Community composition and physiological plasticity control microbial carbon storage across natural and experimental soil fertility gradients

Many microorganisms synthesise carbon (C)-rich compounds under resource deprivation. Such compounds likely serve as intracellular C-storage pools that sustain the activities of microorganisms growing on stoichiometrically imbalanced substrates, making them potentially vital to the function of ecosystems on infertile soils. We examined the dynamics and drivers of three putative C-storage compounds (neutral lipid fatty acids [NLFAs], polyhydroxybutyrate [PHB], and trehalose) across a natural gradient of soil fertility in eastern Australia. Together, NLFAs, PHB, and trehalose corresponded to 8.5–40% of microbial C and 0.06–0.6% of soil organic C. When scaled to “structural” microbial biomass (indexed by polar lipid fatty acids; PLFAs), NLFA and PHB allocation was 2–3-times greater in infertile soils derived from ironstone and sandstone than in comparatively fertile basalt- and shale-derived soils. PHB allocation was positively correlated with belowground biological phosphorus (P)-demand, while NLFA allocation was positively correlated with fungal PLFA : bacterial PLFA ratios. A complementary incubation revealed positive responses of respiration, storage, and fungal PLFAs to glucose, while bacterial PLFAs responded positively to PO(4)(3-). By comparing these results to a model of microbial C-allocation, we reason that NLFA primarily served the “reserve” storage mode for C-limited taxa (i.e., fungi), while the variable portion of PHB likely served as “surplus” C-storage for P-limited bacteria. Thus, our findings reveal a convergence of community-level processes (i.e., changes in taxonomic composition that underpin reserve-mode storage dynamics) and intracellular mechanisms (e.g., physiological plasticity of surplus-mode storage) that drives strong, predictable community-level microbial C-storage dynamics across gradients of soil fertility and substrate stoichiometry.