Microbial responses to long-term warming differ across soil microenvironments

Abstract

Soil carbon loss is likely to increase due to climate warming, but microbiomes and microenvironments may dampen this effect. In a 30-year warming experiment, physical protection within soil aggregates affected the thermal responses of soil microbiomes and carbon dynamics. In this study, we combined metagenomic analysis with physical characterization of soil aggregates to explore mechanisms by which microbial communities respond to climate warming across different soil microenvironments. Long-term warming decreased the relative abundances of genes involved in degrading labile compounds (e.g. cellulose), but increased those genes involved in degrading recalcitrant compounds (e.g. lignin) across aggregate sizes. These changes were observed in most phyla of bacteria, especially for Acidobacteria, Actinobacteria, Bacteroidetes, Chloroflexi, and Planctomycetes. Microbial community composition was considerably altered by warming, leading to declined diversity for bacteria and fungi but not for archaea. Microbial functional genes, diversity, and community composition differed between macroaggregates and microaggregates, indicating the essential role of physical protection in controlling microbial community dynamics. Our findings suggest that microbes have the capacity to employ various strategies to acclimate or adapt to climate change (e.g. warming, heat stress) by shifting functional gene abundances and community structures in varying microenvironments, as regulated by soil physical protection.

Keywords: bacterial necromass; biogeochemical cycles; carbon storage and sequestration; degradation enzymes; functional genomics; microbial evolution; organic matter decomposition; plant soil interactions; soil aggregation; substrate accessibility.

Figure 1

Changes of microbial functional genes associated with metabolism and cellular processes in different aggregates under long-term warming; MA and MI are macroaggregates and microaggregates (250–2000; <250 μm); black symbols indicate significant effect sizes of warming ([heated-control]/control), while red symbols indicate significant differences between MA and MI (^#, ^*, ^**, ^*** at P < .10, .05, .01, and .001).

Figure 2

Changes of microbial functional genes in different aggregates under long-term warming; MA and MI are macroaggregates and microaggregates (250–2000; <250 μm); black symbols indicate significant effect sizes of warming ([heated-control]/control), while red symbols indicate significant differences between MA and MI (^#, ^*, ^**, ^*** at P < .10, .05, .01, and .001).

Figure 3

Changes of microbial functional genes associated with carbon degradation in different aggregates under long-term warming; MA and MI are macroaggregates and microaggregates (250–2000; <250 μm); black symbols indicate significant effect sizes of warming ([heated-control]/control ×100%) (^*, ^**, ^*** at P < .05, .01, and .001); different uppercase and lowercase letters indicate differences within macroaggregates or microaggregates.

Figure 4

Changes of bacterial relative abundances in different aggregates over long-term warming; MA and MI are macroaggregates and microaggregates (250–2000; <250 μm); black symbols indicate significant effect sizes of warming ([heated-control]/control×100%)), while red symbols indicate significant differences between MA and MI (^#, ^*, ^**, ^*** at P < .10, .05, .01, and .001).

Figure 5

Microbial diversity as affected by aggregate size in response to long-term warming (different letters indicate differences between macroaggregates and microaggregates in control (blue) or heated plots (red); P values for diversity were obtained from two-way ANOVA (^* and ^*** at P<.05 and .001).

Figure 6

Community composition of different microbial groups as affected by aggregate size in response to long-term warming; P values for community composition were obtained from Permanova (Adonis) test; dispersion test (betadisper) showed no significant treatment effects.