Habitat heterogeneity induced by pyrogenic organic matter in wildfire-perturbed soils mediates bacterial community assembly processes

Abstract

Although pyrogenic organic matter (PyOM) generated during wildfires plays a critical role in post-fire ecosystem recovery, the specific mechanisms by which PyOM controls soil microbial community assembly after wildfire perturbation remain largely uncharacterized. Herein we characterized the effect of PyOM on soil bacterial communities at two independent wildfire-perturbed forest sites. We observed that α-diversity of bacterial communities was the highest in wildfire-perturbed soils and that bacterial communities gradually changed along a sequence of unburnt soil → burnt soil → PyOM. The microbial communities reconstructed from unburnt soil and PyOM resembled the real bacterial communities in wildfire-perturbed soils in their α-diversity and community structure. Bacterial specialists in PyOM and soils clustered in phylogenetic coherent lineages with intra-lineage pH-niche conservatism and inter-lineage pH-niche divergence. Our results suggest that PyOM mediates bacterial community assembly in wildfire-perturbed soils by a combination of environmental selection and dispersal of phylogenetic coherent specialists with habitat preference in the heterogeneous microhabitats of burnt soils with distinct PyOM patches.

Fig. 1. Schematic diagram of conserved niche and its phylogenetic response.

a Conserved niche is a convergent value of one functional trait of genetic variants in some lineages, representing a niche shared by all the genetic variants in the lineages. b Conserved niche is recognized as coherence of habitat-preference in phylogenies. Statistical significance was tested using binominal tests.

Fig. 2. pH and α-diversity of samples at the Zhejiang and Jiangxi sites.

(a–f) The Zhejiang site. (g–l) The Jiangxi site. An αNTI value >2 is considered phylogenetic clustering. The curvilinear polygons indicate estimates of frequency densities. The upper/lower hinges of boxes represent the 75th/25th quantiles, and the lines inside boxes indicate the median value. The whiskers above/below boxes extend to the maximum/minimum values within ≤1.5 inter-quantile-range, whereas data points outside the range are plotted separately. *, ** and *** indicate significance at P ≤ 0.05, ≤ 0.01 and ≤ 0.001, respectively.

Fig. 3. Correlations among environmental pH, α-diversity and NMDS1 scores.

(a, b, e, f, i, j) The Zhejiang site. (c, d, g, h, k, l) The Jiangxi site. Relationships were tested using linear (a and c) or quadratic (b, d, e–l) regressions. A solid curve or line indicates statistical significance at the 0.05 level with the dashed line indicating insignificance. The gray shading represents the 95% confident interval for regressions. Notations and abbreviations: r, Pearson’s r statistics; P₂, P values for the quadratic coefficients, which reflect the inverted-U shape.

Fig. 4. Microbial community changes after wildfire perturbation.

Unconstraint ordinations (NMDS) among all samples based on generalized UniFrac distances for Zhejiang (a) and Jiangxi (b) sites. Statistical significance was tested using PERMANOVA by assigning 3 (high), 2 (medium) and 1 (no) influence of PyOM, to PyOM, burnt soils and unburnt soils. Curves next to and below the ordinations are estimations of frequency densities for the corresponding axes. Procrustes analysis between PyOM and its adjacent burnt soils at Zhejiang (c) and Jiangxi (d) sites. The adjacency relationship is indicated by arrows.

Fig. 5. Relative abundances of dominant phyla.

(a) The Zhejiang site. (b) The Jiangxi site. Phyla are selected as dominant phyla if their relative abundance is >1% in at least one sample type (unburnt soils, burnt soils or PyOM) at each site. Phyla are labeled with ** if their relative abundance is associated with a specific sample type (Kruskal–Wallis test with Bonferroni correction, P < 0.01).

Fig. 6. Comparison of reconstructed and measured communities of the burnt soils.

Statistical significance was tested using Kolmogorov-Smirnov tests. Symbols and abbreviations: n.s., * and *** stand for insignificant at P = 0.05, P < 0.05 and P < 0.001, respectively. a, c Biodiversity metrics. The shapes have the same meaning as in Fig. 1. b, d Unconstrained ordinations using NMDS based on generalized UniFrac. The curves next to and below the ordinations are estimations of frequency densities for the corresponding axes.

Fig. 7. Phylogenetic coherence and conservatism of specialists.

(a) The Zhejiang site. (b) the Jiangxi site. Markers in the outer ring of the aura indicate habitat preference of OTUs with blank areas indicating a neutral response. The coherent markers in the inner ring indicate coherent lineages (Table S2) and their habitat preference. The statistic inside the aura is Fritz’s 1 – D, which is noted in the 6 largest phyla of phylogenetic conservationism (P < 0.01, based on label permutation). A higher 1 – D value indicates stronger phylogenetic conservatism.