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 cycling—typically 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.
Highlights
During the latter half of the 20th century, maritime Antarctica was one of the fastest warming regions on Earth, with increases in near-surface mean annual air temperatures of 1–3°C being recorded between the early 1950s and the turn of the millennium (Adams et al, 2009)
The observations from the field and laboratory experiments reported here collectively indicate that exposure to temperatures exceeding 20°C inhibits the growth and extracellular enzyme activities of P. roseus, the most widespread soil decomposer fungus in maritime Antarctic fellfield soils (Newsham et al, 2016)
The field observations were corroborated by laboratory studies, in which isolates of P. roseus were grown at water potentials and diurnally fluctuating temperatures similar to those occurring in soils in the natural environment
Summary
During the latter half of the 20th century, maritime Antarctica was one of the fastest warming regions on Earth, with increases in near-surface mean annual air temperatures of 1–3°C being recorded between the early 1950s and the turn of the millennium (Adams et al, 2009). The influence of climate change on the metabolism of soil decomposer fungi in the maritime Antarctic natural environment has hitherto received no attention The hyphae of these microbes, microscopic tubular cells that collectively attain lengths of up to 6.3 km g−1 dwt soil in maritime Antarctica (Dowding & Widden, 1974), ramify through soil and dead organic matter, secreting extracellular enzymes that break down organic compounds and release nutrients in forms that can be assimilated by plants and other soil microbes. Given that climate change will force further increases in soil surface temperatures (Fang et al, 2019; Qian et al, 2011), it follows that the exposure of fellfield soils in polar regions to temperatures exceeding 20°C has the potential to influence the future growth and enzyme synthesis of psychrophilic and psychrotrophic microbes, with consequent effects on soil nutrient cycling. We focused on P. roseus because it is the most widespread maritime Antarctic fellfield soil decomposer fungus, with a DNA sequencing study showing it to be the only fungal taxon present in all 29 fellfield soils sampled from along a transect between Signy Island at 60°S and Alexander Island at 72°S (see figure S3 of Newsham et al, 2016), and because allied species in the P. roseus complex (notably Pseudogymnoascus pannorum; Minnis & Lindner, 2013), are psychrotrophs that have frequently been isolated from Antarctic, High Arctic, and alpine soils (e.g., Azmi & Seppelt, 1997; Domsch et al, 2007; Dowding & Widden, 1974; Edgington et al, 2014; Flanagan & Bunnell, 1980; Kerry, 1990; Kirtsideli, 2009; Zucconi et al, 1996)
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