Future climate conditions accelerate wheat straw decomposition alongside altered microbial community composition, assembly patterns, and interaction networks

Abstract

Although microbial decomposition of plant litter plays a crucial role in nutrient cycling and soil fertility, we know less about likely links of specific microbial traits and decomposition, especially in relation to climate change. We study here wheat straw decomposition under ambient and manipulated conditions simulating a future climate scenario (next 80 years) in agroecosystems, including decay rates, macronutrient dynamics, enzyme activity, and microbial communities. We show that future climate will accelerate straw decay rates only during the early phase of the decomposition process. Additionally, the projected climate change will increase the relative abundance of saprotrophic fungi in decomposing wheat straw. Moreover, the impact of future climate on microbial community assembly and molecular ecological networks of both bacteria and fungi will strongly depend on the decomposition phase. During the early phase of straw decomposition, stochastic processes dominated microbial assembly under ambient climate conditions, whereas deterministic processes highly dominated bacterial and fungal communities under simulated future climate conditions. In the later decomposition phase, similar assembly processes shaped the microbial communities under both climate scenarios. Furthermore, over the early phases of decomposition, simulated future climate enhanced the complexity of microbial interaction networks. We concluded that the impact of future climate on straw decay rate and associated microbial traits like assembly processes and inter-community interactions is restricted to the early phase of decomposition.

Fig. 1. Decomposition rate and chemical analysis of wheat straw.

a Mass loss and b decomposition rates (k) of wheat straw under ambient and future climate regimes. c–i Chemical analysis and dynamics of nutrients content of wheat straw over 420 days of decomposition. Values in a given graph (means ± SE, n = 5) labeled with different letters differ significantly (repeated-measured ANOVA, followed by Bonferroni, p < 0.05). Asterisks show significantly different values under climate regimes.

Fig. 2. Microbial diversity on decomposing wheat straw over time.

a Bacteria and (b) fungal Shannon’s diversity under ambient and future climate regimes. c Radar chart showing factors significantly correlated with bacterial and fungal diversity (Spearman’s rank correlation, p < 0.05, Benjamini-Hochberg corrected). Impacts of climate regime, decomposition time, and their interaction on (d) bacterial and (g) fungal community compositions. Principal Coordinate Analysis (PCoA) dissimilarity matrix (Bray–Curtis dissimilarity matrix, permutations = 999) of the bacteria at (e) early and (f) later phase and fungi at (h) early and (i) later phase of decomposition. Vector fitting of the edaphic and wheat variables of plots subjected to ambient and future climate regimes. Significant variables were plotted in black, MOI straw moisture, temp soil temperature at 3 cm depth, ppt precipitation (mm).

Fig. 3. The composition of bacterial communities colonizing wheat straw over 420 days under ambient and future climate regimes.

a Order level taxonomy (>1% relative abundance). b Phylogenetic tree showing the top 100 amplicon sequences variants (ASVs) with highest relative abundance. The taxonomic affiliation at the family level of different Phyla of each ASV is identified by the colors range in the below panel and within the tree. The clade colors showing taxonomy classification at the phylum level; blue: Proteobacteria, red: Actinobacteriota, yellow: Bacteroidota. Microbial abundance at the early (0–60 D) and later (12–420 D) stages of decomposition is indicated in the outer stalked bars. c Heat map showing the dynamic of the top 20 ASVs assigned to genus level under both climate regimes. d The relative abundance of potential metabolic functional genes of Kyoto Encyclopedia of Genes and Genomes (KEGG) orthologs (KOs) assigned to KEGG pathways involved in wheat straw decomposition. ▲ significant shift of the relative abundance of bacterial taxa or predicted metabolic function over time; * significant effect of climate regime on the relative abundance of bacterial taxa or predicted function.

Fig. 4. The composition of fungal communities colonizing wheat straw over 420 days under ambient and future climate regimes.

a Order level taxonomy (>1% relative abundance). b Phylogenetic tree showing the top 100 amplicon sequences variants (ASVs) with the highest cumulative relative abundance. The taxonomic affiliation at the family level of different Phyla of each ASV is identified by the colors range in the below panel and within the tree. The clade colors showing taxonomy classification at the phylum level; green: Ascomycota, red: Basidiomycota. Microbial abundance at the early (0D–60D) and later (120D–420D) stages of decomposition are indicated in the outer stalked bars. c Heat map showing the dynamic of the top 20 ASVs assigned to genus level under both climate regimes. d The relative abundance of predicted ecological fungal traits involved in wheat straw decomposition. ▲ significant shift of the relative abundance of fungal taxa or potential ecological function over time, * significant effect of climate regime on the relative abundance of fungal taxa or predicted ecological function.

Fig. 5. Impact of future climate and time on assembly processes of straw-inhabiting microorganisms.

Ecological stochasticity in potential (a–c) bacterial and (d–f) fungal community assembly estimated by the phylogenetic normalized stochasticity ratio (pNST) and RC_bray index based on Bray–Curtis distance. The value of 0.5 as the boundary point between more deterministic (<0.5) and more stochastic (>0.5) assembly. Differences between ambient and future climates were examined by t test (*p < 0.05; **, p < 0.01; ***p < 0.001). The relative contributions (%) of the community assembly processes based on pNST (c, d) and RC_bray (e, f) in shaping microbial communities. Different upper and lower letters indicate the significant differences among decomposition phases under ambient and future climate regimes, respectively. HS homogeneous selection, VS variable selection, HD homogenizing dispersal, UP undominated process, DL dispersal limitation.

Fig. 6. Microbial ecological networks (MENs) under ambient and future climate regimes.

Microbial interaction networks at (a, b) early and (c, d) later phases of wheat straw decomposition. The size of circles roughly represents relative scores of betweenness centrality. Nodes were colored according to taxonomic group.