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The Institute of Zoology, Regent's Park, London NW1 4RY, UK
G. L. Koenig
T. J. White
Roche Molecular Systems, 1145 Atlantic Avenue, Alameda, California 94501, USA
J. W. Taylor
Department of Plant and Microbial Biology, University of California at Berkeley, Berkeley, California 94720-3102, USA
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSTAXONOMYDISCUSSIONLITERATURE CITED |
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Coccidioides posadasii sp. nov., formerly known as non-California (non-CA) Coccidioides immitis, is described. Phylogenetic analyses using single nucleotide polymorphisms, genes, and microsatellites show that C. posadasii represents a divergent, genetically recombining monophyletic clade. Coccidioides posadasii can be distinguished from C. immitis by numerous DNA polymorphisms, and we show how either of two microsatellite loci may be used as diagnostic markers for this species. Growth experiments show that C. posadasii has significantly slower growth rates on high-salt media when compared with C. immitis, suggesting that other phenotypic characters may exist.
Key words: allele, Coccidioidomycosis, microsatellite, Onygenales, phylogeny, systematics
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSTAXONOMYDISCUSSIONLITERATURE CITED |
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, Simpson 1961
, Wiley 1978
) and is the most inclusive species concept to date (Mayden 1997
). Molecular genetics (Reynolds and Taylor 1991
) and cladistic analyses provide a method of diagnosing species under the ESC by describing shared exclusive characters (apomorphies) using an operational method known as phylogenetic species recognition (PSR). A subset of PSR uses genealogical concordance (GCPSR) to detect genetically isolated groups by comparing the gene trees from a number of different loci (Avise and Ball 1990
). Different genes will have different genealogies within a species due to recombination, but between species the genealogies will be concordant due to the effects of genetic isolation and drift causing lineage sorting and coalescence. Detecting the common branches between these gene trees is the key to GCPSR.
GCPSR is finding increasing usage within both meiosporic and mitosporic fungal taxa (Taylor et al 2000
), for instance the Gibberella fujikuroi complex (O'Donnell et al 1998
), Ajellomyces capsulatus (Kwon-Chung) McGinnis and Katz (Kasuga et al 1999
), Aspergillus flavus Link (Geiser et al 1998
) and Coccidioides immitis Rixford and Gilchrist 1896
(Koufopanou et al 1997, 1998
). Here, we use GCPSR to demarcate barriers to gene flow between individuals of the pathogenic fungus Coccidioides immitis. Our analysis and those of others clearly show the existence of two genetically isolated and deeply divergent clades within C. immitis and we use this as the basis for describing a new species, Coccidioides posadasii. Knowledge of genetically defined species enables workers to look closely for previously undetectable morphological and phenotypic differences. We use this approach to show that C. immitis has a tendency to grow faster than C. posadasii on high-salt media. This demonstrates that other, perhaps clinically important, characters may exist.
Coccidioides immitis is a dimorphic pathogenic fungus found in the southwestern United States, Mexico, Central and South America (Pappagianis 1988
). In the saphrobic phase C. immitis is characteristically found inhabiting the arid, sandy soils of the Lower Sonoran Life Zone. Inhalation of arthroconidia causes a chronic pulmonary infection in humans and other vertebrates. In ca 0.5% of cases, secondary coccidioidomycosis occurs, a serious disseminated infection that is often fatal (Rippon 1988
). Immunity generated from resolving the infection is specific and usually lifelong.
Coccidioidomycosis was originally described by Alejandro Posadas (and later confirmed by Robert Wernicke) from a soldier, Domingo Ezcurra, who acquired his infection in the Argentine pampas (Posadas 1892
, Wernicke 1892
). Posadas and Wernicke recognized the presence of an organism, likened to a protozoon of the order Coccidia. Formal description of C. immitis was performed by Rixford and Gilchrist from a case observed in California (Rixford and Gilchrist 1896
). However, the parasite was then still thought to be a protozoan. The correct taxonomic status of C. immitis as an ascomycete fungus was demonstrated by Ophüls and Moffit (1900)
by culture on artificial media of the fungal mycelia using arthrospores isolated from laboratory infections of guinea pigs. The etiological relationship between C. immitis and coccidioidomycosis was also demonstrated by showing that arthroconidia cause infection in several types of laboratory animal. The lack of any known meiosporic state in vitro or in vivo hampered further classification until work by Sigler and Carmichael (1976)
recognized the similarity between the asexual spores (arthroconidia) of C. immitis and those (aleurioconidia) found in the mitosporic genus Malbranchea Sacc., placing C. immitis in the order Onygenaceae. This relationship was confirmed by molecular phylogenetic methods (Bowman et al 1992
, Pan et al 1994
, Bowman et al 1996
), and Uncinocarpus reesii Sigler and Orr was shown to be the sister group to C. immitis.
Research on the intraspecific relationships of C. immitis was first attempted by Zimmerman et al (1994)
, who compared RFLPs of total genomic DNA and showed that 15 clinical isolates formed two groups, referred to as Group I and Group II. Group I contained the isolate ‘Silveira’ that is extensively used in laboratory studies. Subsequent work by Burt et al (1997)
using RFLPs of 10 DNA loci demonstrated the occurrence of highly significant differences in allele frequencies between clinical isolates from California, Arizona and Texas, the Californian population being the most divergent. This result was corroborated by Koufopanou et al (1997, 1998
) who used genealogies of five nuclear genes to show that C. immitis consists of two non-interbreeding taxa, CA (centered in California) and non-CA (represented by clinical isolates from Arizona, Texas, Mexico, and Argentina). The ‘Silveira’ isolate was included in non-CA C. immitis, showing that Zimmerman's Group I and Koufopanou's non-CA were synonymous. Nucleotide sequence divergence between CA and non-CA showed that they had been reproductively isolated from one another for the past 11 million years, a result that was subsequently corroborated using a separate set of loci and C. immitis isolates (Fisher et al 2000b)
. That independent loci were randomly assorting with respect to one another within CA and non-CA showed that genetic recombination had occurred between individuals within the two groups, despite no teleomorph ever having been described for C. immitis (Burt et al 1996
, Fisher et al 2000a
). This observation suggests that the species described here are evolutionary species and could be recognized as biological species, as well as phylogenetic species, if a teleomorph were to be found.
Recently, the sampling of the C. immitis biogeographic distribution was extended to include previously unsampled populations from Southern California, Central and Southern Mexico, Venezuela, and Brazil, and analyzed using a suite of microsatellite markers (Fisher et al 1999
, Fisher et al 2000b
). Phylogenetic analyses showed that, despite the increased breadth and depth of sampling, the C. immitis phylogeny still contained two major clades (Fisher et al 2000c)
. Here, we use our dataset of microsatellite alleles to show that these clades correspond to the previous classifications of CA (Group II) and non-CA (Group I) C. immitis. Species rank is proposed for the two clades.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSTAXONOMYDISCUSSIONLITERATURE CITED |
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). Polymerase chain reaction (PCR) amplification of nine microsatellite-containing loci (GAC, 621, GA37, GA1, ACJ, KO3, KO7, KO1, KO9) was performed for each isolate using the fluorescently labelled primers and conditions described previously (Fisher et al 1999
). The multilocus genotype of each isolate was determined by electrophoresing the PCR products through a 6% denaturing polyacrylamide gel using an automated sequencer (Applied Biosystems), the alleles present at each locus being determined by reference against a TAMRA-labelled internal size standard. A standardized method for typing the alleles at each locus is available as a. pdf file at http://plantbio.berkeley.edu/~taylor/mf.html.
Phylogenetic analyses were performed using the microsatellite genetic distances DAS (Stephens et al 1992
, Bowcock et al 1994
) and (
µ)2 (Goldstein et al 1995
). Here, DAS = 1 - (the total number of shared alleles at all loci / n) where n is the number of loci compared. Pairwise distances calculated using the mean character distance option in PAUP* 4.0b1 (Swofford 1998
) are identical to DAS and were used here. The neighbor-joining algorithm in PAUP clustered these user-defined distances using the minimum evolution option, and support for each clade was estimated by 1000 neighbor-joining bootstrap replications of the dataset. Genetic distance between populations was assessed using the microsatellite distance (µ)2. This measure more closely reflects the genetic distance that has accrued within loci by accounting for the size of alleles, as well as their frequencies. (µ)2 equals the square of the difference in mean allele size (x) between two populations A and B such that (µ)2 = (xA - xB)2. Confidence intervals for (µ)2 were calculated by bootstrapping over loci using the program MICROSAT (Minch et al 1995
). Alignments were deposited in Tree Base, and are available under study accession number S692.
We looked for differences in the phenotype of CA and non-CA by (i) comparing the growth rates of colonies on media with salt concentrations increasing to near-inhibitory levels and by (ii) comparing spore-size. Pilot experiments were performed where 8 isolates were chosen (four of the CA and four of the non-CA genotype) and grown on YEG agar (1% yeast extract, 1% glucose, 1.5% agar, Difco, BD Microbiology Systems, Sparks, Maryland 21152) containing the following concentrations of NaCl; 0.034 M (2%), 0.068 M (4%), 0.102 M (6%). Each isolate was initially grown on YEG plates and 3 mm diameter plugs removed from the colony margin. These were then placed on the test media, incubated in the dark at 30 C, and colonies were measured across their diameters after 15 d of growth. Subsequently, an expanded experiment was performed where 20 clinical isolates (10 each of the CA and non-CA genotypes) were grown in replicates of 4 on YEG agar containing either 0.034 M (2%) or 0.136 M (8%) NaCl, colony growth being measured after 4, 8, 10, and 15 d of incubation at 30 C.
The length of arthroconidia were measured for a selection of strains of the CA and non-CA genotypes. Cultures were grown on malt extract agar (4% malt extract, 1.5% agar, Difco, BD Microbiology Systems, Sparks, Maryland 21152), stained with lactophenol cotton blue (Hardy Diagnostics, Santa Maria, California 93455) and sealed with nail varnish. Lengths were then determined for a minimum of 20 arthroconidia from each culture.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSTAXONOMYDISCUSSIONLITERATURE CITED |
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and Fisher et al (2000b)
onto this tree shows that the ‘upper’ clade (comprising 106 samples) contains isolates that are exclusively of the non-CA genotype (Fig. 2A
), and that the ‘lower’ clade (comprising 61 isolates) contains isolates that are exclusively of the CA genotype. This demonstrates that the original division of C. immitis into CA and non-CA (Koufopanou et al 1997
) using GCPSR holds across the entire distribution of fungi represented in this study, and is the phylogenetic basis for our proposing species status for CA and non-CA. The distribution of alleles at each locus for CA (white) and non-CA (black) are shown in Fig. 1
. These show that two loci, GAC2 and 621, are diagnostic for CA and non-CA. The other microsatellite-containing loci all show overlapping distributions in the sizes of alleles between CA and non-CA, however, in all cases the allele frequencies are dramatically different illustrating the deep genetic divergence between these two clades. The results of taking into account allele size as well as frequency are shown in Fig. 3
. The tree inferred using (µ)2 illustrates a tenfold increase in genetic distance between CA and non-CA genotypes when compared to the distance seen between populations within each clade, and has strong (99%) bootstrap support.
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We tested four different culture media in order to examine the colony growth rates of CA and non-CA isolates. In a pilot experiment, a trend was observed where non-CA isolates (filled circles) appeared to grow more slowly than CA isolates (open circles) as NaCl concentration in the medium was increased (Fig. 4 ). We investigated this effect further by increasing the scale of the experiment; 10 isolates from CA and non-CA were grown in quadruple replicates on media containing either 0.034 M (low salt) or 0.136 M (high-salt) NaCl. Fig. 5 shows the population mean and 95% confidence intervals for the growth rates of CA (open bars) and non-CA (filled bars) on the two media. While CA grew initially faster on low salt medium, by day 10 there was no significant difference between the two groups. On high-salt (inhibitory) medium, growth of CA and non-CA was restricted relative to the low-salt medium. However, on this medium significant inter-group variation was seen; growth of CA was significantly faster than non-CA for the duration of the experiment. The ranges of each group overlap, showing that this characteristic is not diagnostic between CA and non-CA (Fig. 5 ). Therefore, growth on high-salt plates appears to reflect phenotypic differences that have accrued between CA and non-CA, but these are not discrete and may not be used to distinguish between the two species.
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TAXONOMY |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSTAXONOMYDISCUSSIONLITERATURE CITED |
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). Based on the geographical distributions of CA and non-CA, this infection was most likely to have been caused by CA C. immitis, which should therefore retain the name. Coccidioides posadasii Fisher, Koenig, White et Taylor, sp. nov.
Morphologia idem ac Coccidioides immitis, distinguibilis characteribus sequentibus nucleotiditis fixationibus mutuis inter Coccidioidem immitem et Coccidioidem posadasii: positiones synthase chitinis 192 (A), 288 (T); positiones dioxygenase 872 (C), 1005 (C), 1020 (G), 1179 (C), 1272 (T); positiones orotidine decarboxylase 473 (A), 506 (C), 606 (C), 647 (A); positiones serine 477 (G), 517 (C), 632 (C), 744 (G), 887 (C); positio chitinase 910 (T) (Koufopanou et al 1997
, Koufopanou et al 1998
); positio z 134 (T) (Burt et al 1997
). Loci sequentes microsatellitum distributionibus propriis allelones: GAC2, PCR amplitudo operis primeribus GAC2.1 et GAC2.2 = 206 bp; 621, PCR amplitudo operis primeribus 621U et 621L = 397–401 bp.
Coccidioides posadasii is morphologically indistinguishable from Coccidioides immitis. C. posadasii is diagnosed by the following nucleotide characters (given as the gene, the nucleotide position in the gene, and, parenthetically, the nucleotide fixed in C. posadasii) showing reciprocal fixation between C. immitis and C. posadasii: Chitin synthase positions 192 (A), 288 (T); Dioxygenase positions 872 (C), 1005 (C), 1020 (G), 1179 (C), 1272 (T); Orotidine decarboxylase positions 473 (A), 506 (C), 606 (C), 647 (A); Serine proteinase positions 477 (G), 517 (C), 632 (C), 744 (G), 887 (C); Chitinase position 910 (T) (Koufopanou et al 1997
, Koufopanou et al 1998
). z position 134 (T) (Burt et al 1997
). The following microsatellite loci have exclusive allele distributions: GAC2, PCR product size using primers GAC2.1 and GAC2.2 = 206bp; 621, PCR product size using primers 621U and 621L = 397–401bp. Distribution: southwestern United States, Central and South America.
HOLOTYPE: Pappagianis isolate ‘Silveira’ (RMSCC Silveira, appendix) isolated in the San Joaquin Valley, California 1951. Widely used laboratory isolate, maintained by the American Type Culture Collection (ATCC) #28868. This isolate is currently on regulatory hold at the ATCC due to C. immitis being a controlled pathogen. A killed sample of RMSCC Silveira has been lodged in the Jepson Herbarium, University of California at Berkeley, Berkeley, California 94720, USA. Frozen samples of RMSCC Silveira are stored at Roche Molecular Systems, Alameda, California and the Centers for Disease Control and Prevention, Atlanta, Georgia.
Etymology. posadasii; after Alejandro Posadas who described the first case of coccidioidomycosis, which was from Argentina (Posadas 1892
)
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSTAXONOMYDISCUSSIONLITERATURE CITED |
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and seven described by Fisher et al 2000b
), thus fulfilling the criteria of GCPSR, (ii) the two species are deeply divergent, estimations of the time of genetic isolation ranging from 11 (Koufopanou et al 1998
)— 12.8 (Fisher et al 2000b)
million years ago, (iii) C. immitis and C. posadasii have been shown, separately, to genetically recombine in nature (Burt et al 1996
, Fisher et al 2000a
) and (iv) we have sampled the entire worldwide distribution of this pathogen, therefore we feel that the possibility is small of discovering further cryptic species of Coccidioides that would change the taxonomic relationships described here.
Coccidioides immitis appears to have the smaller biogeographic distribution of the two species, centered on the San Joaquin Valley, California. In this region, C. immitis appears to be the only species, however two clinical isolates of C. posadasii, Silveira and K-727, were recovered from this area. Silveira was isolated from a patient in Bakersfield in 1951 and K-727 from a patient in 1992; however, it is not known whether either patient had a history of travel to other parts of the southwest where these infections may have been acquired. Such movements of patients suffering from coccidioidomycosis have been previously detected using molecular markers (Burt et al 1997
). Coccidioides immitis and C. posadasii appear to be sympatric in southern California and Mexico. Here, significant intraspecific differences in allele frequencies between populations show that these are bona fida populations, and are not solely due to the immigration of patients with infections that were gained from other areas (Fisher et al 2000c)
.
In this paper, we have used phylogenetic analyses of microsatellite loci to identify isolates as C. immitis or C. posadasii. This approach was used because acquiring multiple gene genealogies for all the isolates described in this paper would be very difficult due to the amount of sequencing involved. Instead, the microsatellites provided a means of acquiring multilocus genotypes for many isolates with far less effort and expense. However, this technique must be used with caution as concerns exist when using microsatellites for phylogenetic analyses due to their mode and rate of mutation. Constraints exist on the sizes of microsatellites, causing a limit on the genetic distance that can accrue between genetically isolated taxa (Garza et al 1995
, Lehmann et al 1996
). Further, the high mutation rates seen at microsatellite loci cause the re-appearance of alleles that were previously lost from populations, resulting in mutational convergence (homoplasy) of alleles that are identical by size but not by descent. Such homoplasy can be directly observed from the allele distributions illustrated in Fig. 1
, where C. immitis and C. posadasii share identical alleles at all loci except GAC2 and 621. A cursory analysis of the data might lead to the conclusion that genetic isolation between C. immitis and C. posadasii was not absolute, due to the occurrence of alleles that are shared between the two taxa. We have addressed these concerns in a previous study by comparing the phylogeny inferred using the microsatellites against the phylogeny inferred using genes, and there showed that (i) they were identical, and that (ii) microsatellite alleles shared between the two taxa were a result of mutational convergence and not interbreeding (Fisher et al 2000b)
. This demonstrated that the Coccidioides microsatellite loci were correctly diagnosing taxonomic units that had been identified using the GCPSR, and were therefore suitable for extending the GCPSR to include the isolates used in this study. However, it should be recognized that, without performing this initial study, using microsatellite phylogenies alone to describe a species may not be valid.
Recognition of the two species has enabled us to show that C. posadasii grows more slowly on media containing high salt concentrations. The range in growth rates overlaps between the two species, showing that, although the difference in growth rates is significant, this phenotype is not diagnostic. The presence of differences in the amino acid composition of proteins between the two species (Koufopanou et al 1997
, Peng et al 1999
) suggests that other phenotypic differences may exist. This difference may extend to variation in the antigenicity of key proteins or pathogenicity factors. Recognizing the existence of C. posadasii is instrumental in allowing researchers and physicians to investigate these possibilities.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Accepted for publication June 4, 2001.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSTAXONOMYDISCUSSIONLITERATURE CITED |
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Bowcock AM, Ruiz-Linares A, Tomfohrde J, Minch EK, Kidd JR, Cavalli-Sforza LL., 1994 High resolution of human evolutionary trees with polymorphic microsatellites Nature 368:455-457[Medline]
Bowman BH, Taylor JW, White TJ., 1992 Molecular evolution of the fungi: Human pathogens Mol Biol Evol 9:893-904[Abstract]
Bowman BH, Taylor JW, White TJ., 1996 Human pathogenic fungi and their close non-pathogenic relatives Mol Phylo Evol 6:89-96[Medline]
Burt A, Carter DA, Koenig GL, White TJ, Taylor JW., 1995 A safe method of extracting DNA from Coccidioides immitis Fungl Genet Newsletter 42:23
Burt A, Carter DA, Koenig GL, White TJ, Taylor JW., 1996 Molecular markers reveal cryptic sex in the human pathogen Coccidioides immitis Proc Natl Acad Sci USA 93:770-773
Burt A, Dechairo BM, Koenig GL, Carter DA, White TJ, Taylor JW., 1997 Molecular markers reveal differentiation among isolates of Coccidioides immitis from California, Arizona and Texas Mol Ecol 6:781-786[Medline]
Fisher MC, Koenig GL, White TJ, Taylor JW., 1999 Primers for genotyping single nucleotide polymorphisms and microsatellites in the pathogenic fungus Coccidioides immitis Mol Ecol 8:1082-1084[Medline]
Fisher MC, Koenig GL, White TJ, Taylor JW., 2000a Pathogenic clones versus environmentally driven population increase: analysis of an epidemic of the human fungal pathogen Coccidioides immitis J Clin Microbiol 38:807-813
Fisher MC, Koenig GL, White TJ, Taylor JW., 2000b A test for concordance between the multilocus genealogies of genes and microsatellites in the pathogenic fungus Coccidioides immitis Mol Biol Evol 17:1164-1174
Fisher MC, Koenig GL, White TJ, San-Blas G, Negroni R, Gutiérrez-Alvarez I, Wanke B, Taylor JW., 2000c Biogeographic range expansion into South America by the pathogenic fungus Coccidioides immitis mirrors human patterns of migration Proc Natl Acad Sci USA 98:4558-4562
Garza JC, Slatkin M, Freimer NB., 1995 Microsatellite allele frequencies in humans and chimpanzees, with implications for constraints on allele size Mol Biol Evol 12:594-603[Abstract]
Geiser DM, Pitt JI, Taylor JW., 1998 Cryptic speciation and recombination in the aflatoxin producing fungus Aspergillus flavus Proc Natl Acad Sci USA 95:388-393
Goldstein DB, Ruiz Linares A, Cavalli-Sforza LL, Feldman MW., 1995 Genetic absolute dating based on microsatellites and the origin of modern humans Proc Natl Acad Sci USA 92:6723-6727
Kasuga T, Taylor JW, White TJ., 1999 Phylogenetic relationships of varieties and geographical groups of the human pathogenic fungus, Histoplasma capsulatum Darling J Clin Microbiol 37:653-663
Koufopanou V, Burt A, Taylor JW., 1997 Concordance of gene genealogies reveals reproductive isolation in the pathogenic fungus Coccidioides immitis Proc Natl Acad Sci USA 94:5478-5482
Koufopanou V, Burt A, Taylor JW., 1998 Concordance of gene genealogies reveals reproductive isolation in the pathogenic fungus Coccidioides immitis (vol 94, pg 5478, 1997) Proc Natl Acad Sci USA 95:8414
Lehmann T, Hawley WA, Collins FH., 1996 An evaluation of evolutionary constraints on microsatellite loci using null alleles Genetics 144:1155-1163[Abstract]
Mayden RL, ed 1997 A hierarchy of species concepts: the denouement in the saga of the species problem In: Claridge MF, Dawah HA, Wilson MR, eds. Species: the units of biodiversity. London and New York: Chapman and Hall. p 381–424
Minch E, Ruiz-Linares A, Goldstein D, Feldman M, Cavalli-Sforza LL., 1995 MICROSAT, The microsatellite distance program http://human.stanford.edu/ Stanford California: Stanford University
O'Donnell K, Cigelnik E, Nirenberg HI., 1998 Molecular systematics and phylogeography of the Gibberella fujikuroi species complex Mycologia 90:465-493
Ophüls W, Moffitt HC., 1900 A new pathogenic mould (formerly described as a protozoan: Coccidioides immitis pyogenes): preliminary report Phila Med J 5:1471-1472
Pan S, Sigler L, Cole GT., 1994 Evidence for a phylogenetic connection between Coccidioides immitis and Uncinocarpus reesii (Onygenaceae) Microbiology (Reading, England) 140:1481-1494[Abstract]
Pappagianis D., 1988 Epidemiology of coccidioidomycosis In: McGinnis MR, ed. Current topics in medical mycology. New York: Springer Verlag. p 199–238
Peng T, Orsborn KI, Orbach MJ, Galgiani JN., 1999 Proline-rich vaccine candidate antigen of Coccidioides immitis: conservation among isolates and differential expression with spherule maturation J Infect Dis 179:518-521[Medline]
Posadas A., 1892 Un nuevo caso de micosis fungoidea con psorospermias Ann Circ Med Argent 15:585-597
Reynolds DR, Taylor JW., 1991 DNA specimens and the ‘International code of botanical nomenclature’ Taxon 40:311-315
Rippon JW., 1988 Medical mycology: the pathogenic fungi and pathogenic actinomycetes Philadelphia: Harcourt Brace. 797 p
Rixford E, Gilchrist TC., 1896 Two cases of protozoan (coccidioidal) infection of the skin and other organs Johns Hopkins Hosp Rep 1:209-268
Sigler L, Carmichael JW., 1976 Taxonomy of Malbranchea and some other hypomycetes with arthroconidia Mycotaxon 4:349-488
Simpson GG., 1951 The species concept Evolution 5:285-298
Simpson GG., 1961 Principles of animal taxonomy New York: Columbia University Press. 247 p
Stephens JC, Gilbert DA, Yuhki N, O'Brien SJ., 1992 Estimation of heterozygosity for single-probe multilocus DNA fingerprints Mol Biol Evol 9:729-743[Abstract]
Swofford DL, 1998 PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4 Sunderland, Massachusetts: Sinauer Associates
Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser DM, Hibbett DS, Fisher MC., 2000 Phylogenetic species recognition and species concepts in fungi Fungal Genet Biol 31:21-32[Medline]
Wernicke R., 1892 Ueber einen Protozoenbefund bei Mycosis fungoides Zentralbl Bakteriol 12:859-861
Wiley EO., 1978 The evolutionary species concept reconsidered Syst Zool 27:17-26
Zimmerman CR, Snedker CJ, Pappagianis D., 1994 Characterization of Coccidioides immitis isolates by restriction fragment length polymorphisms J Clin Microbiol 32:3040-3042
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M. A. Saubolle, P. P. McKellar, and D. Sussland Epidemiologic, Clinical, and Diagnostic Aspects of Coccidioidomycosis J. Clin. Microbiol., January 1, 2007; 45(1): 26 - 30. [Full Text] [PDF]
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M. J. Binnicker, S. P. Buckwalter, J. J. Eisberner, R. A. Stewart, A. E. McCullough, S. L. Wohlfiel, and N. L. Wengenack Detection of Coccidioides Species in Clinical Specimens by Real-Time PCR J. Clin. Microbiol., January 1, 2007; 45(1): 173 - 178. [Abstract] [Full Text] [PDF]
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M. R. McGinnis, M. B. Smith, and E. Hinson Use of the Coccidioides posadasii {Delta}chs5 Strain for Quality Control in the ACCUPROBE Culture Identification Test for Coccidioides immitis. J. Clin. Microbiol., November 1, 2006; 44(11): 4250 - 4251. [Abstract] [Full Text] [PDF]
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M. Blackwell, D. S. Hibbett, J. W. Taylor, and J. W. Spatafora Research Coordination Networks: a phylogeny for kingdom Fungi (Deep Hypha) Mycologia, November 1, 2006; 98(6): 829 - 837. [Abstract] [Full Text] [PDF]
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 R. d. A. Cordeiro, R. S. N. Brilhante, M. F. G. Rocha, M. A. B. Fechine, Z. P. d. Camargo, and J. J. C. Sidrim In vitro inhibitory effect of antituberculosis drugs on clinical and environmental strains of Coccidioides posadasii J. Antimicrob. Chemother., September 1, 2006; 58(3): 575 - 579. [Abstract] [Full Text] [PDF]
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W. Morrow Holocene coccidioidomycosis: Valley Fever in early Holocene bison (Bison antiquus). Mycologia, September 1, 2006; 98(5): 669 - 677. [Abstract] [Full Text] [PDF]
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J. I. Pounder, D. Hansen, and G. L. Woods Identification of Histoplasma capsulatum, Blastomyces dermatitidis, and Coccidioides Species by Repetitive-Sequence-Based PCR. J. Clin. Microbiol., August 1, 2006; 44(8): 2977 - 2982. [Abstract] [Full Text] [PDF]
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 P. W. Abrahams Soil, geography and human disease: a critical review of the importance of medical cartography Progress in Physical Geography, August 1, 2006; 30(4): 490 - 512. [Abstract] [PDF]
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 D. J. DiCaudo, J. A. Yiannias, S. D. Laman, and K. E. Warschaw The exanthem of acute pulmonary coccidioidomycosis: clinical and histopathologic features of 3 cases and review of the literature. Arch Dermatol, June 1, 2006; 142(6): 744 - 746. [Abstract] [Full Text] [PDF]
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T. Umeyama, A. Sano, K. Kamei, M. Niimi, K. Nishimura, and Y. Uehara Novel Approach to Designing Primers for Identification and Distinction of the Human Pathogenic Fungi Coccidioides immitis and Coccidioides posadasii by PCR Amplification. J. Clin. Microbiol., May 1, 2006; 44(5): 1859 - 1862. [Abstract] [Full Text] [PDF]
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J. R. Dettman, D. J. Jacobson, and J. W. Taylor Multilocus sequence data reveal extensive phylogenetic species diversity within the Neurospora discreta complex. Mycologia, May 1, 2006; 98(3): 436 - 446. [Abstract] [Full Text] [PDF]
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N. Vanittanakom, C. R. Cooper Jr., M. C. Fisher, and T. Sirisanthana Penicillium marneffei Infection and Recent Advances in the Epidemiology and Molecular Biology Aspects Clin. Microbiol. Rev., January 1, 2006; 19(1): 95 - 110. [Abstract] [Full Text] [PDF]
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F. Mirbod-Donovan, R. Schaller, C.-Y. Hung, J. Xue, U. Reichard, and G. T. Cole Urease Produced by Coccidioides posadasii Contributes to the Virulence of This Respiratory Pathogen Infect. Immun., January 1, 2006; 74(1): 504 - 515. [Abstract] [Full Text] [PDF]
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E. J. Tarcha, V. Basrur, C.-Y. Hung, M. J. Gardner, and G. T. Cole A Recombinant Aspartyl Protease of Coccidioides posadasii Induces Protection against Pulmonary Coccidioidomycosis in Mice Infect. Immun., January 1, 2006; 74(1): 516 - 527. [Abstract] [Full Text] [PDF]
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 D. R. Matute, J. G. McEwen, R. Puccia, B. A. Montes, G. San-Blas, E. Bagagli, J. T. Rauscher, A. Restrepo, F. Morais, G. Nino-Vega, et al. Cryptic Speciation and Recombination in the Fungus Paracoccidioides brasiliensis as Revealed by Gene Genealogies Mol. Biol. Evol., January 1, 2006; 23(1): 65 - 73. [Abstract] [Full Text] [PDF]
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non-clinical isolates from armadillo burrows, Brazil. 
‘blind’ duplicated isolates used as genotype controls. 
1932, 1933, and 2030, respectively are isolates of ‘Silveira’ from R. Cox. SILV is an isolate of ‘Silveira’ from D. Pappagianis and shows length mutations at 2 loci compared with 1932, 1933, and 2030. RMSCC 2233A/B were two separate genotypes recovered from a single clinical sample. Z’94, K’97, B’97 and F’00 are references to the original papers that describe genotypes of the isolate (see Appendix)
