Deciphering the keystone position of abundant species within surface-dwelling microbial aggregates in paddy soils

The surface soil horizon, functioning as the biogeochemical nexus in paddy ecosystems, harbors architecturally complex microbial consortia where abundant and rare taxa exhibit functional redundancy. While these aggregates drive critical nutrient cycling processes, the mechanistic partitioning of ecological roles between abundant and rare subcommunities remains obscured, limiting the development of microbiota-targeted agricultural optimization strategies. To experimentally dissect their functional hierarchies, we developed a controlled culturing system (26°C, 12 h light-dark cycle, 10,000-12,000 lux; nutrient supply: 10% soil leachate + 0.5% mineral solution) to selectively suppress rare taxa while preserving the abundant taxa. Systematic functional partitioning revealed three cardinal determinants of abundant subcommunity ecological predominance: abundant taxa (i) account for >50% of the microbial diversity; (ii) dominate community assembly processes; and (iii) exert greater influence on carbon, nitrogen, and sulfur cycling compared to rare taxa. Our approach establishes causal relationships beyond bioinformatic speculation, providing a functional disentanglement framework that redefines abundant taxa as keystone engineers of aggregate stability and functionality. This conceptual shift holds significant promise for the advancement of precision agriculture and the development of more sustainable nutrient management approaches.IMPORTANCEMoving beyond traditional approaches to bioinformation analysis, this study employed an experimental strategy featuring a novel microbial filtration system. This system was designed to selectively remove rare species, thereby enabling the identification of the predominant roles played by abundant species within microbial aggregates. The findings demonstrate that abundant species are critical for maintaining community stability, governing assembly processes, and exerting greater ecological functions. Beyond introducing a filtration technique capable of distinguishing abundant and rare species in periphyton-like microbial communities, this work provides experimental evidence supporting the prioritization of abundant species in future efforts aimed at regulating periphyton growth or developing periphyton-based biotechnologies for nutrient cycling optimization.

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Publication Details

Journal
Applied and Environmental Microbiology
Published
2025-11-11
DOI
https://doi.org/10.1128/aem.01399-25
Primary Topic
Microbial Community Ecology and Physiology
Type
article
Field-Weighted Citation Impact
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article

Deciphering the keystone position of abundant species within surface-dwelling microbial aggregates in paddy soils

Pengfei Sun, Yin Chen, Eleonora Silvano, Hua Hu et al.
Applied and Environmental Microbiology
Microbial Community Ecology and Physiology
article

Deciphering the keystone position of abundant species within surface-dwelling microbial aggregates in paddy soils

Pengfei Sun, Yin Chen, Eleonora Silvano, Hua Hu, Danfeng Jin, Chen Zhou, Lingjia Liu, Niwen Tang
article en

Abstract

The surface soil horizon, functioning as the biogeochemical nexus in paddy ecosystems, harbors architecturally complex microbial consortia where abundant and rare taxa exhibit functional redundancy. While these aggregates drive critical nutrient cycling processes, the mechanistic partitioning of ecological roles between abundant and rare subcommunities remains obscured, limiting the development of microbiota-targeted agricultural optimization strategies. To experimentally dissect their functional hierarchies, we developed a controlled culturing system (26°C, 12 h light-dark cycle, 10,000-12,000 lux; nutrient supply: 10% soil leachate + 0.5% mineral solution) to selectively suppress rare taxa while preserving the abundant taxa. Systematic functional partitioning revealed three cardinal determinants of abundant subcommunity ecological predominance: abundant taxa (i) account for >50% of the microbial diversity; (ii) dominate community assembly processes; and (iii) exert greater influence on carbon, nitrogen, and sulfur cycling compared to rare taxa. Our approach establishes causal relationships beyond bioinformatic speculation, providing a functional disentanglement framework that redefines abundant taxa as keystone engineers of aggregate stability and functionality. This conceptual shift holds significant promise for the advancement of precision agriculture and the development of more sustainable nutrient management approaches.IMPORTANCEMoving beyond traditional approaches to bioinformation analysis, this study employed an experimental strategy featuring a novel microbial filtration system. This system was designed to selectively remove rare species, thereby enabling the identification of the predominant roles played by abundant species within microbial aggregates. The findings demonstrate that abundant species are critical for maintaining community stability, governing assembly processes, and exerting greater ecological functions. Beyond introducing a filtration technique capable of distinguishing abundant and rare species in periphyton-like microbial communities, this work provides experimental evidence supporting the prioritization of abundant species in future efforts aimed at regulating periphyton growth or developing periphyton-based biotechnologies for nutrient cycling optimization.

Applied and Environmental MicrobiologyVol. 92(1)
Chinese Academy of Sciences (CN), University of Warwick (GB), Environmental Protection Engineering (Greece) (GR), Yonker Environmental Protection (China) (CN), University of Chinese Academy of Sciences (CN), Institute of Soil Science (CN), Yuzhang Normal University, University of Birmingham (GB)
Openalex Percentile: Top 67%
Microbial Community Ecology and Physiology
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