Skip to main content

Advertisement

Log in

Investigating the Role of Animal Burrows on the Ecology and Distribution of Coccidioides spp. in Arizona Soils

  • Original Paper
  • Published:
Mycopathologia Aims and scope Submit manuscript

Abstract

The lack of knowledge regarding the ecology of Coccidioides spp. makes both modeling the potential for disease outbreaks and predicting the distribution of the organism in the environment challenging. No single ecological parameter explains the biogeography of the pathogen. Previous investigations suggest an association with desert mammals, but these results should be confirmed with modern molecular techniques. Therefore, we used molecular tools to analyze soils associated with animal activity (i.e., burrows) to better define the ecology and biogeography of Coccidioides spp. in Arizona. Soils were collected from locations predicted to have favorable habitat outside of the established endemic regions to better understand the ecological niche of the organism in this state. Our central hypothesis is that soils taken from within animal burrows will have a higher abundance of Coccidioides spp. when compared to soils not directly associated with animal burrows. Our results show that there is a positive relationship with Coccidioides spp. and animal burrows. The organism was detected in two locations in northern Arizona at sites not known previously to harbor the fungus. Moreover, this fungus is able to grow on keratinized tissues (i.e., horse hair). These results provide additional evidence that there is a relationship between Coccidioides spp. and desert animals, which sheds new light on Coccidioides’ ecological niche. These results also provide evidence that the geographic range of the organism may be larger than previously thought, and the concept of endemicity should be reevaluated for Coccidioides.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Canteros CE, et al. Genetic characterization of the fungus involved in the first case of coccidioidomycosis described by Alejandro Posadas in 1892. Med B Aires. 2009;69(2):215–20.

    Google Scholar 

  2. Fisher MC, et al. Molecular and phenotypic description of Coccidioides posadasii sp. nov., previously recognized as the non-California population of Coccidioides immitis. Mycologia. 2002;94(1):73–84.

    Article  CAS  PubMed  Google Scholar 

  3. Lee CY, et al. Coccidioides endospores and spherules draw strong chemotactic, adhesive, and phagocytic responses by individual human neutrophils. PLoS one. 2015;10(6):e0129522.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Smith CE, Beard RR, et al. Varieties of coccidioidal infection in relation to the epidemiology and control of the diseases. Am J Public Health Nations Health. 1946;36(12):1394–402.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Thompson GR 3rd, et al. Current concepts and future directions in the pharmacology and treatment of coccidioidomycosis. Med Mycol. 2019;57(Supplement_1):S76–84.

    Article  PubMed  Google Scholar 

  6. Teixeira MM, Barker BM. Use of population genetics to assess the ecology, evolution, and population structure of Coccidioides. Emerg Infect Dis. 2016;22(6):1022–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Altschul SF, et al. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–10.

    Article  CAS  PubMed  Google Scholar 

  8. Engelthaler DM, et al. local population structure and patterns of western hemisphere dispersal for Coccidioides spp., the fungal cause of valley fever. MBio. 2016;7(2):e00550-16.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Emmons C, Ashburn L. The isolation of Haplosporangium parvum n. sp. and Coccidioides immitis from wild rodents. Their relationship to coccidioidomycosis. Public Health Rep. 1942;57(46):1715–27.

    Article  Google Scholar 

  10. Emmons CW. Coccidioidomycosis in wild rodents. A method of determining the extent of endemic areas. Public Health Rep (1896–1970). 1943;58:1–5.

    Article  Google Scholar 

  11. Greene DR, et al. Soil isolation and molecular identification of Coccidioides immitis. Mycologia. 2000;92(3):406–10.

    Article  Google Scholar 

  12. Kolivras KN, Comrie AC. Modeling valley fever (coccidioidomycosis) incidence on the basis of climate conditions. Int J Biometeorol. 2003;47(2):87–101.

    Article  PubMed  Google Scholar 

  13. Sharpton TJ, et al. Comparative genomic analyses of the human fungal pathogens Coccidioides and their relatives. Genome Res. 2009;19(10):1722–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Tamerius JD, Comrie AC. Coccidioidomycosis incidence in Arizona predicted by seasonal precipitation. PLoS one. 2011;6(6):e21009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Untereiner WA, et al. The Ajellomycetaceae, a new family of vertebrate-associated Onygenales. Mycologia. 2004;96(4):812–21.

    Article  PubMed  Google Scholar 

  16. Taylor JW, Barker BM. The endozoan, small-mammal reservoir hypothesis and the life cycle of Coccidioides species. Med Mycol. 2019;57(Supplement_1):S16–20.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Barker BM, et al. Detection and phylogenetic analysis of Coccidioides posadasii in Arizona soil samples. Fungal Ecol. 2012;5(2):163–76.

    Article  Google Scholar 

  18. Cordeiro Rde A, et al. Coccidioides posadasii infection in bats, Brazil. Emerg Infect Dis. 2012;18(4):668–70.

    PubMed  Google Scholar 

  19. Eulalio KD, et al. Coccidioides immitis isolated from armadillos (Dasypus novemcinctus) in the state of Piaui, northeast Brazil. Mycopathologia. 2001;149(2):57.

    Article  CAS  PubMed  Google Scholar 

  20. Fisher FS, et al. Coccidioides niches and habitat parameters in the southwestern United States: a matter of scale. Ann N Y Acad Sci. 2007;1111:47–72.

    Article  PubMed  Google Scholar 

  21. Elconin AF, Egeberg RO, Egeberg MC. Significance of soil salinity on the ecology of Coccidioides immitis. J Bacteriol. 1964;87:500–3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Lacy GH, Swatek FE. Soil ecology of Coccidioides immitis at Amerindian middens in California. Appl Microbiol. 1974;27(2):379–88.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Swatek FE, Omieczynski DT. Isolation and identification of Coccidioides immitis from natural sources. Mycopathol Mycol Appl. 1970;41(1):155–66.

    Article  CAS  PubMed  Google Scholar 

  24. Lauer A, et al. Detection of Coccidioides immitis in Kern County, California, by multiplex PCR. Mycologia. 2012;104(1):62–9.

    Article  CAS  PubMed  Google Scholar 

  25. Chow NA, et al. Molecular detection of airborne Coccidioides in Tucson, Arizona. Med Mycol. 2016;54(6):584–92.

    Article  CAS  PubMed  Google Scholar 

  26. Johnson SM, et al. Demonstration of Coccidioides immitis and Coccidioides posadasii DNA in soil samples collected from Dinosaur National Monument, Utah. Med Mycol. 2014;52(6):610–7.

    Article  PubMed  Google Scholar 

  27. Alvarado P, et al. Detection of Coccidioides posadasii from xerophytic environments in Venezuela reveals risk of naturally acquired coccidioidomycosis infections. Emerg Microbes Infect. 2018;7(1):46.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Baptista-Rosas RC, et al. Molecular detection of Coccidioides spp. from environmental samples in Baja California: linking valley fever to soil and climate conditions. Fungal Ecol. 2012;5(2):177–90.

    Article  Google Scholar 

  29. Bowers JR, et al. Direct detection of Coccidioides from Arizona soils using CocciENV, a highly sensitive and specific real-time PCR assay. Med Mycol. 2019;57(2):246–55.

    Article  CAS  PubMed  Google Scholar 

  30. Saubolle MA, et al. Multicenter clinical validation of a cartridge-based real-time PCR system for detection of Coccidioides spp. in lower respiratory specimens. J Clin Microbiol. 2018;56(2):e01277-17.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Liu CM, et al. FungiQuant: a broad-coverage fungal quantitative real-time PCR assay. BMC Microbiol. 2012;12(1):255.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Litvintseva AP, et al. Valley fever: finding new places for an old disease: Coccidioides immitis found in Washington State soil associated with recent human infection. Clin Infect Dis. 2014;60(1):e1–3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Xie J, et al. Identification of mammalian species using the short and highly variable regions of mitochondrial DNA. Mitochondrial DNA. 2015;26(4):550–4.

    Article  CAS  PubMed  Google Scholar 

  34. Kwon-Chung KJ. Studies on Emmonsiella capsulata. I. heterothallism and development of the ascocarp. Mycologia. 1973;65(1):109–21.

    Article  CAS  PubMed  Google Scholar 

  35. Watson JC. Establishing evidence for internal structure using exploratory factor analysis. Meas Eval Couns Dev. 2017;50(4):232–8.

    Article  Google Scholar 

  36. Colson AJ, et al. Large-scale land development, fugitive dust, and increased coccidioidomycosis incidence in the antelope valley of California, 1999–2014. Mycopathologia. 2017;182(5–6):439–58.

    Article  CAS  PubMed  Google Scholar 

  37. Nguyen C, et al. Recent advances in our understanding of the environmental, epidemiological, immunological, and clinical dimensions of coccidioidomycosis. Clin Microbiol Rev. 2013;26(3):505–25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Edwards PQ, Palmer CE. Prevalence of sensitivity to coccidioidin, with special reference to specific and nonspecific reactions to coccidioidin and to histoplasmin. Dis Chest. 1957;31(1):35–60.

    Article  CAS  PubMed  Google Scholar 

  39. Bennett N, Jarvis J. The reproductive biology of the Cape mole-rat, Georychus capensis (Rodentia, Bathyergidae). J Zool. 1988;214(1):95–106.

    Article  Google Scholar 

  40. Mayer W. The protective value of the burrow system to the hibernating arctic ground squirrel, Spermophilus-undulatus. in anatomical record. Wiley, 605 third ave, New York, NY 10158-0012; 1955.

  41. Kennerly T. Microenvironmental conditions of pocket gopher burrow. Tex J Sci. 1964;16(4):395.

    Google Scholar 

  42. Kay FR, Whitford WG. The burrow environment of the banner-tailed kangaroo rat, Dipodomys spectabilis, in southcentral New Mexico. Am Midl Nat. 1978;99:270–9.

    Article  Google Scholar 

  43. Turnage W. Nocturnal surface-soil temperatures, air temperatures, and ground inversions in southern Arizona. Mon Weather Rev. 1937;65(5):189–90.

    Article  Google Scholar 

  44. Vorhies CT. Water requirements of desert animals in the southwest. Tucson: College of Agriculture, University of Arizona; 1945.

    Google Scholar 

  45. Lewis ER, Bowers JR, Barker BM. Dust devil: the life and times of the fungus that causes valley fever. PLoS Pathog. 2015;11(5):e1004762.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Catalan-Dibene J, et al. Detection of coccidioidal antibodies in serum of a small rodent community in Baja California, Mexico. Fungal Biol. 2014;118(3):330–9.

    Article  PubMed  Google Scholar 

  47. Restrepo A, et al. Clues to the presence of pathogenic fungi in certain environments. Med Mycol. 2000;38(Suppl 1):67–77.

    Article  PubMed  Google Scholar 

  48. Vergara ML, Martinez R. Role of the armadillo Dasypus novemcinctus in the epidemiology of paracoccidioidomycosis. Mycopathologia. 1998;144(3):131–3.

    Article  PubMed  Google Scholar 

  49. Baumgardner DJ, et al. Epidemiology of blastomycosis in a region of high endemicity in north central Wisconsin. Clin Infect Dis. 1992;15(4):629–35.

    Article  CAS  PubMed  Google Scholar 

  50. Baumgardner DJ, Paretsky DP. The in vitro isolation of Blastomyces dermatitidis from a woodpile in north central Wisconsin, USA. Med Mycol. 1999;37(3):163–8.

    Article  CAS  PubMed  Google Scholar 

  51. Chaturvedi VP, et al. In vitro interactions between Blastomyces dermatitidis and other zoopathogenic fungi. Can J Microbiol. 1988;34(7):897–900.

    Article  CAS  PubMed  Google Scholar 

  52. DiSalvo AF. The ecology of Blastomyces dermatitidis, in blastomycosis. Berlin: Springer; 1992. p. 43–73.

    Book  Google Scholar 

  53. Hallmaier-Wacker LK, Munster VJ, Knauf S. Disease reservoirs: from conceptual frameworks to applicable criteria: disease reservoir criteria. Emerg Microbes Infect. 2017;6(1):1–5.

    Article  Google Scholar 

  54. Blanchard R, Blanchard DC, Flannelly KJ. Social stress, mortality and aggression in colonies and burrowing habitats. Behav Process. 1985;11(2):209–13.

    Article  CAS  Google Scholar 

  55. Reichman O, Smith SC. Burrows and burrowing behavior by mammals. Curr Mammal. 1990;2:197–244.

    Google Scholar 

  56. Petrini O. Fungal endophytes of tree leaves, in microbial ecology of leaves. Berlin: Springer; 1991. p. 179–97.

    Book  Google Scholar 

  57. Baumgardner DJ. Soil-related bacterial and fungal infections. J Am Board Fam Med. 2012;25(5):734–44.

    Article  PubMed  Google Scholar 

  58. Andreou D, Gozlan RE. Associated disease risk from the introduced generalist pathogen Sphaerothecum destruens: management and policy implications. Parasitology. 2016;143(9):1204–10.

    Article  PubMed  Google Scholar 

  59. Holmes JC. Parasite populations and host community structure. In: Nickol BB, editor. Host-parasite interfaces. New York: Academic Press; 1979. p. 27–46.

    Google Scholar 

  60. Solter LF, Maddox JV. Physiological host specificity of microsporidia as an indicator of ecological host specificity. J Invertebr Pathol. 1998;71(3):207–16.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Thanks to Austin Blackmon and Kaitlyn Parra for technical support. Thanks to Dr. David Wagner and Dr. Matthew Bowker for advisement and consultation throughout this study. This work was supported by an Arizona Biomedical Research Centre grant (ABRC 16-162415) to BMB.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bridget M. Barker.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest. This article does not contain any studies with human participants or animals performed by any of the authors. Informed consent was obtained from all individual participants included in the study.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Handling Editor: Sybren deHoog.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kollath, D.R., Teixeira, M.M., Funke, A. et al. Investigating the Role of Animal Burrows on the Ecology and Distribution of Coccidioides spp. in Arizona Soils. Mycopathologia 185, 145–159 (2020). https://doi.org/10.1007/s11046-019-00391-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11046-019-00391-2

Keywords

Navigation