Assessing soil microbes that drive fairy ring patterns in temperate semiarid grasslands

Abstract Background Fairy rings occur in diverse global biomes; however, there is a critical knowledge gap regarding drivers of fairy rings in grassland ecosystems. Grassland fairy rings are characterized belowground by an expanding mycelial front and aboveground by vigorous vegetation rings that de...

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Main Authors: Jiahuan Li, Lizhu Guo, Gail W. T. Wilson, Adam B. Cobb, Kun Wang, Li Liu, Huan Zhao, Ding Huang
Format: Article
Language:English
Published: BMC 2022-11-01
Series:BMC Ecology and Evolution
Subjects:
Online Access:https://doi.org/10.1186/s12862-022-02082-x
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author Jiahuan Li
Lizhu Guo
Gail W. T. Wilson
Adam B. Cobb
Kun Wang
Li Liu
Huan Zhao
Ding Huang
author_facet Jiahuan Li
Lizhu Guo
Gail W. T. Wilson
Adam B. Cobb
Kun Wang
Li Liu
Huan Zhao
Ding Huang
author_sort Jiahuan Li
collection DOAJ
description Abstract Background Fairy rings occur in diverse global biomes; however, there is a critical knowledge gap regarding drivers of fairy rings in grassland ecosystems. Grassland fairy rings are characterized belowground by an expanding mycelial front and aboveground by vigorous vegetation rings that develop concentrically with each growing season. We evaluated fairy ring dynamics in a field study conducted in semiarid grasslands to elucidate above- and belowground interactions driving distinct vegetation patterns. We followed this initial field investigation with a complementary greenhouse experiment, using soils collected from specific fairy ring zones (inside, ring-edge, outside) to examine plant-soil-microbial interactions under controlled conditions. We selected Leymus chinensis (a dominant grass) as our model plant species to assess the role of diverse fairy ring microbial communities on plant growth and nutrition. Results In our field study, plants on the ring-edge produced greater shoot biomass with higher concentrations of N and P, compared to plants inside the ring or adjacent (outside) controls. Soil microbial community biomarkers indicate shifts in relative microbial biomass as fairy rings expand. Inside the ring, plant roots showed greater damage from pathogenic fungi, compared to outside or ring-edge. Our greenhouse experiment confirmed that inoculation with live ring-edge soil generally promoted plant growth but decreased shoot P concentration. Inoculation with soil collected from inside the ring increased root pathogen infection and reduced shoot biomass. Conclusion We propose that soil microbial activity within ring-edges promotes plant growth via mobilization of plant-available P or directed stimulation. However, as the ring expands, L. chinensis at the leading edge may increase pathogen accumulation, resulting in reduced growth at the center of the ring in subsequent growing seasons. Our results provide new insights into the plant-soil-microbial dynamics of fairy rings in grasslands, helping to elucidate these mysterious vegetation patterns.
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spelling doaj.art-3a478a3ce8eb421d9a07893f55057dc72022-12-22T04:38:22ZengBMCBMC Ecology and Evolution2730-71822022-11-0122111310.1186/s12862-022-02082-xAssessing soil microbes that drive fairy ring patterns in temperate semiarid grasslandsJiahuan Li0Lizhu Guo1Gail W. T. Wilson2Adam B. Cobb3Kun Wang4Li Liu5Huan Zhao6Ding Huang7College of Grassland Science and Technology, West Campus of China Agricultural UniversityInstitute of Grassland, Flowers and Ecology, Beijing Academy of Agriculture and Forestry SciencesOklahoma State UniversityOklahoma State UniversityCollege of Grassland Science and Technology, West Campus of China Agricultural UniversityCollege of Grassland Science and Technology, West Campus of China Agricultural UniversityAcademy of Inventory and Planning, National Forestry and Grassland AdministrationCollege of Grassland Science and Technology, West Campus of China Agricultural UniversityAbstract Background Fairy rings occur in diverse global biomes; however, there is a critical knowledge gap regarding drivers of fairy rings in grassland ecosystems. Grassland fairy rings are characterized belowground by an expanding mycelial front and aboveground by vigorous vegetation rings that develop concentrically with each growing season. We evaluated fairy ring dynamics in a field study conducted in semiarid grasslands to elucidate above- and belowground interactions driving distinct vegetation patterns. We followed this initial field investigation with a complementary greenhouse experiment, using soils collected from specific fairy ring zones (inside, ring-edge, outside) to examine plant-soil-microbial interactions under controlled conditions. We selected Leymus chinensis (a dominant grass) as our model plant species to assess the role of diverse fairy ring microbial communities on plant growth and nutrition. Results In our field study, plants on the ring-edge produced greater shoot biomass with higher concentrations of N and P, compared to plants inside the ring or adjacent (outside) controls. Soil microbial community biomarkers indicate shifts in relative microbial biomass as fairy rings expand. Inside the ring, plant roots showed greater damage from pathogenic fungi, compared to outside or ring-edge. Our greenhouse experiment confirmed that inoculation with live ring-edge soil generally promoted plant growth but decreased shoot P concentration. Inoculation with soil collected from inside the ring increased root pathogen infection and reduced shoot biomass. Conclusion We propose that soil microbial activity within ring-edges promotes plant growth via mobilization of plant-available P or directed stimulation. However, as the ring expands, L. chinensis at the leading edge may increase pathogen accumulation, resulting in reduced growth at the center of the ring in subsequent growing seasons. Our results provide new insights into the plant-soil-microbial dynamics of fairy rings in grasslands, helping to elucidate these mysterious vegetation patterns.https://doi.org/10.1186/s12862-022-02082-xSteppe grasslandsBiotic and abiotic factorsPlant–soil–microbial interactionsP-releaseMicrobial direct stimulationPathogen accumulation
spellingShingle Jiahuan Li
Lizhu Guo
Gail W. T. Wilson
Adam B. Cobb
Kun Wang
Li Liu
Huan Zhao
Ding Huang
Assessing soil microbes that drive fairy ring patterns in temperate semiarid grasslands
BMC Ecology and Evolution
Steppe grasslands
Biotic and abiotic factors
Plant–soil–microbial interactions
P-release
Microbial direct stimulation
Pathogen accumulation
title Assessing soil microbes that drive fairy ring patterns in temperate semiarid grasslands
title_full Assessing soil microbes that drive fairy ring patterns in temperate semiarid grasslands
title_fullStr Assessing soil microbes that drive fairy ring patterns in temperate semiarid grasslands
title_full_unstemmed Assessing soil microbes that drive fairy ring patterns in temperate semiarid grasslands
title_short Assessing soil microbes that drive fairy ring patterns in temperate semiarid grasslands
title_sort assessing soil microbes that drive fairy ring patterns in temperate semiarid grasslands
topic Steppe grasslands
Biotic and abiotic factors
Plant–soil–microbial interactions
P-release
Microbial direct stimulation
Pathogen accumulation
url https://doi.org/10.1186/s12862-022-02082-x
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