Linking cell division and storage: seasonally intensifying drought shifts microbial C allocation towards storage, with relative fungal resistance

Microbial communities are central to soil biogeochemical cycling. They assimilate organic carbon and either allocate it to biomass or return to the atmosphere as CO₂. Assimilated carbon can support cell division (growth sensu stricto) and also the synthesis of storage compounds or osmolytes (growth sensu lato). Yet, microbial growth is commonly quantified solely based on cell division. Under steady-state conditions, the partitioning of carbon between replicative and non-replicative growth may remain relatively constant (balanced growth), but climate change likely alters microbial growth dynamics and C allocation to different processes (unbalanced growth).

In this study, we investigated responses of microbial growth and storage compound synthesis in a multifactorial climate change experiment (ClimGrass) that included 4 treatments: (i) future climate conditions (elevated temperatures, +3°C, and increased atmospheric CO₂ concentrations, +300 ppm), (ii) a twelve-week summer drought, and (iii) a combination of future climate conditions and drought, as well as (iv) an ambient control. For this study, samples were collected from May (at the onset of drought) to August to capture intensifying drought conditions. We measured deuterium incorporation from ²H-labelled water into PLFAs (phospholipid fatty acids) to quantify growth, and into NLFAs (neutral lipid fatty acids) and PHB (poly-3-hydroxybutyrate) to assess storage compound synthesis.

Over the progression of drought, bacterial mass-specific growth rates decreased more strongly than fungal growth rates, with fungi showing greater relative resistance to drought. Mass-specific NLFA production rates increased over the sampling period in all treatments, suggesting a seasonal increase in storage compound production that was not affected by drought or future climate conditions. However, the ratio of NLFA production to PLFA-derived growth indicated a shift in carbon allocation toward storage NLFA synthesis under drought. In contrast, PHB production rates exhibited no clear seasonal pattern. Yet, normalized to bacterial growth, PHB synthesis also significantly increased under drought in July and August.

In summary, although overall microbial activity declines, drought shifts C allocation from replicative growth to storage compound synthesis, consistent with microbes responding to prolonged summer droughts. This change in allocation of acquired carbon emphasizes the need to quantify both replicative (cell division) and non-replicative (storage) growth to interpret microbial responses and ecosystem feedbacks.