Core functional convergence and spatiotemporal complementarity of soil microbial communities between rhizosphere and decomposing habitats in Foding Mountain Nature Reserve, China

Technical Summary: Core Functional Convergence and Spatiotemporal Complementarity of Soil Microbial Communities

Problem Statement
Forest ecosystems rely on soil microorganisms to drive material cycling, nutrient transformation, and energy flow. While the roles of plant rhizosphere microorganisms and decomposers are individually recognized, the intrinsic linkages between their community assembly mechanisms and functional differentiation remain poorly understood. Specifically, gaps exist in understanding: (1) whether plants regulate rhizosphere microbial communities through unidirectional "enrichment" or more complex bidirectional modes; (2) the precise successional trajectories and niche differentiation dynamics of fungi and bacteria during the multi-stage decomposition of deadwood and litter; and (3) the synergistic or competitive relationships between these two functionally complementary but spatiotemporally distinct microbial guilds within a single ecosystem. Current research often focuses on single plant species or single decomposition stages, lacking systematic studies that integrate multi-species rhizosphere effects with multi-stage decomposition dynamics.

Methodology
The study was conducted in the Foding Mountain National Nature Reserve, a subtropical evergreen broad-leaved forest in Guizhou, China. The research design encompassed two primary habitat types:

1. Rhizosphere Habitats: Soil samples were collected from the rhizosphere of 15 typical woody plant species (e.g., Albizia julibrissin, Castanopsis fargesii, Phoebe zhennan).
2. Decomposing Habitats: Samples were collected from decaying wood and litter at three distinct stages: undecomposed, partially decomposed, and fully decomposed.

A total of 63 samples (15 rhizosphere groups × 3 replicates + 6 decomposition groups × 3 replicates) were processed using high-throughput sequencing.

• Sequencing: Bacterial 16S rRNA genes (V3-V4 regions) and fungal ITS regions were amplified and sequenced on the Illumina MiSeq platform.
• Bioinformatics: Data processing involved quality control (fastp), assembly (FLASH), and denoising (DADA2) to generate Amplicon Sequence Variants (ASVs).
• Analysis: Diversity metrics (ACE, Shannon, Simpson) and beta-diversity (PCoA, ANOSIM) were calculated. Functional predictions were performed using the FUNGuild database for fungi and the FAPROTAX database for bacteria.

Key Results

• Microbial Diversity and Composition: Across all rhizosphere samples, 1,324 fungal genera (16 phyla) and 1,124 bacterial genera (45 phyla) were identified. Host plants exerted significant directional regulation, with specific genera showing enrichment or inhibition depending on the plant species. For instance, Mortierella and Penicillium showed varying relative abundances across different plant rhizospheres.
• Bidirectional Regulation in Rhizosphere: The study revealed a "bidirectional regulation" mechanism where plants simultaneously perform selective enrichment of beneficial or specific functional microbes (e.g., Streptomyces, Aspergillus) and directed inhibition of others (e.g., Xanthomonas, Pseudomonas in specific contexts) via root exudates and allelopathic substances.
• Spatiotemporal Complementarity in Decomposition:
  • Fungi: Exhibited the highest niche differentiation during the early (undecomposed) stage of decomposition. The number of endemic fungal taxa increased as decomposition progressed (from 71 in undecomposed wood to 284 in fully decomposed wood), indicating a continued role in breaking down recalcitrant components.
  • Bacteria: Showed peak niche differentiation and functional specialization during the semi-decomposed stage (e.g., 4,581 endemic taxa in semi-degraded litter). Bacteria dominated the transformation of intermediate metabolites released during partial breakdown.
  • Succession: Fungi acted as pioneer colonizers for lignin and complex polymers, while bacteria specialized in the degradation of hemicellulose and intermediate products, followed by mineralization in the final stages.
• Functional Convergence: Despite distinct environmental conditions and substrate origins, the functional architecture of microbial communities in both rhizosphere and decomposing habitats showed high convergence.
  • Fungi: "Undefined saprotrophs" were the dominant functional group in both habitats, with symbiotic and pathogenic groups serving auxiliary roles.
  • Bacteria: "Chemoheterotrophy" was the foundational functional group in both habitats, supported by key elemental cycling functions (nitrogen and sulfur cycling).

Significance and Claims
The authors claim that this study advances the understanding of microbially driven material cycling in forest ecosystems by elucidating three core patterns:

1. Bidirectional Regulation: It challenges the traditional view of unidirectional plant-microbe enrichment, proposing a complex network where plants simultaneously enrich and suppress specific microbial taxa to maintain stability.
2. Spatiotemporal Complementarity: It clarifies the division of labor between fungi and bacteria, demonstrating that fungi dominate the initial colonization and late-stage mineralization of recalcitrant materials, while bacteria dominate the intermediate transformation of organic matter. This "fungi-begin/end, bacteria-middle" strategy optimizes decomposition efficiency.
3. Core Functional Conservation: The study reveals that while species composition undergoes dramatic succession, the core functional architecture (saprotrophy for fungi, chemoheterotrophy for bacteria) remains conserved across different habitats. This suggests that ecosystem functions are buffered against environmental disturbances through functional redundancy and stability, implying that monitoring functional groups may be more predictive of ecosystem responses to global change than monitoring species composition alone.

These findings provide a theoretical basis for understanding microbial community assembly and offer scientific support for biodiversity conservation and sustainable forest management in the Foding Mountain Nature Reserve.