Inhibitory effects of climate change on the growth and extracellular enzyme activities of a widespread Antarctic soil fungus

Abstract

Temperatures approaching or exceeding 20°C have been measured during summer in polar regions at the surfaces of barren fellfield soils under cloudless skies around solar noon. However, despite the upper temperature limit for the growth of cold-adapted microbes-which are abundant in polar soils and have pivotal roles in nutrient cyclingtypically being close to this temperature, previous studies have not addressed the consequences of climate change for the metabolism of these organisms in the natural environment. Here in a 5-year field experiment on Alexander Island in the southern maritime Antarctic, we show that the abundance of Pseudogymnoascus roseus, the most widespread decomposer fungus in maritime Antarctic fellfield soils, is reduced by 1-2 orders of magnitude when irrigated and nutrient-amended soils are warmed to >20°C during summer. Laboratory experiments under conditions mimicking those during midsummer in the natural environment indicated that the hyphal extension rates of P. roseus isolates and the activities of five extracellular enzymes are reduced by 54%-96% at high water availability after exposure to temperatures cycling daily from 2 to 21°C and 2 to 24°C, relative to temperatures cycling from 2 to 18°C. Given that the temperatures of surface soils at the study site already reach 19°C during midsummer, the observations reported here suggest that, at predicted rates of warming arising from moderate greenhouse gas emissions, inhibitory effects of climate change on the metabolism of P. roseus could manifest themselves within the next few decades. Furthermore, with peak temperatures at the surfaces of fellfield soils at other maritime Antarctic locations and in High Arctic and alpine regions already exceeding 20°C during summer, the observations suggest that climate warming has the potential to inhibit the growth of other cold-adapted microbes, with negative effects on soils as the Earth's climate continues to warm.

Environmental effects of stratospheric ozone depletion, UV radiation, and interactions with climate change: UNEP Environmental Effects Assessment Panel, Update 2021

“…In Polar Regions, variability and trends in the downward coupling from the stratosphere to the troposphere have contributed to changes in climate patterns on seasonal and interannual time scales [4,7,94,95]. In Antarctica, interaction between stratospheric ozone change and the strength of the dynamical coupling from the stratosphere may be partially responsible at a regional scale for trends in surface temperature and precipitation, placing the stability of these fragile ecosystems at risk [96][97][98][99][100][101]. There is also concern that changes in atmospheric circulation patterns may lead to more sustained periods of cold winter and spring temperatures from mid-latitudes to Polar Regions [19], which could delay growth and reproduction until later in the year, thereby increasing the exposure to UV radiation of young leaves and buds.…”

Biosynthetic potential of uncultured Antarctic soil bacteria revealed through long-read metagenomic sequencing

“…During midwinter, the temperatures of surface soils decline to −32°C. Mean annual air temperature is c. −10°C [31].…”

Towards understanding diversity, endemicity and global change vulnerability of soil fungi

“…Patterns of vulnerability in fungi are somewhat similar to those of terrestrial plants and animals, where vulnerability peaks in drylands prone to desertification (Warren et al 2013), arctic/alpine areas (cold-adapted species), and regions with dense human populations (Watson et al 2013). The relatively low vulnerability to heat in tundra-inhabiting fungi can be explained by their relatively high temperature optima (Maynard et al 2019; but see Misiak et al 2021), acclimation (Romero-Olivares et al 2017), and poleward migration potential, despite relatively greater predicted warming in Arctic ecosystems. Above certain tolerance thresholds, soil organisms may be physiologically constrained by increasing soil temperature and evaporation, lower soil water potentials, and loss of oxygen due to greater respiration and faster decomposition, which result in hampered soil functioning and ecosystem multifunctionality (Delgado-Baquerizo et al 2017).…”

“…As for plants and animals, soil fungal communities are likely vulnerable to global change drivers. For instance, high-temperature stress (Malcolm et al 2008; Barcenas-Moreno et al 2009; Morgado et al 2015; Misiak et al 2021) and prolonged drought (Schmidt et al 2017; de Vries et al 2018) can alter fungal growth, functionality and community composition. Likewise, changes in land use that result in habitat fragmentation may lead to shifts in prevalence of pathogenic, mutualistic, and free-living fungal groups (Brinkmann et al 2019; Makiola et al 2019; Le Provost et al 2021; Rodriguez-Ramos et al 2021).…”