
  • Archives of Microbiology, Vol. 175, Issue 1
  • DOI: 10.1007/s002030000231

Diversity of Nitrite Reductase (nirK and nirS) Gene Fragments in Forested Upland and Wetland Soils
journal, April 2002


Assessing the gene space in draft genomes
journal, November 2008

  • Parra, Genis; Bradnam, Keith; Ning, Zemin
  • Nucleic Acids Research, Vol. 37, Issue 1
  • DOI: 10.1093/nar/gkn916

Comparative genomics in acid mine drainage biofilm communities reveals metabolic and structural differentiation of co-occurring archaea
journal, January 2013

  • Yelton, Alexis P.; Comolli, Luis R.; Justice, Nicholas B.
  • BMC Genomics, Vol. 14, Issue 1
  • DOI: 10.1186/1471-2164-14-485

2016 update of the PRIDE database and its related tools
journal, November 2015

  • Vizcaíno, Juan Antonio; Csordas, Attila; del-Toro, Noemi
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1145

Heterotrophic Archaea Contribute to Carbon Cycling in Low-pH, Suboxic Biofilm Communities
journal, September 2012

  • Justice, Nicholas B.; Pan, Chongle; Mueller, Ryan
  • Applied and Environmental Microbiology, Vol. 78, Issue 23
  • DOI: 10.1128/AEM.01938-12

A new Generation of Homology Search Tools Based on Probabilistic Inference
conference, March 2012


Genomes from Metagenomics
journal, November 2013


Fungal denitrification and nitric oxide reductase cytochrome P450nor
journal, May 2012

  • Shoun, Hirofumi; Fushinobu, Shinya; Jiang, Li
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 367, Issue 1593
  • DOI: 10.1098/rstb.2011.0335

De Novo Assembly of the Pneumocystis jirovecii Genome from a Single Bronchoalveolar Lavage Fluid Specimen from a Patient
journal, December 2012


Metagenomes of the Picoalga Bathycoccus from the Chile Coastal Upwelling
journal, June 2012


Characterization of Extracellular Polymeric Substances from Acidophilic Microbial Biofilms
journal, March 2010

  • Jiao, Y.; Cody, G. D.; Harding, A. K.
  • Applied and Environmental Microbiology, Vol. 76, Issue 9
  • DOI: 10.1128/AEM.02289-09

Denitrification Across Landscapes and Waterscapes: a Synthesis
journal, December 2006


Diverse Lifestyles and Strategies of Plant Pathogenesis Encoded in the Genomes of Eighteen Dothideomycetes Fungi
journal, December 2012


A new acidophilic Scytalidium
journal, February 1974

  • Sigler, Lynne; Carmichael, J. W.
  • Canadian Journal of Microbiology, Vol. 20, Issue 2
  • DOI: 10.1139/m74-043

The COG database: an updated version includes eukaryotes
journal, January 2003

  • Tatusov, Roman L.; Fedorova, Natalie D.; Jackson, John D.
  • BMC Bioinformatics, Vol. 4, Article No. 41
  • DOI: 10.1186/1471-2105-4-41

Fungal oxygen exchange between denitrification intermediates and water: Fungal oxygen exchange during denitrification
journal, December 2013

  • Rohe, Lena; Anderson, Traute-Heidi; Braker, Gesche
  • Rapid Communications in Mass Spectrometry, Vol. 28, Issue 4
  • DOI: 10.1002/rcm.6790

Quantification of denitrifying bacteria in soils by nirK gene targeted real-time PCR
journal, December 2004

  • Henry, Sonia; Baudoin, Ezékiel; López-Gutiérrez, Juan C.
  • Journal of Microbiological Methods, Vol. 59, Issue 3
  • DOI: 10.1016/j.mimet.2004.07.002

Phylogenetic identification and in situ detection of individual microbial cells without cultivation.
journal, January 1995


2016 update of the PRIDE database and its related tools
journal, September 2016

  • Vizcaíno, Juan Antonio; Csordas, Attila; del-Toro, Noemi
  • Nucleic Acids Research, Vol. 44, Issue 22
  • DOI: 10.1093/nar/gkw880

Works referencing / citing this record:

Fungi in Biofilms of Highly Acidic Soils
book, July 2019

  • Hujslová, Martina; Gryndler, Milan
  • Fungi in Extreme Environments: Ecological Role and Biotechnological Significance
  • DOI: 10.1007/978-3-030-19030-9_11

Acidomyces acidophilus: Ecology, Biochemical Properties and Application to Bioremediation
book, July 2019

  • Chan, Wai Kit; Wildeboer, Dirk; Garelick, Hemda
  • Fungi in Extreme Environments: Ecological Role and Biotechnological Significance, p. 505-515
  • DOI: 10.1007/978-3-030-19030-9_25

Community Composition of Nitrite Reductase Gene Sequences in an Acid Mine Drainage Environment
journal, August 2019


Interactions among microfungi and pyrite-chalcopyrite mineralizations: tolerance, mineral bioleaching, and metal bioaccumulation
journal, March 2019


The genome of opportunistic fungal pathogen Fusarium oxysporum carries a unique set of lineage-specific chromosomes
journal, January 2020


Genome Sequence of the Extremely Acidophilic Fungus Acidomyces richmondensis FRIK2901
journal, October 2018

  • Rosienski, Matthew D.; Lee, Mi-Kyung; Yu, Jae-Hyuk
  • Microbiology Resource Announcements, Vol. 7, Issue 16
  • DOI: 10.1128/mra.01314-18

New insights on unspecific peroxygenases: superfamily reclassification and evolution
journal, March 2019


Genome-scale data resolve ancestral rock-inhabiting lifestyle in Dothideomycetes (Ascomycota)
journal, October 2019


Hiding in plain sight: New virus genomes discovered via a systematic analysis of fungal public transcriptomes
journal, July 2019


Comparative Genomics Unravels the Functional Roles of Co-occurring Acidophilic Bacteria in Bioleaching Heaps
journal, May 2017