The Missing Fungi: New Insights from Culture-Independent Molecular Studies of Soil

Molecular surveys of soil fungi have received much less attention despite the fact that fungi dominate decomposition and nutrient cycles in many soils. The ability to sequence fungal DNA from soil samples has opened up a new realm of possibilities for identifying new fungal groups. A clone library approximates a random sample of fungi in the soil, and is likely to be biased toward some groups of fungi over others based on variables in each step of the procedure used. The Assembling the Fungal Tree of Life (AFTOL) initiative has definitively clarified the phylogenetic tree for all known fungi. Three rDNA regions are commonly used to identify fungi: the 18S small subunit (SSU); the internal transcriber spacer sequences ITS-1 and ITS-2; and the 28S large subunit (LSU). This chapter reviews the new fungal lineages that have been discovered in various soil libraries over the past 10 years. Most soil libraries to date have discovered new fungi only at the genus or species level. The chapter talks about two main discoveries, Chytridiomycota and Ascomycota, after reviewing other important but unrelated clades that have also been discovered in soil libraries. It is important to flesh out the fungal family tree as quickly as possible, as it is possible that many of the missing fungi can go extinct before it is known that they ever existed.

[1]  S. K. Schmidt,et al.  Phylogeny and Ecophysiology of Opportunistic “Snow Molds” from a Subalpine Forest Ecosystem , 2008, Microbial Ecology.

[2]  Andrew P. Martin,et al.  Widespread occurrence and phylogenetic placement of a soil clone group adds a prominent new branch to the fungal tree of life. , 2008, Molecular phylogenetics and evolution.

[3]  S. Reed,et al.  Biogeochemical consequences of rapid microbial turnover and seasonal succession in soil. , 2007, Ecology.

[4]  James Long,et al.  TOPO TA is A-OK: a test of phylogenetic bias in fungal environmental clone library construction. , 2007, Environmental microbiology.

[5]  Kenji Matsuura,et al.  Reconstructing the early evolution of Fungi using a six-gene phylogeny , 2006, Nature.

[6]  M. Lynch,et al.  Diversity of Basidiomycetes in Michigan Agricultural Soils , 2006, Applied and Environmental Microbiology.

[7]  A. J. Jones,et al.  New Screening Software Shows that Most Recent Large 16S rRNA Gene Clone Libraries Contain Chimeras , 2006, Applied and Environmental Microbiology.

[8]  Jo Handelsman,et al.  Toward a Census of Bacteria in Soil , 2006, PLoS Comput. Biol..

[9]  D. Hopkins,et al.  Fungal diversity in maritime Antarctic soils determined using a combination of culture isolation, molecular fingerprinting and cloning techniques , 2006, Polar Biology.

[10]  P. Janssen.  Identifying the Dominant Soil Bacterial Taxa in Libraries of 16S rRNA and 16S rRNA Genes , 2006, Applied and Environmental Microbiology.

[11]  R. Monson,et al.  Winter forest soil respiration controlled by climate and microbial community composition , 2006, Nature.

[12]  Vanja Klepac-Ceraj,et al.  PCR-Induced Sequence Artifacts and Bias: Insights from Comparison of Two 16S rRNA Clone Libraries Constructed from the Same Sample , 2005, Applied and Environmental Microbiology.

[13]  A. J. Jones,et al.  At Least 1 in 20 16S rRNA Sequence Records Currently Held in Public Repositories Is Estimated To Contain Substantial Anomalies , 2005, Applied and Environmental Microbiology.

[14]  John R Spear,et al.  Phylogenetic diversity and ecology of environmental Archaea. , 2005, Current opinion in microbiology.

[15]  A. Jumpponen,et al.  Can rDNA analyses of diverse fungal communities in soil and roots detect effects of environmental manipulations—a case study from tallgrass prairie , 2005, Mycologia.

[16]  Andrew F. S. Taylor,et al.  Fungal communities in mycorrhizal roots of conifer seedlings in forest nurseries under different cultivation systems, assessed by morphotyping, direct sequencing and mycelial isolation , 2005, Mycorrhiza.

[17]  Rytas Vilgalys,et al.  Fungal Community Analysis by Large-Scale Sequencing of Environmental Samples , 2005, Applied and Environmental Microbiology.

[18]  J. Longcore.  Zoosporic fungi from Australian and New Zealand tree-canopy detritus , 2005 .

[19]  Ji‐Zheng He,et al.  Analyses of soil fungal communities in adjacent natural forest and hoop pine plantation ecosystems of subtropical Australia using molecular approaches based on 18S rRNA genes. , 2005, FEMS microbiology letters.

[20]  T. Bruns,et al.  Detection of plot-level changes in ectomycorrhizal communities across years in an old-growth mixed-conifer forest. , 2005, The New phytologist.

[21]  J. Bergsten.  A review of long‐branch attraction , 2005, Cladistics : the international journal of the Willi Hennig Society.

[22]  Yukio Magariyama,et al.  Reevaluation and Reduction of a PCR Bias Caused by Reannealing of Templates , 2004, Applied and Environmental Microbiology.

[23]  D. Hibbett,et al.  Assembling the fungal tree of life: progress, classification, and evolution of subcellular traits. , 2004, American journal of botany.

[24]  Thomas Huber,et al.  Bellerophon: a program to detect chimeric sequences in multiple sequence alignments , 2004, Bioinform..

[25]  T. Cavalier-smith.  Only six kingdoms of life , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[26]  C. Berney,et al.  How many novel eukaryotic 'kingdoms'? Pitfalls and limitations of environmental DNA surveys , 2004, BMC Biology.

[27]  B. Hall,et al.  Body plan evolution of ascomycetes, as inferred from an RNA polymerase II phylogeny. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[28]  S. Giovannoni,et al.  The uncultured microbial majority. , 2003, Annual review of microbiology.

[29]  J. Prosser,et al.  Diversity of fungi in organic soils under a moorland--Scots pine (Pinus sylvestris L.) gradient. , 2003, Environmental microbiology.

[30]  P. Bridge,et al.  On the unreliability of published DNA sequences. , 2003, The New phytologist.

[31]  Rytas Vilgalys,et al.  Taxonomic misidentification in public DNA databases. , 2003, The New phytologist.

[32]  Christopher W. Schadt,et al.  Seasonal Dynamics of Previously Unknown Fungal Lineages in Tundra Soils , 2003, Science.

[33]  T. Kuyper,et al.  Vertical distribution of ectomycorrhizal fungal taxa in a podzol soil profile. , 2003, The New phytologist.

[34]  O. Eriksson,et al.  Morphology and ultrastructure of Neolecta species. , 2003, Mycological research.

[35]  B F Lang,et al.  Evolution of monoblepharidalean fungi based on complete mitochondrial genome sequences. , 2003, Nucleic acids research.

[36]  T. Kuyper,et al.  Molecular Identification of Ectomycorrhizal Mycelium in Soil Horizons , 2003, Applied and Environmental Microbiology.

[37]  T. Lueders,et al.  Evaluation of PCR Amplification Bias by Terminal Restriction Fragment Length Polymorphism Analysis of Small-Subunit rRNA and mcrA Genes by Using Defined Template Mixtures of Methanogenic Pure Cultures and Soil DNA Extracts , 2003, Applied and Environmental Microbiology.

[38]  N. Pace,et al.  Novel kingdom-level eukaryotic diversity in anoxic environments , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[39]  J. Cairney,et al.  Investigation of the influence of prescribed burning on ITS profiles of ectomycorrhizal and other soil fungi at three Australian sclerophyll forest sites , 2002 .

[40]  C. Leyval,et al.  Extensive fungal diversity in plant roots. , 2002, Science.

[41]  C. Schadt,et al.  Changes in Soil Microbial Community Structure and Function in an Alpine Dry Meadow Following Spring Snow Melt , 2002, Microbial Ecology.

[42]  Daniel Schwarzott,et al.  A new fungal phylum, the Glomeromycota: phylogeny and evolution * * Dedicated to Manfred Kluge (Tech , 2001 .

[43]  D. Hawksworth.  The magnitude of fungal diversity: the 1.5 million species estimate revisited * * Paper presented at , 2001 .

[44]  M. Fukui,et al.  Optimization of Annealing Temperature To Reduce Bias Caused by a Primer Mismatch in Multitemplate PCR , 2001, Applied and Environmental Microbiology.

[45]  V. Huss,et al.  Hyaloraphidium curvatum is not a green alga, but a lower fungus; Amoebidium parasiticum is not a fungus, but a member of the DRIPs. , 2000, Protist.

[46]  P. Coley,et al.  Are tropical fungal endophytes hyperdiverse , 2000 .

[47]  Timothy Y. James,et al.  Molecular phylogenetics of the Chytridiomycota supports the utility of ultrastructural data in chytrid systematics , 2000 .

[48]  J. Moncalvo,et al.  High levels of variation in ribosomal DNA sequences within and among spores of a natural population of the arbuscular mycorrhizal fungus Acaulospora colossica , 2000 .

[49]  V. Ramisse,et al.  Quantification of Bias Related to the Extraction of DNA Directly from Soils , 1999, Applied and Environmental Microbiology.

[50]  K. Hyde,et al.  Biodiversity of palm fungi in the tropics: are global fungal diversity estimates realistic? , 1999, Biodiversity & Conservation.

[51]  M. Girlanda,et al.  Psychrooligotrophic fungi from Arctic soils of Franz Joseph Land , 1999, Polar Biology.

[52]  Martin F. Polz,et al.  Bias in Template-to-Product Ratios in Multitemplate PCR , 1998, Applied and Environmental Microbiology.

[53]  U. Göbel,et al.  Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. , 1997, FEMS microbiology reviews.

[54]  A. Cozijnsen,et al.  Organisation of ribosomal DNA in the ascomycete Leptosphaeria maculans. , 1997, Microbiological research.

[55]  M. Blackwell,et al.  Taxonomic diversity and interactions of insect-associated ascomycetes , 1997, Biodiversity & Conservation.

[56]  P. Brooks,et al.  Winter production of CO2 and N2O from alpine tundra: environmental controls and relationship to inter-system C and N fluxes , 1997, Oecologia.

[57]  D. Wynn-Williams.  Antarctic microbial diversity: the basis of polar ecosystem processes , 1996, Biodiversity & Conservation.

[58]  T. Bruns,et al.  Community structure of ectomycorrhizal fungi in a Pinus muricata forest: above- and below-ground views , 1996 .

[59]  H. Nishida,et al.  Archiascomycetes: detection of a major new lineage within the Ascomycota , 1994 .

[60]  J. Palmer,et al.  Animals and fungi are each other's closest relatives: congruent evidence from multiple proteins. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[61]  D. Simmons.  Systematics of the Lobulomycetales, a New Order within the Chytridiomycota , 2007 .

[62]  G. S. Hoog,et al.  Fungi of the Antarctic: Evolution under extreme conditions , 2005 .

[63]  James R. Cole,et al.  The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy , 2003, Nucleic Acids Res..

[64]  J. Prosser,et al.  Potential bias of fungal 18S rDNA and internal transcribed spacer polymerase chain reaction primers for estimating fungal biodiversity in soil. , 2003, Environmental microbiology.

[65]  Thomas Huber,et al.  Chimeric 16S rDNA sequences of diverse origin are accumulating in the public databases. , 2003, International journal of systematic and evolutionary microbiology.