Abstract

We report a previously undescribed member of the Helotiales that is superabundant in soils at two maritime Antarctic islands under Antarctic Hairgrass (Deschampsia antarctica Desv.). High throughput sequencing showed that up to 92% of DNA reads, and 68% of RNA reads, in soils from the islands were accounted for by the fungus. Sequencing of the large subunit region of ribosomal (r)DNA places the fungus close to the Pezizellaceae, Porodiplodiaceae, and Sclerotiniaceae, with analyses of internal transcribed spacer regions of rDNA indicating that it has affinities to previously unnamed soil and root fungi from alpine, cool temperate and Low Arctic regions. The fungus was found to be most frequent in soils containing C aged to 1,000–1,200 years before present. The relative abundances of its DNA and RNA reads were positively associated with soil carbon and nitrogen concentrations and δ13C values, with the relative abundance of its DNA being negatively associated with soil pH value. An isolate of the fungus produces flask-shaped phialides with a pronounced venter bearing masses of conidia measuring 4.5–6(7) × 1.8–2.5 μm, suggestive of anamorphic Chalara. Enzymatic studies indicate that the isolate strongly synthesizes the extracellular enzyme acid phosphatase, and also exhibits alkaline phosphatase and naphthol-AS-BI-phosphohydrolase activities. Ecophysiological measurements indicate optimal hyphal growth of the isolate at a pH of 4.2–4.5 and a water potential of −0.66 MPa. The isolate is a psychrotroph, exhibiting measureable hyphal growth at −2°C, optimal hyphal extension rate at 15°C and negligible growth at 25°C. It is proposed that the rising temperatures that are predicted to occur in maritime Antarctica later this century will increase the growth rate of the fungus, with the potential loss of ancient C from soils. Analyses using the GlobalFungi Database indicate that the fungus is present in cold, acidic soils on all continents. We advocate further studies to identify whether it is superabundant in soils under D. antarctica elsewhere in maritime Antarctica, and for further isolates to be obtained so that the species can be formally described.

Highlights

  • Antarctica has been neglected in global mass sequencing studies of soil fungi (Tedersoo et al, 2014; Bahram et al, 2018; Egidi et al, 2019; Vetrovský et al, 2019), several features are starting to emerge of the fungal communities found in the soils that form on the continent (Bockheim, 2015)

  • RNA of the fungus was detected in 43 out of 45 libraries constructed from Signy Island soil, but at a much lower relative abundance than in DNA libraries, and its RNA was detected in 36 of the 45 RNA libraries from Léonie Island, with a mean relative abundance of 17%

  • The competitive abilities of the fungus reported here have yet to be tested, it strongly synthesizes extracellular enzymes for carbohydrate breakdown (Newsham et al, 2018), and it is abundant and active in soils that are frozen for c. 8 months per annum (Convey et al, 2018) and which are exposed to annual temperature ranges of 48◦C and midwinter temperatures below −20◦C (Bokhorst et al, 2011), suggesting that it expresses stress tolerance genes

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Summary

Introduction

Antarctica has been neglected in global mass sequencing studies of soil fungi (Tedersoo et al, 2014; Bahram et al, 2018; Egidi et al, 2019; Vetrovský et al, 2019), several features are starting to emerge of the fungal communities found in the soils that form on the continent (Bockheim, 2015). Vetrovský et al, 2019), which are associated with decreasing air temperature and, most probably, liquid water availability (Newsham et al, 2016). Perhaps surprisingly for such an isolated continent, another feature of the fungal communities in Antarctic soils is that they exhibit low endemism, with many taxa either having cosmopolitan or bipolar distributions (Cox et al, 2016). Fungi in the class Leotiomycetes and the order Helotiales are frequent in the roots of Antarctic Hairgrass (Deschampsia antarctica), one of the only two native Antarctic higher plant species, and in the soils that form under the grass (Upson et al, 2009; Cox et al, 2016, 2019)

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