Fungi stabilize multi‐kingdom community in a high elevation timberline ecosystem

Abstract Microbes dominate terrestrial ecosystems via their great species diversity and vital ecosystem functions, such as biogeochemical cycling and mycorrhizal symbiosis. Fungi and other organisms form diverse association networks. However, the roles of species belonging to different kingdoms in m...

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Main Authors: Teng Yang, Leho Tedersoo, Xu Liu, Gui‐Feng Gao, Ke Dong, Jonathan M. Adams, Haiyan Chu
Format: Article
Language:English
Published: Wiley 2022-12-01
Series:iMeta
Subjects:
Online Access:https://doi.org/10.1002/imt2.49
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author Teng Yang
Leho Tedersoo
Xu Liu
Gui‐Feng Gao
Ke Dong
Jonathan M. Adams
Haiyan Chu
author_facet Teng Yang
Leho Tedersoo
Xu Liu
Gui‐Feng Gao
Ke Dong
Jonathan M. Adams
Haiyan Chu
author_sort Teng Yang
collection DOAJ
description Abstract Microbes dominate terrestrial ecosystems via their great species diversity and vital ecosystem functions, such as biogeochemical cycling and mycorrhizal symbiosis. Fungi and other organisms form diverse association networks. However, the roles of species belonging to different kingdoms in multi‐kingdom community networks have remained largely elusive. In light of the integrative microbiome initiative, we inferred multiple‐kingdom biotic associations from high elevation timberline soils using the SPIEC‐EASI method. Biotic interactions among plants, nematodes, fungi, bacteria, and archaea were surveyed at the community and network levels. Compared to single‐kingdom networks, multi‐kingdom networks and their associations increased the within‐kingdom and cross‐kingdom edge numbers by 1012 and 10,772, respectively, as well as mean connectivity and negative edge proportion by 15.2 and 0.8%, respectively. Fungal involvement increased network stability (i.e., resistance to node loss) and connectivity, but reduced modularity, when compared with those in the single‐kingdom networks of plants, nematodes, bacteria, and archaea. In the entire multi‐kingdom network, fungal nodes were characterized by significantly higher degree and betweenness than bacteria. Fungi more often played the role of connector, linking different modules. Consistently, structural equation modeling and multiple regression on matrices corroborated the “bridge” role of fungi at the community level, linking plants and other soil biota. Overall, our findings suggest that fungi can stabilize the self‐organization process of multi‐kingdom networks. The findings facilitate the initiation and carrying out of multi‐kingdom community studies in natural ecosystems to reveal the complex above‐ and belowground linkages.
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spelling doaj.art-edfb611dbc0b404abb061ea782a88ca22022-12-22T02:57:14ZengWileyiMeta2770-596X2022-12-0114n/an/a10.1002/imt2.49Fungi stabilize multi‐kingdom community in a high elevation timberline ecosystemTeng Yang0Leho Tedersoo1Xu Liu2Gui‐Feng Gao3Ke Dong4Jonathan M. Adams5Haiyan Chu6State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science Chinese Academy of Sciences Nanjing ChinaMycology and Microbiology Center University of Tartu Tartu EstoniaState Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science Chinese Academy of Sciences Nanjing ChinaState Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science Chinese Academy of Sciences Nanjing ChinaLife Science Major Kyonggi University Suwon South KoreaSchool of Geographic and Oceanographic Sciences Nanjing University Nanjing ChinaState Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science Chinese Academy of Sciences Nanjing ChinaAbstract Microbes dominate terrestrial ecosystems via their great species diversity and vital ecosystem functions, such as biogeochemical cycling and mycorrhizal symbiosis. Fungi and other organisms form diverse association networks. However, the roles of species belonging to different kingdoms in multi‐kingdom community networks have remained largely elusive. In light of the integrative microbiome initiative, we inferred multiple‐kingdom biotic associations from high elevation timberline soils using the SPIEC‐EASI method. Biotic interactions among plants, nematodes, fungi, bacteria, and archaea were surveyed at the community and network levels. Compared to single‐kingdom networks, multi‐kingdom networks and their associations increased the within‐kingdom and cross‐kingdom edge numbers by 1012 and 10,772, respectively, as well as mean connectivity and negative edge proportion by 15.2 and 0.8%, respectively. Fungal involvement increased network stability (i.e., resistance to node loss) and connectivity, but reduced modularity, when compared with those in the single‐kingdom networks of plants, nematodes, bacteria, and archaea. In the entire multi‐kingdom network, fungal nodes were characterized by significantly higher degree and betweenness than bacteria. Fungi more often played the role of connector, linking different modules. Consistently, structural equation modeling and multiple regression on matrices corroborated the “bridge” role of fungi at the community level, linking plants and other soil biota. Overall, our findings suggest that fungi can stabilize the self‐organization process of multi‐kingdom networks. The findings facilitate the initiation and carrying out of multi‐kingdom community studies in natural ecosystems to reveal the complex above‐ and belowground linkages.https://doi.org/10.1002/imt2.49connectivityfungimultiple‐kingdom networksmodularitystabilitytimberline ecosystems
spellingShingle Teng Yang
Leho Tedersoo
Xu Liu
Gui‐Feng Gao
Ke Dong
Jonathan M. Adams
Haiyan Chu
Fungi stabilize multi‐kingdom community in a high elevation timberline ecosystem
iMeta
connectivity
fungi
multiple‐kingdom networks
modularity
stability
timberline ecosystems
title Fungi stabilize multi‐kingdom community in a high elevation timberline ecosystem
title_full Fungi stabilize multi‐kingdom community in a high elevation timberline ecosystem
title_fullStr Fungi stabilize multi‐kingdom community in a high elevation timberline ecosystem
title_full_unstemmed Fungi stabilize multi‐kingdom community in a high elevation timberline ecosystem
title_short Fungi stabilize multi‐kingdom community in a high elevation timberline ecosystem
title_sort fungi stabilize multi kingdom community in a high elevation timberline ecosystem
topic connectivity
fungi
multiple‐kingdom networks
modularity
stability
timberline ecosystems
url https://doi.org/10.1002/imt2.49
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AT xuliu fungistabilizemultikingdomcommunityinahighelevationtimberlineecosystem
AT guifenggao fungistabilizemultikingdomcommunityinahighelevationtimberlineecosystem
AT kedong fungistabilizemultikingdomcommunityinahighelevationtimberlineecosystem
AT jonathanmadams fungistabilizemultikingdomcommunityinahighelevationtimberlineecosystem
AT haiyanchu fungistabilizemultikingdomcommunityinahighelevationtimberlineecosystem