Angiosperm symbioses with non-mycorrhizal fungal partners enhance N acquisition from ancient organic matter in a warming maritime Antarctic

Paul W Hill, Richard Broughton, Jeremy Bougoure, William Havelange, Kevin K Newsham, Helen Grant, Daniel V Murphy, Peta Clode, Soshila Ramayah, Karina A Marsden, Richard S Quilliam, Paula Roberts, Caley Brown, David J Read, Thomas H DeLuca, Richard D Bardgett, DW Hopkins, Davey Leonard Jones

Research output: Contribution to journalLetter

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Abstract

In contrast to the situation in plants inhabiting most of the world’s ecosystems, mycorrhizal fungi are usually absent from roots of the only two native vascular plant species of maritime Antarctica, Deschampsia antarctica and Colobanthus quitensis. Instead, a range of ascomycete fungi, termed dark septate endophytes (DSEs), frequently colonise the roots of these plant species. We demonstrate that colonisation of Antarctic vascular plants by DSEs facilitates not only the acquisition of organic nitrogen as early protein breakdown products, but also as non-proteinaceous D-amino acids and their short peptides, accumulated in slowly-decomposing organic matter, such as moss peat. Our findings suggest that, in a warming maritime Antarctic, this symbiosis has a key role in accelerating the replacement of formerly dominant moss communities by vascular plants, and in increasing the rate at which ancient carbon stores laid down as moss peat over centuries or millennia are returned to the atmosphere as CO2.
Original languageEnglish
Pages (from-to)2111-2119
Number of pages9
JournalEcology Letters
Volume22
Issue number12
Early online date17 Oct 2019
DOIs
Publication statusFirst published - 17 Oct 2019

Fingerprint

symbiosis
vascular plant
angiosperm
vascular plants
moss
Angiospermae
endophyte
warming
Sphagnum
organic matter
endophytes
peat
Deschampsia antarctica
fungus
organic nitrogen
carbon sinks
Ascomycota
peptide
Antarctica
mycorrhizal fungi

Keywords

  • Soil
  • Nitrogen cycle
  • Carbon cycle
  • Climate change
  • Enantiomers
  • Polar
  • Dark septate endophytes

Cite this

Hill, P. W., Broughton, R., Bougoure, J., Havelange, W., Newsham, K. K., Grant, H., ... Jones, D. L. (2019). Angiosperm symbioses with non-mycorrhizal fungal partners enhance N acquisition from ancient organic matter in a warming maritime Antarctic. Ecology Letters, 22(12), 2111-2119. https://doi.org/10.1111/ele.13399
Hill, Paul W ; Broughton, Richard ; Bougoure, Jeremy ; Havelange, William ; Newsham, Kevin K ; Grant, Helen ; Murphy, Daniel V ; Clode, Peta ; Ramayah, Soshila ; Marsden, Karina A ; Quilliam, Richard S ; Roberts, Paula ; Brown, Caley ; Read, David J ; DeLuca, Thomas H ; Bardgett, Richard D ; Hopkins, DW ; Jones, Davey Leonard. / Angiosperm symbioses with non-mycorrhizal fungal partners enhance N acquisition from ancient organic matter in a warming maritime Antarctic. In: Ecology Letters. 2019 ; Vol. 22, No. 12. pp. 2111-2119.
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title = "Angiosperm symbioses with non-mycorrhizal fungal partners enhance N acquisition from ancient organic matter in a warming maritime Antarctic",
abstract = "In contrast to the situation in plants inhabiting most of the world’s ecosystems, mycorrhizal fungi are usually absent from roots of the only two native vascular plant species of maritime Antarctica, Deschampsia antarctica and Colobanthus quitensis. Instead, a range of ascomycete fungi, termed dark septate endophytes (DSEs), frequently colonise the roots of these plant species. We demonstrate that colonisation of Antarctic vascular plants by DSEs facilitates not only the acquisition of organic nitrogen as early protein breakdown products, but also as non-proteinaceous D-amino acids and their short peptides, accumulated in slowly-decomposing organic matter, such as moss peat. Our findings suggest that, in a warming maritime Antarctic, this symbiosis has a key role in accelerating the replacement of formerly dominant moss communities by vascular plants, and in increasing the rate at which ancient carbon stores laid down as moss peat over centuries or millennia are returned to the atmosphere as CO2.",
keywords = "Soil, Nitrogen cycle, Carbon cycle, Climate change, Enantiomers, Polar, Dark septate endophytes",
author = "Hill, {Paul W} and Richard Broughton and Jeremy Bougoure and William Havelange and Newsham, {Kevin K} and Helen Grant and Murphy, {Daniel V} and Peta Clode and Soshila Ramayah and Marsden, {Karina A} and Quilliam, {Richard S} and Paula Roberts and Caley Brown and Read, {David J} and DeLuca, {Thomas H} and Bardgett, {Richard D} and DW Hopkins and Jones, {Davey Leonard}",
year = "2019",
month = "10",
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doi = "10.1111/ele.13399",
language = "English",
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journal = "Ecology Letters",
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Hill, PW, Broughton, R, Bougoure, J, Havelange, W, Newsham, KK, Grant, H, Murphy, DV, Clode, P, Ramayah, S, Marsden, KA, Quilliam, RS, Roberts, P, Brown, C, Read, DJ, DeLuca, TH, Bardgett, RD, Hopkins, DW & Jones, DL 2019, 'Angiosperm symbioses with non-mycorrhizal fungal partners enhance N acquisition from ancient organic matter in a warming maritime Antarctic', Ecology Letters, vol. 22, no. 12, pp. 2111-2119. https://doi.org/10.1111/ele.13399

Angiosperm symbioses with non-mycorrhizal fungal partners enhance N acquisition from ancient organic matter in a warming maritime Antarctic. / Hill, Paul W; Broughton, Richard; Bougoure, Jeremy; Havelange, William; Newsham, Kevin K; Grant, Helen; Murphy, Daniel V; Clode, Peta; Ramayah, Soshila; Marsden, Karina A; Quilliam, Richard S; Roberts, Paula; Brown, Caley; Read, David J; DeLuca, Thomas H; Bardgett, Richard D; Hopkins, DW; Jones, Davey Leonard.

In: Ecology Letters, Vol. 22, No. 12, 12.2019, p. 2111-2119.

Research output: Contribution to journalLetter

TY - JOUR

T1 - Angiosperm symbioses with non-mycorrhizal fungal partners enhance N acquisition from ancient organic matter in a warming maritime Antarctic

AU - Hill, Paul W

AU - Broughton, Richard

AU - Bougoure, Jeremy

AU - Havelange, William

AU - Newsham, Kevin K

AU - Grant, Helen

AU - Murphy, Daniel V

AU - Clode, Peta

AU - Ramayah, Soshila

AU - Marsden, Karina A

AU - Quilliam, Richard S

AU - Roberts, Paula

AU - Brown, Caley

AU - Read, David J

AU - DeLuca, Thomas H

AU - Bardgett, Richard D

AU - Hopkins, DW

AU - Jones, Davey Leonard

PY - 2019/10/17

Y1 - 2019/10/17

N2 - In contrast to the situation in plants inhabiting most of the world’s ecosystems, mycorrhizal fungi are usually absent from roots of the only two native vascular plant species of maritime Antarctica, Deschampsia antarctica and Colobanthus quitensis. Instead, a range of ascomycete fungi, termed dark septate endophytes (DSEs), frequently colonise the roots of these plant species. We demonstrate that colonisation of Antarctic vascular plants by DSEs facilitates not only the acquisition of organic nitrogen as early protein breakdown products, but also as non-proteinaceous D-amino acids and their short peptides, accumulated in slowly-decomposing organic matter, such as moss peat. Our findings suggest that, in a warming maritime Antarctic, this symbiosis has a key role in accelerating the replacement of formerly dominant moss communities by vascular plants, and in increasing the rate at which ancient carbon stores laid down as moss peat over centuries or millennia are returned to the atmosphere as CO2.

AB - In contrast to the situation in plants inhabiting most of the world’s ecosystems, mycorrhizal fungi are usually absent from roots of the only two native vascular plant species of maritime Antarctica, Deschampsia antarctica and Colobanthus quitensis. Instead, a range of ascomycete fungi, termed dark septate endophytes (DSEs), frequently colonise the roots of these plant species. We demonstrate that colonisation of Antarctic vascular plants by DSEs facilitates not only the acquisition of organic nitrogen as early protein breakdown products, but also as non-proteinaceous D-amino acids and their short peptides, accumulated in slowly-decomposing organic matter, such as moss peat. Our findings suggest that, in a warming maritime Antarctic, this symbiosis has a key role in accelerating the replacement of formerly dominant moss communities by vascular plants, and in increasing the rate at which ancient carbon stores laid down as moss peat over centuries or millennia are returned to the atmosphere as CO2.

KW - Soil

KW - Nitrogen cycle

KW - Carbon cycle

KW - Climate change

KW - Enantiomers

KW - Polar

KW - Dark septate endophytes

U2 - 10.1111/ele.13399

DO - 10.1111/ele.13399

M3 - Letter

C2 - 31621153

VL - 22

SP - 2111

EP - 2119

JO - Ecology Letters

JF - Ecology Letters

SN - 1461-023X

IS - 12

ER -