Fungi in the Built Environment is a document that discusses the following in 3 sentences: 1) Fungi are diverse and found in many forms and ecosystems, including pathogens of plants and animals as well as mutualistic partners of plants and algae. 2) The number of known fungal species is around 69,000 but the estimated total number of fungal species worldwide is 1.5 million, highlighting the vast diversity still left to discover. 3) Advances in fungal genomics through projects like the 1000 Fungal Genomes Project are helping to address phylogenetic diversity and discover previously unknown fungi through sequencing hundreds of fungal genomes.

1. Fungi in the Built Environment
Jason Stajich
University of California, Riverside
http://fungidb.org @hyphaltip @fungalgenomes @fungidb http://lab.stajich.org

2. Fungal diversity of forms, functions, ecosystems
Cryptococcus neoformans X. Lin Coprinopsis cinerea Ellison & Stajich Aspergillus niger. N Read Glomus sp. Univ Sydney Rozella allomycis. James et al
Puccinia graminis J. F. Hennen Laccaria bicolor Martin et al. Neurospora crassa. Hickey & Reed Phycomyces blakesleansus T. Ootaki Batrachochytrium dendrobatidis
J. Longcore
Ustilago maydis Kai Hirdes Amanita phalloides. M Wood Xanthoria elegans. Botany POtD Rhizopus stolonifera. Blastocladiella simplex Stajich & Taylor

3. Plantae
Amoebozoa
Choanozoa
Metazoa
Microsporidia Fungi
Rozella
Chytridiomycota
Blastocladiomycota
Multicellular with
Mucoromycotina
differentiated tissues
Entomophthoromycotina
Zoopagomycotina
Loss of flagellum
Kickxellomycotina
Glomeromycota
Mitotic sporangia Pucciniomycotina Basidiomycota
to mitotic conidia Ustilaginomycotina
Regular septa Agaricomycotina
Taphrinomycotina Ascomycota
Meiotic sporangia to Saccharomycotina
external meiospores
Pezizomycotina
1500 1000 500 0
Millions of years Stajich et al. Current Biol 2009

4. Fungi interact with many organisms
10.3389/fpls.2011.00100
Betsy Arnold doi: 10.3389/fpls.2011.00100
Endophytes
Mycorrhiza doi: 10.1016/j.pbi.2009.05.007,
F. Martin

5. Organisms interacting with Fungi - fungi as the host
REPORTS
to the Midwest Regional Center of Excellence for was supported by the NIH Institutional NRSA T32 SOM Text
Biodefense and Emerging Infectious Disease Research GM07067 to the Washington University School of Figs. S1 to S4
(MRCE) and by NIH grant AI53298. The DDRCC is Medicine. Tables S1 and S2
supported by NIH grant DK52574. W.W.L. was supported References
Supporting Online Material
Plant + Fungus + Mycovirus
by the Clinical/Translational Fellowship Program of the
MRCE, the W.M. Keck Foundation, and the NIH National www.sciencemag.org/cgi/content/full/315/5811/509/DC1 6 November 2006; accepted 14 December 2006
Research Service Award (NRSA) F32 AI069688-01. P.A.P. Materials and Methods 10.1126/science.1137195
A Virus in a Fungus in a Plant:
S2). The 2.2-kb fragment (RNA 1) is involved in
virus replication, as both of its ORFs are similar
to viral replicases. The first, ORF1a, has 29%
Three-Way Symbiosis Required for amino acid sequence identity with a putative
RNA-dependent RNA polymerase (RdRp) from
Thermal Tolerance the rabbit hemorrhagic disease virus. The amino
acid sequence of the second, ORF1b, has 33%
identity with the RdRp of a virus of the fungal
Luis M. Márquez,1 Regina S. Redman,2,3 Russell J. Rodriguez,2,4 Marilyn J. Roossinck1* pathogen Discula destructiva. These two ORFs
overlap and could be expressed as a single
DOI: 10.1126/science.1136237
Downloaded from www.sciencemag.org on September 18, 2012
A mutualistic association between a fungal endophyte and a tropical panic grass allows both protein by frameshifting, a common expression
organisms to grow at high soil temperatures. We characterized a virus from this fungus that is strategy of viral replicases. The two ORFs of
involved in the mutualistic interaction. Fungal isolates cured of the virus are unable to confer RNA 2 have no similarity to any protein with
heat tolerance, but heat tolerance is restored after the virus is reintroduced. The virus-infected known function. As in most dsRNA mycovi-
fungus confers heat tolerance not only to its native monocot host but also to a eudicot host, ruses, the 5′ ends (21 bp) of both RNAs are
which suggests that the underlying mechanism involves pathways conserved between these two conserved. Virus particles purified from C.
groups of plants. protuberata are similar to those of other fungal
viruses: spherical and ~27 nm in diameter (fig.
E
ndophytic fungi commonly grow within known mutualistic endophyte, Epichloë festucae, S3). This virus is transmitted vertically in the
plant tissues and can be mutualistic in but no phenotype has been associated with this conidiospores. We propose naming this virus
some cases, as they allow plant adaptation virus (9). Curvularia thermal tolerance virus (CThTV) to
APPLIED AND ENVIRONMENTAL MICROBIOLOGY, June 2010, p. 4063–4075 Vol. 76, No. 12 to extreme environments (1). A plant-fungal Fungal virus genomes are commonly com- reflect its host of origin and its phenotype.
0099-2240/10/$12.00 doi:10.1128/AEM.02928-09 symbiosis between a tropical panic grass from posed of double-stranded RNA (dsRNA) (10). The ability of the fungus to confer heat
Copyright © 2010, American Society for Microbiology. All Rights Reserved. geothermal soils, Dichanthelium lanuginosum, Large molecules of dsRNA do not normally tolerance to its host plant is related to the
and the fungus Curvularia protuberata allows occur in fungal cells and, therefore, their presence presence of CThTV. Wild-type isolates of C.
both organisms to grow at high soil temperatures is a sign of a viral infection (9). Using a protocol protuberata contained the virus in high titers, as
in Yellowstone National Park (YNP) (2). Field for nucleic acid extraction with enrichment for evidenced by their high concentration of dsRNA
Diverse Bacteria Inhabit Living Hyphae of Phylogenetically and laboratory experiments have shown that
when root zones are heated up to 65°C, non-
dsRNA (11), we detected the presence of a virus
in C. protuberata. The dsRNA banding pattern
(~2 mg/g of lyophilized mycelium). However, an
isolate obtained from sectoring (change in
Diverse Fungal Endophytesᰔ†
symbiotic plants either become shriveled and consists of two segments of about 2.2 and 1.8 kb. morphology) of a wild-type colony contained a
chlorotic or simply die, whereas symbiotic plants A smaller segment, less than 1 kb in length, was very low titer of the virus, as indicated by a low
tolerate and survive the heat regime. When variable in presence and size in the isolates concentration of dsRNA (~0.02 mg/g of lyophi-
grown separately, neither the fungus nor the plant analyzed and, later, was confirmed to be a sub- lized mycelium). These two isolates were iden-
Michele T. Hoffman and A. Elizabeth Arnold* alone is able to grow at temperatures above 38°C, genomic element, most likely a defective RNA tical by simple sequence repeat (SSR) analysis
but symbiotically, they are able to tolerate ele- (fig. S1 and Fig. 1, A and B). Using tagged with two single-primer polymerase chain reac-
Downloaded from http://
Division of Plant Pathology and Microbiology, School of Plant Sciences, 1140 E. South Campus Drive, vated temperatures. In the absence of heat stress, random hexamer primers, we transcribed the tion (PCR) reactions and by sequence analysis of
symbiotic plants have enhanced growth rate virus with reverse transcriptase (RT), followed by the rDNA ITS1-5.8S-ITS2 region (figs. S4 and
University of Arizona, Tucson, Arizona 85721 compared with nonsymbiotic plants and also amplification and cloning. Sequence analysis S5). Desiccation and freezing-thawing cycles are
show significant drought tolerance (3). revealed that each of the two RNA segments known to disrupt virus particles (12); thus, my-
Received 3 December 2009/Accepted 20 April 2010 Fungal viruses or mycoviruses can modulate contains two open reading frames (ORFs) (fig. celium of the isolate obtained by sectoring was
plant-fungal symbioses. The best known exam-
ple of this is the hypovirus that attenuates the
Both the establishment and outcomes of plant-fungus symbioses can be influenced by abiotic factors, the virulence (hypovirulence) of the chestnut blight Fig. 1. Presence or absence of
CThTV in different strains of C.
interplay of fungal and plant genotypes, and additional microbes associated with fungal mycelia. Recently fungus, Cryphonectria parasitica (4). Virus regu-
protuberata, detected by ethid-
lation of hypovirulence has been demonstrated
bacterial endosymbionts were documented in soilborne Glomeromycota and Mucoromycotina and in at least
Domestication: Ant farmed fungi
experimentally in several other pathogenic fungi ium bromide staining (A),
Northern blot using RNA 1 (B)
one species each of mycorrhizal Basidiomycota and Ascomycota. Here we show for the first time that phylo- (5–8). However, the effect of mycoviruses on
and RNA 2 (C) transcripts of
mutualistic fungal endophytes is unknown. There
genetically diverse endohyphal bacteria occur in living hyphae of diverse foliar endophytes, including repre- is only one report of a mycovirus from the well-
the virus as probes, and RT-
PCR using primers specific for
sentatives of four classes of Ascomycota. We examined 414 isolates of endophytic fungi, isolated from photo-

6. Estimates of the number of species of Fungi
Mycol. Res. 9S (6): 641--655 (1991) Printed in Great Britain 641
Presidential address 1990
1.5 Million based on fungus to
The fungal dimension of biodiversity: magnitude, significance, plant ratio of 6:1
and conservation
D. L. HAWKSWORTH
International Mycological Institute, Kew, Surrey TW9 3AF, UK
American Journal of Botany 98(3): 426–438. 2011.
Don’t forget the endophytes...
Fungi, members of the kingdoms Chromista, Fungi S.str. and Protozoa studied by mycologists, have received scant consideration in
discussions on biodiversity. The number of known species is about 69000, but that in the world is conservatively estimated at THE FUNGI: 1, 2, 3 … 5.1 MILLION SPECIES?1
and the soil...
1'5 million; six-times higher than hitherto suggested. The new world estimate is primarily based on vascular plant:fungus ratios in
different regions. It is considered conservative as: (1) it is based on the lower estimates of world vascular plants; (2) no separate Meredith Blackwell2
provision is made for the vast numbers of insects now suggested to exist; (3) ratios are based on areas still not fully known
mycologically; and (4) no allowance is made for higher ratios in tropical and polar regions. Evidence that numerous new species Department of Biological Sciences; Louisiana State University; Baton Rouge, Louisiana 70803 USA
remain to be found is presented. This realization has major implications for systematic manpower, resources, and classification. Fungi DOI:10.3732/ajb.1000298
• Premise of the study: Fungi are major decomposers in certain ecosystems and essential associates of many organisms. They
have and continue to playa vital role in the evolution of terrestrial life (especially through mutualisms), ecosystem function and the
provide enzymes and drugs and serve as experimental organisms. In 1991, a landmark paper estimated that there are 1.5 million
maintenance of biodiversity, human progress, and the operation of Gaia. Conservation in situ and ex situ are complementary, andon the Earth. Because only 70 000 fungi had been described at that time, the estimate has been the impetus to search for
fungi the
significance of culture collections is stressed. International collaboration is required to develop a world inventory, quantify functional unknown fungi. Fungal habitats include soil, water, and organisms that may harbor large numbers of understudied
previously
roles, and for effective conservation. fungi, estimated to outnumber plants by at least 6 to 1. More recent estimates based on high-throughput sequencing methods
Upwards of 6M species - Lee Taylor (pers comm)
suggest that as many as 5.1 million fungal species exist.
• Methods: Technological advances make it possible to apply molecular methods to develop a stable classification and to dis-
cover and identify fungal taxa.
'Biodiversity', the extent of biological variation on Earth, has species, or populations. Knowledge of all of theseKey pertinent
• is results: Molecular methods have dramatically increased our knowledge of Fungi in less than 20 years, revealing a mono-
“Thus, the Fungi is likely equaled only by the Insecta with respect to eukaryote species richness.”
come to the fore as a key issue in science and politics for the
1990s. First used as 'BioDiversity' in the title of a scientific
to a thorough appreciation of the fungal dimension, butkingdom and increased diversity among early-diverging lineages. Mycologists are making significant advances in
phyletic here
I will centre on species biodiversity; that is basal to discussions but many fungi remain to be discovered.
species discovery,
• Conclusions: Fungi are essential to the survival of many groups of organisms with which they form associations. They also

7. Fungal genome sequencing
400+ genomes of Fungi
http://www.diark.org/diark/statistics

8. http://1000.fungalgenomes.org

9. Addressing the phylogenetic diversity: 1000 Fungal genomes project
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Blue = completed or in progress, Red= proposed for Tier One sampling,
Green = remaining unsampled families Numbers or Percent of Families in each clade and their current or proposed genome sampling

10. FungiDB
Strategy queries Genome Browser
Data-mining Synteny
Functional Phylogenomic
Genomics profiles
Data
Annotation &
Function Gene function curation tool

12. • Eurotiomycetes; Ascomycota
◦ Aspergillus clavatus
◦ Aspergillus flavus
◦ Aspergillus fumigatus strain Af293
◦ Aspergillus nidulans strain A4
FungiDB 2.0 ◦ Aspergillus niger
◦ Aspergillus terreus
◦ Coccidoidies immitis strain RS
◦ Coccidoidies immitis strain H538.4
• Sordariomycetes; Ascomyocta
◦ Fusarium oxysporum f. sp. lycopersici
• 31 genomes - 25 Fungi and 6 Oomycetes ◦ Fusarium graminearum
◦ Gibberella moniliformis (Fusarium verticillioides)
◦ Magnaporthea oryzae
• RNA-Seq for 6 species, Microarray for 2 sp, KEGG, EC, ◦ Neurospora crassa strain OR74A
◦ Neurospora tetrasperma
and GO annotations for several species ◦ Neurospora discreta
◦ Sordaria macrospora
• Taphrinomycotina; Ascomyocta
◦ Schizosaccharomyces pombe
• Ortholog tables with OrthoMCL • Saccharomycotina; Ascomyocta
◦ Candida albicans
◦ Saccharomyces cerevisiae
• Gene function predictions from InterPro • Basidiomycota
◦ Cryptococcus neoformans var. grubii) strain H99
◦ Cryptococcus neoformans var. neoformans) strain JEC21
◦ Cryptococcus neoformans var. neoformans) strain B3501
◦ Cryptococcus gattii strain WM276
◦ Cryptococcus gattii strain R265
◦ Tremella mesenterica
• Oomycetes; Stramenopiles
◦ Phytophthora capsici
◦ Phytophthora infestans
◦ Phytophthora ramorum
◦ Phytophthora sojae
◦ Pythium ultimatum
◦ Hyaloperonospora arabidopsidis

19. Combining queries
• Results from one query combined with a second one.
• Can be intersection, union, or left or right overlaps

22. Microbial Ecology of Indoor Fungi
• Sloan Foundation initiative to provide a data coordination center for indoor microbiome data
• In collaboration with Rob Knight (QIIME), Mitch Sogin (VAMPS), Folker Meyer (MG-RAST)
• Fungi - names and taxonomy in flux
• Marker Genes and data collection approaches
• A sample indoor environment dataset analysis

23. Fungal Taxonomy and naming undergoing a revolution
One fungus, one name
IMA FuNgus · voluMe 2 · No 1: 105–112
The Amsterdam Declaration on Fungal Nomenclature
A RT I C L E
1 3 3
Taylor 6
*, Özlem Abaci7 , Ahmet Asan , Feng-Yan Bai10 6
, Dominik
Begerow11, Derya Berikten , Teun Boekhout 13
, Treena Burgess , Walter Buzina 16
17
, Ulrike Damm , Irina Druzhinina ,
Ursula Eberhardt ,
10
,
30 31
, Ahmed
Ismail 13 33
, Urmas Kõljalg 36
, Paul-Emile Lagneau37,
3
, Xingzhong Liu10, Lorenzo Lombard , Wieland Meyer , Andrew Miller , Mohammad
Javad Najafzadeh , Lorelei Norvell 13 36
,
, William Quaedvlieg 1
, Johan Schnürer ,
, Bernard Slippers6 , Masako Takashima , Marco Thines , Ulf Thrane , Alev
, Bevan
13
, Neriman Yilmaz , Andrey Yurkov , and Ning Zhang

24. http://www.biology.duke.edu/fungi/mycolab/primers.htm

25. Barcoding consortium has chosen ITS as primary marker
Nuclear ribosomal internal transcribed spacer (ITS)
region as a universal DNA barcode marker for Fungi
Conrad L. Schocha,1, Keith A. Seifertb,1, Sabine Huhndorfc, Vincent Robertd, John L. Spougea, C. André Levesqueb,
Wen Chenb, and Fungal Barcoding Consortiuma,2
a
National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20892; bBiodiversity (Mycology
and Microbiology), Agriculture and Agri-Food Canada, Ottawa, ON, Canada K1A 0C6; cDepartment of Botany, The Field Museum, Chicago, IL 60605; and
d
Centraalbureau voor Schimmelcultures Fungal Biodiversity Centre (CBS-KNAW), 3508 AD, Utrecht, The Netherlands
Edited* by Daniel H. Janzen, University of Pennsylvania, Philadelphia, PA, and approved February 24, 2012 (received for review October 18, 2011)
Six DNA regions were evaluated as potential DNA barcodes for the intron of the trnK gene. This system sets a precedent for
Fungi, the second largest kingdom of eukaryotic life, by a multina- reconsidering CO1 as the default fungal barcode.
tional, multilaboratory consortium. The region of the mitochondrial CO1 functions reasonably well as a barcode in some fungal
cytochrome c oxidase subunit 1 used as the animal barcode was genera, such as Penicillium, with reliable primers and adequate
excluded as a potential marker, because it is difficult to amplify in species resolution (67% in this young lineage) (9); however,
fungi, often includes large introns, and can be insufficiently vari- results in the few other groups examined experimentally are in-
able. Three subunits from the nuclear ribosomal RNA cistron were consistent, and cloning is often required (10). The degenerate
compared together with regions of three representative protein- primers applicable to many Ascomycota (11) are difficult to as-
coding genes (largest subunit of RNA polymerase II, second largest sess, because amplification failures may not reflect priming
subunit of RNA polymerase II, and minichromosome maintenance mismatches. Extreme length variation occurs because of multiple
protein). Although the protein-coding gene regions often had introns (9, 12–14), which are not consistently present in a species.
MICROBIOLOGY
a higher percent of correct identification compared with ribosomal Multiple copies of different lengths and variable sequences oc-
markers, low PCR amplification and sequencing success eliminated cur, with identical sequences sometimes shared by several species
them as candidates for a universal fungal barcode. Among the (11). Some fungal clades, such as Neocallimastigomycota (an
regions of the ribosomal cistron, the internal transcribed spacer early diverging lineage of obligately anaerobic, zoosporic gut
(ITS) region has the highest probability of successful identification fungi), lack mitochondria (15). Finally, because most fungi are
for the broadest range of fungi, with the most clearly defined bar- microscopic and inconspicuous and many are unculturable, ro-
code gap between inter- and intraspecific variation. The nuclear bust, universal primers must be available to detect a truly rep-
ribosomal large subunit, a popular phylogenetic marker in certain
resentative profile. This availability seems impossible with CO1.
groups, had superior species resolution in some taxonomic groups,
The nuclear rRNA cistron has been used for fungal dia-
such as the early diverging lineages and the ascomycete yeasts, but
gnostics and phylogenetics for more than 20 y (16), and its
was otherwise slightly inferior to the ITS. The nuclear ribosomal
components are most frequently discussed as alternatives to CO1
small subunit has poor species-level resolution in fungi. ITS will be
(13, 17). The eukaryotic rRNA cistron consists of the 18S, 5.8S,
formally proposed for adoption as the primary fungal barcode
and 28S rRNA genes transcribed as a unit by RNA polymerase I.
http://fungalbarcoding.org
marker to the Consortium for the Barcode of Life, with the possibil-
Posttranscriptional processes split the cistron, removing two in-
ity that supplementary barcodes may be developed for particular
narrowly circumscribed taxonomic groups.
ternal transcribed spacers. These two spacers, including the 5.8S
gene, are usually referred to as the ITS region. The 18S nuclear

26. One published indoor microbiome
• Amend et al PNAS 2010 “Indoor fungal composition is geographically patterned and more diverse in
temperate zones than in the tropics.”
• 72 samples of fungi from 6 continents. Sampled ITS2 region and the D1-D2 region of LSU with 454-FLX
• Main finding of increasing species diversity with increasing latitude

27. Fig 1. Amend et al 2010

29. ITS 28S
PCA
of
normalized
counts
–
Painted
by
rRNA
type MG-­‐RAST
tools

30. PCA
of
normalized
counts
–
Painted
by
sampled
country
MG-­‐RAST
tools

31. PCA
of
normalized
counts
–
Painted
by
sampled
elevaCon
MG-­‐RAST
tools

32. From barcodes to organisms
Dilution to Extinction (d2e)
‘High throughput’ isolation from global dust samples
Sarea resinae
Cryptocoryneum rilstonei
Keith Seifert

33. Summary
• New tool development for interacting with genome and metagenome data for Fungi
• FungiDB is a resource for genome investigations and repeatable queries and workflows
• Development of a centralized resource for ITS sequences will enable better analysis of amplicon
metagenomics of Fungi

34. Acknowledgements
Marine
Biological
Lab
-­‐
VAMPS
Stajich
lab
@UCR
lab Undergraduates Mitch
Sogin
Peng
Liu Jessica
De
Anda Sue
Huse
Brad
Cavinder Sapphire
Ear Anna
Shipunova Anthony Amend
Sofia
Robb Lorena
Rivera Univ
of
Colorado
at
Boulder
-­‐
QIIME Keith Seifert
Steven
Ahrendt Carlos
Rojas Rob
Knight
Divya
Sain
Erum
Khan ScoW
Bates
Yizhou
Wang Ramy
Wissa Gail
Ackerman
Yi
Zhou Annie
Nguyen Jesse
Stombaugh
FungiDB
Programmers Argonne
NaConal
Lab
-­‐
MG-­‐RAST
Daniel
Borcherding Folker
Meyer
Raghu
Ramamurthy Daniel
Braithwaite
Edward
Liaw Travis
Harrison
Greg
Gu Kevin
Keegan
Andreas
Wilke
EuPathDB @UPenn & UGA
David Roos, Jessica Kissinger, Chris Stoeckert
Steve Fischer - John Brestelli
Brian Brunk - Debbie Pinney
Wei Li - Sufen Hu