Evidence that chytrids dominate fungal communities in high-elevation soils

Abstract

Periglacial soils are one of the least studied ecosystems on Earth, yet they are widespread and are increasing in area due to retreat of glaciers worldwide. Soils in these environments are cold and during the brief summer are exposed to high levels of UV radiation and dramatic fluctuations in moisture and temperature. Recent research suggests that these environments harbor immense microbial diversity. Here we use sequencing of environmental DNA, culturing of isolates, and analysis of environmental variables to show that members of the Chytridiomycota (chytrids) dominate fungal biodiversity and perhaps decomposition processes in plant-free, high-elevation soils from the highest mountain ranges on Earth. The zoosporic reproduction of chytrids requires free water, yet we found that chytrids constituted over 70% of the ribosomal gene sequences of clone libraries from barren soils of the Himalayas and Rockies; by contrast, they are rare in other soil environments. Very few chytrids have been cultured, although we were successful at culturing chytrids from high-elevation sites throughout the world. In a more focused study of our sites in Colorado, we show that carbon sources that support chytrid growth (eolian deposited pollen and microbial phototrophs) are abundant and that soils are saturated with water for several months under the snow, thus creating ideal conditions for the development of a chytrid-dominated ecosystem. Our work broadens the known biodiversity of the Chytridomycota, and describes previously unsuspected links between aquatic and terrestrial ecosystems in alpine regions.

Fig. 1.

Percent relative abundance of chytrid phylotypes in fungal clone libraries from soils collected across a range of environments. More than 60% of phylotypes from our Nepal and Colorado unvegetated, high-elevation soils were chytrids, whereas in all other environments chytrids comprised less than 10% of fungi. P1 and P2 represent different primer sets used at our sites in Colorado. Error bars are standard error of the mean of spatially separated replicates from a given environment. Data for other sites were obtained from the literature: subtropical forest and plantation (12), Antarctic dry (38), dry volcano (4), alpine dry meadow (39), four land-use types in Southeast USA (10), Arctic shrub (26), alpine dry meadow 2 (11), wheat rhizosphere (14), volcanic wetland (4), U.K. grassland (17), soybean field (40), intertussock and tussock tundra (26), Antarctic moist and wet (38). For our data, fungi comprised 45% and 36% of all eukaryotic sequences obtained from Colorado and Nepal, respectively. In contrast, in the only other study that reported similar data for soils, fungi comprised only 9% of the total eukaryotes (4).

Fig. 2.

Inferred phylogenetic relationships of sequences obtained from cultures and clone libraries in the present study compared to the known diversity of major groups of chytrids. (A) shows clades C1–C11; sequences in these clades are most closely related to the orders Spizellomycetales and Rhizophlyctidales. (B) clades C12–C14, sequences in these clades are most closely related to the order Chytridiales. (C) clades C15–C21; sequences in these clades are most closely related to the order Rhizophydiales. Black arrows indicate where on the tree the other groups of chytrids attach. An overview of how the major groups of chytrids link to one another is presented in Fig. S1. Bootstrap values are indicated at nodes above 90%; numbered clades had bootstrap support of at least 90% and/or branch lengths of subtending clades long enough to warrant separate discussion (>1% sequence evolution). An asterisk indicates those clades that include a cultured isolate reported in this study.

Fig. 2.

Inferred phylogenetic relationships of sequences obtained from cultures and clone libraries in the present study compared to the known diversity of major groups of chytrids. (A) shows clades C1–C11; sequences in these clades are most closely related to the orders Spizellomycetales and Rhizophlyctidales. (B) clades C12–C14, sequences in these clades are most closely related to the order Chytridiales. (C) clades C15–C21; sequences in these clades are most closely related to the order Rhizophydiales. Black arrows indicate where on the tree the other groups of chytrids attach. An overview of how the major groups of chytrids link to one another is presented in Fig. S1. Bootstrap values are indicated at nodes above 90%; numbered clades had bootstrap support of at least 90% and/or branch lengths of subtending clades long enough to warrant separate discussion (>1% sequence evolution). An asterisk indicates those clades that include a cultured isolate reported in this study.

Fig. 3.

Soil temperature and moisture data (4 cm depth) from a typical year at our Colorado sites. Soils are saturated for several months under the melting snowpack, ideal conditions for the growth of chytrids. In contrast, the short summer period was dry with large, diurnal temperature fluctuations. The spike in soil water at the end of the snow-covered period was due to a large rainfall event that washed away the remaining snowpack (8).