Highlights: • Diversity was insufficient to assess microbial response to environmental stress. • Rhizosphere networks differed between long- and short-termed disturbances. • Short-termed anthropic disturbances resulted in the lower network stability. • Natural environments and long termed disturbances favor network stability. • Fungi improved the crossdomain networks stability in the long-termed disturbance. Abstract: Growing pressure from climate change and agricultural land use is destabilizing soil microbial community interactions. Yet little is known about microbial community resistance and adaptation to disturbances over time. This hampers our ability to determine the recovery latency of microbial interactions after disturbances, with fundamental implications for ecosystem functioning and conservation measures. Here we examined the response of bacterial and fungal community networks in the rhizosphere of Haloxylon salicornicum (Moq.) Bunge ex Boiss. over the course of soil disturbances resulting from a history of different hydric constraints involving flooding-drought successions. An anthropic disturbance related to past agricultural use, with frequent successions of flooding and drought, was compared to a natural disturbance, i.e., an evaporation basin, with yearly flooding-drought successions. The anthropic disturbance resulted in a specific microbial network topology characterized by lower modularity and stability, reflecting the legacy of past agricultural use on soil microbiome. In contrast, the natural disturbance resulted in a network topology and stability close to those of natural environments despite the lower alpha diversity, and a different community composition compared to that of the other sites. These results highlighted the temporality in the response of the microbial community structure to disturbance, where long-term adaptation to flooding-drought successions lead to a higher stability than disturbances occurring over a shorter timescale.
Authors
Kenji Maurice, Amélia Bourceret, Sami Youssef, Stéphane Boivin, Liam Laurent-Webb, Coraline Damasio, Hassan Boukcim, Marc-André Selosse, Marc Ducousso
- Bibliographic Reference
- Kenji Maurice, Amélia Bourceret, Sami Youssef, Stéphane Boivin, Liam Laurent-Webb, et al.. Anthropic disturbances impact the soil microbial network structure and stability to a greater extent than natural disturbances in an arid ecosystem. Science of the Total Environment, 2024, 907, pp.167969. ⟨10.1016/j.scitotenv.2023.167969⟩. ⟨hal-04285898⟩
- DOI
- https://doi.org/10.1016/j.scitotenv.2023.167969
- Funding
- This work was supported supported by the SoFunLand project, part of the Oasis program funded under the partnership between the RCU (Royal Commission for AlUla) and AFALULA (Agence Française pour le development d'AlUla).
- HAL Collection
- ['IRD - Institut de recherche pour le développement', 'CIRAD - Centre de coopération internationale en recherche agronomique pour le développement', "Muséum National d'Histoire Naturelle", 'École Pratique des Hautes Études', 'Université des Antilles', 'CNRS - Centre national de la recherche scientifique', 'Laboratoire des symbioses tropicales et méditerranéennes', 'GIP Bretagne Environnement', 'Institut de Systématique, Evolution, Biodiversité', 'Sorbonne Université', 'Université Paris sciences et lettres', 'Archive ouverte en agrobiosciences', 'Université de Montpellier', 'Sorbonne Université 01/01/2018', 'Faculté des Sciences de Sorbonne Université', 'TEST-DEV', 'MONTPELLIER-SUPAGRO', 'Institut National de Recherche en Agriculture, Alimentation et Environnement', 'INRAE Occitanie Montpellier', 'École pratique des hautes études - PSL', 'Sorbonne Université - Texte Intégral', 'Alliance Sorbonne Université', 'Université de Montpellier (2015-2021)', 'Université de Montpellier - EPE', 'Réseau "Systèmes Agricoles et Eau"', 'Institut Agro', 'Institut écologie et environnement du CNRS']
- HAL Identifier
- 4285898
- Institution
- ['Centre de Coopération Internationale en Recherche Agronomique pour le Développement', 'Institut de Recherche pour le Développement', 'Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement', 'Institut Agro Montpellier', "Muséum national d'Histoire naturelle", 'École Pratique des Hautes Études', 'Valorhiz', 'Université Mohammed VI Polytechnique [Ben Guerir]', 'African Sustainable Agriculture Research Institute', "Ministère de l'Education nationale, de l’Enseignement supérieur et de la Recherche"]
- Laboratory
- ['Laboratoire des symbioses tropicales et méditerranéennes', 'Institut de Systématique, Evolution, Biodiversité', 'Department of Plant Taxonomy and Nature Conservation', 'Institut Universitaire de France']
- Published in
- France
Table of Contents
- Anthropic disturbances impact the soil microbial network structure and stability to a greater extent than natural disturban ... 2
- 1 Introduction 3
- 2 Material and methods 3
- 2.1 Sampling site 3
- 2.2 Soil chemical composition and pH 3
- 2.3 DNA extraction 3
- 2.4 PCR conditions 4
- 2.5 Purification of PCR products and preparation of sequencing libraries 4
- 2.6 Illumina MiSeq sequencing and data processing 4
- 2.7 Compositional analysis of X-ray fluorescence soil atomic elements 4
- 2.8 Microbial alpha and beta diversity analysis 4
- 2.9 Network construction 4
- 2.10 Network structural properties 5
- 2.11 Network stability analysis 5
- 2.12 Topological roles of network nodes 5
- 3 Results 5
- 3.1 Disturbance results in distinct soil cover and chemistry compared to natural environments 5
- 3.2 Microbial diversity is highly impacted by natural long-term disturbance 5
- 3.3 Microbial network topological properties and stability across sites 6
- 3.4 Topological properties of nodes and keystones ASVs 6
- 4 Discussion 7
- 4.1 Lower microbial diversity only in the natural disturbance conditions 7
- 4.2 Microbial network structure and stability is context dependent when impacted by disturbance 8
- 4.3 Fungi mediate bacterial interactions and network stability 10
- 4.4 Bacterial interactions support the stress-gradient hypothesis 10
- 5 Conclusion and perspectives 10
- Funding 10
- CRediT authorship contribution statement 10
- Declaration of competing interest 11
- Data availability 11
- Acknowledgement 11
- References 11
