A Previously Undescribed Helotialean Fungus That Is Superabundant in Soil Under Maritime Antarctic Higher Plants

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 a...

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Main Authors: Kevin K. Newsham, Filipa Cox, Chester J. Sands, Mark H. Garnett, Naresh Magan, Claire A. Horrocks, Jennifer A. J. Dungait, Clare H. Robinson
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-12-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2020.615608/full
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author Kevin K. Newsham
Filipa Cox
Filipa Cox
Chester J. Sands
Mark H. Garnett
Naresh Magan
Claire A. Horrocks
Jennifer A. J. Dungait
Clare H. Robinson
author_facet Kevin K. Newsham
Filipa Cox
Filipa Cox
Chester J. Sands
Mark H. Garnett
Naresh Magan
Claire A. Horrocks
Jennifer A. J. Dungait
Clare H. Robinson
author_sort Kevin K. Newsham
collection DOAJ
description 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.
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spelling doaj.art-95b284a43df046648720aa8c98df04692022-12-21T22:51:46ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-12-011110.3389/fmicb.2020.615608615608A Previously Undescribed Helotialean Fungus That Is Superabundant in Soil Under Maritime Antarctic Higher PlantsKevin K. Newsham0Filipa Cox1Filipa Cox2Chester J. Sands3Mark H. Garnett4Naresh Magan5Claire A. Horrocks6Jennifer A. J. Dungait7Clare H. Robinson8British Antarctic Survey, Natural Environment Research Council, Cambridge, United KingdomBritish Antarctic Survey, Natural Environment Research Council, Cambridge, United KingdomDepartment of Earth and Environmental Sciences, The University of Manchester, Manchester, United KingdomBritish Antarctic Survey, Natural Environment Research Council, Cambridge, United KingdomNational Environmental Isotope Facility Radiocarbon Laboratory, Glasgow, United KingdomApplied Mycology Group, Environment and AgriFood Theme, Cranfield University, Cranfield, United KingdomSustainable Agriculture Sciences, Rothamsted Research, Okehampton, United KingdomSustainable Agriculture Sciences, Rothamsted Research, Okehampton, United KingdomDepartment of Earth and Environmental Sciences, The University of Manchester, Manchester, United KingdomWe 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.https://www.frontiersin.org/articles/10.3389/fmicb.2020.615608/fullAntarctica14C (or carbon-14)carbon13CChalaraHelotiales
spellingShingle Kevin K. Newsham
Filipa Cox
Filipa Cox
Chester J. Sands
Mark H. Garnett
Naresh Magan
Claire A. Horrocks
Jennifer A. J. Dungait
Clare H. Robinson
A Previously Undescribed Helotialean Fungus That Is Superabundant in Soil Under Maritime Antarctic Higher Plants
Frontiers in Microbiology
Antarctica
14C (or carbon-14)
carbon
13C
Chalara
Helotiales
title A Previously Undescribed Helotialean Fungus That Is Superabundant in Soil Under Maritime Antarctic Higher Plants
title_full A Previously Undescribed Helotialean Fungus That Is Superabundant in Soil Under Maritime Antarctic Higher Plants
title_fullStr A Previously Undescribed Helotialean Fungus That Is Superabundant in Soil Under Maritime Antarctic Higher Plants
title_full_unstemmed A Previously Undescribed Helotialean Fungus That Is Superabundant in Soil Under Maritime Antarctic Higher Plants
title_short A Previously Undescribed Helotialean Fungus That Is Superabundant in Soil Under Maritime Antarctic Higher Plants
title_sort previously undescribed helotialean fungus that is superabundant in soil under maritime antarctic higher plants
topic Antarctica
14C (or carbon-14)
carbon
13C
Chalara
Helotiales
url https://www.frontiersin.org/articles/10.3389/fmicb.2020.615608/full
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