The Candida genome database incorporates
multiple Candida species: multispecies search
and analysis tools with curated gene and
protein information for Candida albicans
and Candida glabrata
Diane O. Inglis, Martha B. Arnaud*, Jonathan Binkley, Prachi Shah, Marek S. Skrzypek,
Farrell Wymore, Gail Binkley, Stuart R. Miyasato, Matt Simison and Gavin Sherlock
Department of Genetics, Stanford University Medical School, Stanford, CA 94305-5120, USA
Received September 9, 2011; Accepted October 11, 2011
The Candida Genome Database (CGD, http://www
genomic sequence data and manually curated
functional information about genes and proteins
of the fungal pathogen Candida albicans and other
Candida species. As the scope of Candida research,
and the number of sequenced strains and related
species, has grown in recent years, the need for
expanded genomic resources has also grown. To
answer this need, CGD has expanded beyond
storing data solely for C. albicans, now integrating
data from multiple species. Herein we describe the
incorporation of thismultispecies
which includes curated gene information and the
reference sequence for C. glabrata, as well as
orthology relationships that interconnect Locus
Summary pages, allowing easy navigation between
genes of C. albicans and C. glabrata. These
orthology relationships are also used to predict
GO annotations of their products. We have also
chemical properties; bibliographic pages highlight-
ing important topic areas in Candida biology;
and a laboratory strain lineage page that describes
the lineage of commonly used laboratory strains.
All of these data are freely available at http://www
Candida albicans is the most common fungal pathogen
causing invasive and bloodstream infections in immuno-
compromised patients, although in recent years, several
non-albicans species and other yeasts have also emerged
as major opportunistic pathogens (1,2). Studies in the US
identify Candida glabrata as the second most common
Candida species involved in invasive fungal infections.
azoles, is common among C. glabrata clinical strains
isolated from patients with prior azole treatment (1).
The availability of genome sequences for these pathogenic
fungi has made it possible to study genes that play a role in
pathogenesis and drug resistance in Candida species,
thereby increasing our understanding of the mechanisms
of virulence in fungal pathogens.
The Candida Genome Database (CGD, http://www
.candidagenome.org/) is an online resource for the scien-
tific research community studying fungal molecular
biology and pathogenesis. The primary mission of CGD
is to facilitate and accelerate Candida research by
providing both an extensively curated compendium of
Candida gene, protein and sequence information, and
easy-to-use web-based tools for accessing, analyzing and
exploring these data.
When the CGD project began in 2004, our initial efforts
focused on curation of C. albicans, because it is the
best-characterized species of the group and has the
*To whom correspondence should be addressed. Tel: +1 650 736 0075; Fax: +1 650 724 3701; Email: email@example.com
Published online 7 November 2011Nucleic Acids Research, 2012, Vol. 40, Database issueD667–D674
? The Author(s) 2011. Published by Oxford University Press.
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/
by-nc/3.0), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
We have now expanded the scope of the project to include
other Candida species, and provide an extensive suite of
tools and resources that have been redesigned to facilitate
the analysis of multiple species concurrently. The CGD
Locus Summary Page (LSP) has been updated with infor-
mation about the identity of orthologous genes in
C. glabrata, and with orthology-based functional predic-
tions and gene descriptions. We currently display both
quence information about C. albicans and the recently
added species, C. glabrata. We also provide genomic
and protein sequence downloads and BLAST (3) re-
sources for multipleCandida
including C. albicans strains SC5314 (4) and WO-1 (5),
C. dubliniensis (6), C. guilliermondii (5), C. lusitaniae (5),
C. parapsilosis (5), C. tropicalis (5), Debaryomyces hansenii
(7) and Lodderomyces elongisporus (5). We will be adding
curated information for all these other Candida species in
All of the data in CGD are freely available. We also
have an extensive suite of online user documentation, and
gene, proteinand se-
species and strains,
LITERATURE CURATION FOR MULTIPLE CANDIDA
At CGD, PHD level curators perform ongoing manual
curation of the scientific literature to collect, organize,
summarize and present a comprehensive picture of each
characterized gene. Manual curation includes the record-
ing of gene names, addition and updates to our summary
gene descriptions, capture of mutant phenotype data and
the assignment of relevant GO annotations with evidence
The manual curation of the previously published litera-
ture pertaining to genes of C. albicans and C. glabrata is
now complete (Table 1). We have combed the scientific
describing the function, role and localization of gene
products; and mutant phenotypes. These are now
reported in CGD for all of the genes for which this infor-
mation is available. At this time, there are 6203 predicted
chromosomes in the current (Assembly 21) reference
gene set, 22% with manually annotated gene and protein
information. For C. glabrata, the reference annotation set
contains 5212 predicted genes, each of which has a LSP
(Figure 1), and 3% of which have manually curated an-
notations. CGD now includes a detailed Genome
Snapshot for C. glabrata in addition to C. albicans,
which provides a graphical and tabular summary of infor-
mation about the total number of chromosomal features
and feature types, changes to the reference sequence and a
distribution of gene products by functional categories and
cellular localization (Figure 2).
In addition, CGD curators have composed in-depth de-
scriptive Locus Summaries for 272 selected C. albicans
genes, which, in contrast to the very concise Locus
Descriptions, are more detailed enumerations of the char-
acteristics of each gene, presented in a bullet-point format
on the CGD LSPs. They provide additional experimental
details and gene regulatory information that cannot be
accommodated within the space limits of the Locus
Description line. These lists are displayed in the Locus
Summary section located near the bottom of the page
and are fully searchable through the CGD Text Search
The curation of the entire body of scientific literature
for these organisms is a large and ongoing endeavor as
new papers are published, and we welcome suggestions
from users as to papers that should be prioritized or
other data that should be included. We greatly appreciate
the beneficial interactions with members of the Candida
research community who have already volunteered to
review specific LSPs and provide feedback on the
curation content for specific genes. The comments we
have received have resulted in refinement of description
lines, improvements to phenotype and GO annotations,
and addition of new references that we had not encoun-
tered in our literature searches—improvements that
benefit the entire community of CGD users.
TOOLS FOR SEARCH AND DISPLAY OF
MULTISPECIES INFORMATION IN CGD
CGD was originally modeled after the Saccharomyces
Genome Database (SGD) (8), a database that provides
the Saccharomyces cerevisiae reference sequence with
Table 1. CGD curation statistics
Candida albicansCandida glabrata
Number of ORFs
Number of tRNAs
Manual GO annotations
Features with manual GO annotations
Orthology-based GO annotations
Features with orthology-based GO annotations
Protein-domain (InterPro)-based GO annotations
Features with protein-domain (InterPro)-based GO annotations
Features with orthology-based description lines
D668Nucleic AcidsResearch, 2012, Vol.40,Database issue
Figure 1. Updates to the CGD Locus Summary Page (LSP). The LSP is the hub around which the CGD gene information is organized. LSPs for
both C. albicans and C. glabrata now feature new expanded orthology information sections, orthology-based description lines for uncharacterized
genes, orthology-based GO term predictions and protein domain-based GO term predictions.
Nucleic Acids Research, 2012,Vol.40, Database issueD669
literature curation, and gene, protein and sequence
analysis tools for the S. cerevisiae research community.
SGD, and initially CGD, were designed to store and
display data for only a single species at a time. To accom-
modate the incorporation of additional species in the
database, user interface and analysis tools, significant
design modifications to the software and the underlying
database structure were necessary.
The CGD search tools, such as Quick Search, Text
Search, Gene/Sequence Resources, Ortholog Search and
Pattern Match have been redesigned to search multiple
species. In order to accommodate search results for
multiple species, the new results page for the CGD
Quick Search and Text Search tools now displays three
sections. Search results that apply to all species (e.g. GO
terms, authors and reference information, colleagues) are
displayed at the top, with sections for species-specific
search results displayed below. All of the tools that
perform species- or sequence-specific searches (e.g. Gene/
Sequence Resources, Pattern Match, Advanced Search,
Batch Download, Restriction Mapper, GO Term Finder,
GO Slim Mapper) have been updated, and they now
prompt users to select the species of interest. The
Ortholog Search now retrieves ortholog and best-hit
matches among all of the species in CGD and SGD (cur-
rently C. albicans, C. glabrata and S. cerevisiae). BLAST
searches at CGD have also been redesigned to allow
queries against any combination of the several Candida
species for which we have complete sequence sets
(C. albicans, C. glabrata, C. dubliniensis, C. guilliermondii,
C. lusitaniae, C. parapsilosis, C. tropicalis, Debaryomyces
hansenii and Lodderomyces elongisporus). In addition, the
curation tools have been extensively modified to facilitate
the curation of multiple species.
Each gene in CGD is represented on a LSP, which is the
central organizing unit of the CGD web site. The LSP
contains the basic information that describes the gene
and provides access to tools for retrieval, analysis and
visualization of gene data. We have reengineered the
(Figure 1). LSPs for each C. albicans and C. glabrata
gene now feature an expanded orthology section, by
which the LSPs of each C. albicans gene are hyperlinked
to the LSPs of their C. glabrata orthologs, and vice versa.
The LSP for C. glabrata genes also provide external links
to gene pages available at Ge nolevures (http://www.
genolevures.org/cagl.html#) This section also serves as a
Saccharomyces cerevisiae, providing hyperlinks to the
LSP of each ortholog in the SGD. Including S. cerevisiae
C. glabrata LSPs: the evolutionary divergence between
C. glabrata and S. cerevisiae is considerably more recent
(100-300 million years ago) (7,9) than the divergence
between these two species and C. albicans (700-800
million years ago) (10), and thus C. glabrata shares a
larger number of orthologs with S. cerevisiae than with
C. albicans, 4372 and 3201, respectively (as predicted by
InParanoid). To define orthology relationships, we use the
InParanoid algorithm, which identifies reciprocal best
BLAST hits between species (11). These mappings and
links are updated quarterly in order to reflect changes in
gene models and annotations at CGD and SGD.
In addition to the new orthology relationships displayed
in CGD, another level of similarity-based information is
provided via the new Protein tab on the LSP of each
protein-coding gene (Figure 3). This tab opens the
Protein Information page that provides descriptions and
a graphical display of conserved protein domains and
motifs identified using InterProScan software (12,13).
The Protein Information pages also display the structure
of the most similar protein in the Protein Data Bank (14),
and contain information about the predicted protein
length, molecular weight, sequence and a link to a table
of calculated physicochemical properties.
especiallyuseful for the
LEVERAGING MULTISPECIES INFORMATION IN
CGD: HOMOLOGY-BASED FUNCTIONAL
The GO is a structured vocabulary that is used to describe
three aspects of gene products: their molecular function or
178 ORFs, 3.42%
5034 ORFs, 96.58%
1385 ORFs, 22.33%
4666 ORFs, 75.22%
152 ORFs, 2.45%
C. albicansC. glabrata
Verified Verified Dubious
Figure 2. CGD genome snapshots. Pie chart from the CGD Genome Snapshots, comparing the current extent of the characterization of the
predicted protein-coding genes in the C. albicans and C. glabrata genomes. ORFs are classified as ‘Verified’ if there is experimental evidence for
a functional gene product. ‘Uncharacterized’ ORFs are predicted based on sequence analysis but currently lack experimental characterization.
Candida albicans ORFs labeled as ‘Dubious’ have no experimental characterization and appear to be indistinguishable from random non-coding
D670 Nucleic AcidsResearch, 2012, Vol.40,Database issue
Figure 3. Protein information page. The Protein Information page provides data including structural information inferred from homologs in PDB
(RCSB Protein Data Bank), an interactive domains/motifs browser, protein sequence and physicochemical property details, BLASTP search against
other CGD sequences and links to external protein resources such as UniProt.
Nucleic Acids Research, 2012,Vol.40, Database issueD671
activity, the broader biological process in which they par-
ticipate, and the cellular location in which they reside (15).
A gene product can be annotated with any number of
terms about any of the three aspects, depending on the
available data. Each GO term assignment is associated
with an evidence code that describes the type of data the
assignment is based on, and with a reference to its source.
The GO is in wide use in genomic research and because it
is rigorously structured, it ensures consistency in capturing
of functional information about genes from different or-
ganisms and thus enables reliable analysis of biological
significance of genomic data (15–21).
C. glabrata, all of the available gene-related literature per-
taining to these two species has been read and all possible
GO assignments from these papers have been made. To
augment the manual curation, we have leveraged the
orthology relationships to infer GO annotations for
genes having an experimentally characterized ortholog in
SGD or CGD. Predictions for C. albicans are made based
on S. cerevisiae and C. glabrata orthologs, whereas pre-
dictions for C. glabrata are based on orthologs from
S. cerevisiae and C. albicans. Despite the evolutionary
distances between C. albicans, C. glabrata and S.
cerevisiae, the use of orthology relationships to infer GO
annotations between C. albicans and C. glabrata allow the
transfer ofa significant
pathogenesis-related terms to be transferred between
these two fungal pathogens. Candidate GO annotations
to be used as the basis for these inferences are limited to
those with experimental evidence, i.e. associated with
evidence codes of ‘Inferred from Direct Assay (IDA)’,
‘Inferred from Physical Interaction (IPI)’, ‘Inferred from
Genetic Interaction (IGI)’, or ‘Inferred from Mutant
Phenotype (IMP)’. Any annotations that are themselves
predicted in S. cerevisiae or in Candida, either based on
sequence similarity or by some other methods, are
excluded from this group to avoid transitive propagation
of predictions. Also excluded from the predicted anno-
tation set are annotations that are redundant with
existing, manually curated annotations, or those that
assign a related but less specific GO term other than
candidate annotations. These orthology-based GO as-
signments are associated with evidence code ‘Inferred
from Electronic Annotation (IEA)’ and displayed with
the source species and gene name they are derived from
along with a hyperlink to the appropriate LSP at CGD
CGD has also taken advantage of protein domain and
motif homology to assign GO annotations for C. albicans
conserved domains in CGD protein sequences using
InterProScan (12), and then use the InterPro-to-GO
mappings (12,13) provided by the GO Consortium to
proteins. These annotations are assigned the evidence
code IEA and are displayed with the InterPro identifier
of the protein that serves as the basis for the annotation.
The identifier is linked to the EMBL-EBI database to
provide access to more extensive information about each
structural domain. We have also used the tRNAscan-SE
number of important
software to predict tRNA genes, and have inferred pre-
dicted GO annotations for these tRNAs (22).
The new annotations that have been transferred from
S. cerevisiae to C. albicans and C. glabrata, and between
C. albicans and C. glabrata, are summarized in Table 1. In
addition to having the evidence code IEA, all these
orthology-based annotations are identified as being
derived computationally, rather than manually extracted
from the scientific literature. Predictions are updated
several times a year to make sure they remain current
with annotation updates and new curation in CGD,
SGD and in the protein domain datasets.
for C. albicans and C. glabrata, and all orthology-based
and protein domain-based predictions have been made,
we consider curation of both species to be ‘GO-
complete’. For the remaining uncharacterized genes, we
indicate that to the best of our knowledge no data are
We have also used the multispecies information to
create informative descriptions for those Candida genes
that lack any experimental characterization, and which
therefore have no literature-based description on the
orthology-based functional predictions into the gene de-
scription in cases where there would otherwise be no in-
CURATED INFORMATIONAL PAGES AT CGD
Additional CGD resources for the Candida research com-
munity include a new collection of bibliographies on
topics relevant to Candida biology, which is accessible
under ‘Community Resources’ from the navigation
sidebar on the CGD Home page. These Highlights in
Candida Biology contain lists of important references,
including many key reviews, and are designed to provide
an overview of selected subject areas in C. albicans and
C. glabrata biology. This resource will be particularly
valuable for those new to Candida research. As new
species are curated at CGD, Highlights in Candida
Biology will expand to include bibliographies on these
species as well. The curated bibliographies are available
We have also curated a directory of strains, which
provides descriptions and references for commonly used
Candida laboratory strains, along with a lineage diagram
that graphically depicts the relationship among these
strains. This information is available on the CGD web
resource is especially important for researchers because
differences in strain background are known to have a sig-
nificant impact on observed mutant phenotypes. In some
cases, genes have been found to be lethal in one genetic
background while successful gene disruption is possible in
another. An example of this is the C. albicans UME6 gene,
for which homozygous mutants are viable in the SN152
genetic background (23) yet inviable in the BWP17 strain
background (24). Because of its importance, we also
D672Nucleic AcidsResearch, 2012, Vol.40,Database issue
provide all available strain background information along
with all of the curated phenotypes for each gene.
Now that the underlying database has been re-tooled to
accommodate the curation of multiple species, we will add
curated information for other Candida-related species
including C. dubliniensis, C. guilliermondii, C. lusitaniae,
C. parapsilosis, C. tropicalis, Debaryomyces hansenii and
Lodderomyces elongisporus. In order to facilitate naviga-
tion across multiple genomes, we will provide links to an
interactive comparative visualization tool, which will
allow users to explore ortholog clusters in their genomic
Recent advances in genomics technologies have created
a deluge of information that poses a significant challenge
of making all these data organized and readily available to
researchers. We have adapted our genome browser,
GBrowse, to enable users to visualize unannotated tran-
scripts in C. albicans that have been identified by RNAseq
(25–27). These transcripts are aligned to the reference
genome and displayed alongside the existing set of
features in the reference annotation. We will further
develop and/or integrate existing software to incorporate
and visualize more types of data and more data sets from
The authors would like to thank Ge ´ nolevures for making
the C. glabrata CBS138 sequence available, Brendan
Cormack and Suzanne Noble for strain lineage informa-
tion, and Mike Cherry and SGD for their help. CGD is
grateful to the many members of the Candida research
feedback and support for the project.
Funding for open access charge: National Institute of
Dental and Craniofacial Research at the US National
Institutes of Health (grant no. R01 DE015873).
Conflict of interest statement. None declared.
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