Seasonal variation and potential roles of dark septate fungi in an arid grassland

ABSTRACT

High temperatures and extended drought in temperate and tropical arid ecosystems promote the colonization of diverse microenvironments by dark septate fungi (DSF). These fungi contribute to soil nutrient cycling, soil stabilization, and plant survival, but the roles of individual DSF species, their distributions, and their community diversity are poorly understood. The objective of this study was to evaluate the distribution, seasonal variation, and potential roles of DSF on plant growth. We collected biocrust (lichen-, moss-, and cyanobacterium-dominated biocrusts) soils at different depths and rhizosphere soils from two grasses, Bromus tectorum and Pleuraphis jamesii, in an arid grassland near Moab, Utah, USA. Seasonal variation of DSF was evaluated using culture-based approaches and compared with fungal community profiles from next-generation sequencing (NGS). Culturing showed that DSF were 30% more abundant in biocrusts compared with the focal rhizospheres. The abundance of DSF varied seasonally in belowground samples (rhizosphere and below-biocrust), with a significant increase during the summer months. Pleosporales was the dominant order (35%) in both biocrust and rhizosphere soils out of 817 isolated fungi. Dominant DSF genera in culture included Alternaria, Preussia, Cladosporium, Phoma, and an unknown Pleosporales. Similar results were observed in biocrust and rhizosphere soils NGS. Further, seed germination experiments using dominant taxa were conducted to determine their potential roles on germination and seedling growth using maize as a model plant. Cladosporium and unknown Pleosporales isolates showed plant growth–promoting ability. The variation in abundance of DSF, their differential occurrence in different microenvironments, and their ability to grow in a xerotolerant medium reflect adaptations to summer environmental conditions and to changes in the abundance of organic matter, as well as a potential increase in plant investment in these fungi when heat and drought stresses are more severe.

KEYWORDS:

• Biocrusts
• Cladosporium
• drylands
• endophytes
• plant growth
• Pleosporales

ACKNOWLEDGMENTS

We thank Dr. Mike Romano and Dr. Esteban Araya for their support in data analysis and Terri Tobias and Katrina Sandona for their support in establishing culture collections.

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Funding

Support for this project was provided by the U.S. Department of Energy (DOE) Biological and Environmental Research Division through a Science Focus Area grant to C.R.K. (LA-UR-18_24858). This project was also supported by the National Science Foundation (BIO-DEB-PCE 1457002). Funding was also provided to Cedric Ndinga Muniania by the Western Illinois University (WIU) College of Arts and Sciences and the WIU Graduate College, the Research Inspiring Student Excellence (RISE), and the Mycological Society of America. This material is based upon work supported by the National Science Foundation (A.P.-A.). Any opinion, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation.