Coccidioides undetected in soils from agricultural land and uncorrelated with time or the greater soil fungal community on undeveloped land

Abstract

Coccidioidomycosis is a typically respiratory fungal disease that, in the United States, occurs primarily in Arizona and California. In California, most coccidioidomycosis cases occur in the San Joaquin Valley, a primarily agricultural region where the disease poses a risk for outdoor workers. We collected 710 soil samples and 265 settled dust samples from nine sites in the San Joaquin Valley and examined how Coccidioides detection varied by month, site, and the presence and abundance of other fungal species. We detected Coccidioides in 89 of 238 (37.4%) rodent burrow soil samples at five undeveloped sites and were unable to detect Coccidioides in any of 472 surface and subsurface soil samples at four agricultural sites. In what is the largest sampling effort undertaken on agricultural land, our results provide no evidence that agricultural soils in the San Joaquin Valley harbor Coccidioides. We found no clear association between Coccidioides and the greater soil fungal community, but we identified 19 fungal indicator species that were significantly associated with Coccidioides detection in burrows. We also did not find a seasonal pattern in Coccidioides detection in the rodent burrow soils we sampled. These findings suggest both the presence of a spore bank and that coccidioidomycosis incidence may be more strongly associated with Coccidioides dispersal than Coccidioides growth. Finally, we were able to detect Coccidioides in only five of our 265 near-surface settled dust samples, one from agricultural land, where Coccidioides was undetected in soils, and four from undeveloped land, where Coccidioides was common in the rodent burrow soils we sampled. Our ability to detect Coccidioides in few settled dust samples indicates that improved methods are likely needed moving forward, though raises questions regarding aerial dispersal in Coccidioides, whose key transmission event likely occurs over short distances in rodent burrows from soil to naïve rodent lungs. Valley fever (coccidioidomycosis) is a fungal disease of humans that, in California, most commonly occurs in the San Joaquin Valley. Valley fever is caused by infection with Coccidioides fungi, of which nearly all cases occur though inhalation of airborne spores. Many cases of Valley fever in the San Joaquin Valley occur amongst agricultural workers, though only one other study has attempted to detect Coccidioides in agricultural soils. Furthermore, Valley fever cases follow a seasonal pattern, though no other work has determined whether the abundance of Coccidioides fungi in the environment follows a similar pattern. Here, we undertake what is the largest survey of Coccidioides amongst agricultural soils. Additionally, we provide the most comprehensive monthly survey of Coccidioides, spanning an entire year, amongst soils in the natural environment, namely, within rodent burrows, an environment where Coccidioides is commonly found. We were unable to detect Coccidioides in any of the agricultural soils we sampled, nor did we find a seasonal pattern in Coccidioides detection in the rodent burrow soils we sampled on undeveloped land. Finally, we found few associations between Coccidioides and other soil fungi, and no significant association with the structure of the greater soil fungal community. Taken together, our findings challenge assumptions regarding the prevalence of Coccidioides in agricultural soils and the relative importance of seasonal growth versus dispersal of Coccidioides in the environment.