Intracellular carbon storage by microorganisms is an overlooked pathway of biomass growth

Abstract

The concept of microbial biomass growth is central to microbial carbon (C) cycling and ecosystem nutrient turnover. Growth is usually assumed to occur by cellular replication, despite microorganisms’ capacity to increase biomass by synthesizing storage compounds. Here we examined whether C storage in triacylglycerides (TAGs) and polyhydroxybutyrate (PHB) contribute significantly to microbial biomass growth, under contrasting conditions of C availability and complementary nutrient supply. Together these compounds accounted for 19.1 ± 1.7% to 46.4 ± 8.0% of extractable soil microbial biomass, and revealed up to 279 ± 72% more biomass growth than observed by a DNA-based method alone. Even under C limitation, storage represented an additional 16 – 96% incorporation of added C into microbial biomass. These findings encourage greater recognition of storage synthesis and degradation as key pathways of biomass change and as mechanisms underlying resistance and resilience of microbial communities.

Intracellular carbon storage by microorganisms is an overlooked pathway of biomass growth

“…All source data generated in this study has been deposited in the Zenodo open data repository 52 under https://doi.org/10.5281/zenodo. 6386047.…”

Soil fungi remain active and invest in storage compounds during drought independent of future climate conditions

“…Microbial biomass growth is classically supposed to be directly represented by cell replication rates. However, microorganisms can allocate large amount of C to other processes, such as storage compounds, which can represent a large fraction of the total biomass ( 29 ). The 2 H-vapor-PLFA-SIP method enabled us to additionally characterize the production rates of NLFAs (triglycerides), which represents major storage compounds in eukaryotic cells ( 65 ) and also in many bacterial species ( 38 , 66 ).…”

“…The link between growth rates and microbial identity is a major focus in microbial ecology and can provide mechanistic insights into the role of soil microbial taxa and community dynamics for biogeochemical C and nutrient cycling. Microbial biomass can increase as a result of cell replication, but also through the synthesis of storage compounds ( 29 ). The ability of microbial populations to invest resources in storage enables them to detach their metabolic activity from the immediate resource availability, thereby facilitating a wider range of microbial responses to environmental fluctuations ( 30 ).…”

“…NLFAs are considered as storage compounds found mainly in fungi and many prokaryotic species, they can account for a large C fraction of the total soil microbial biomass pool ( 38 ). While classically biomass growth is investigated by measuring cell replication, soil microbes can produce and accumulate large amount of storage compounds representing up to 46% of the total microbial biomass, especially in ‘stress’ situations ( 29 ). This trait can be particularly relevant in ecosystems experiencing large variations in C and nutrient supply ( 39 ) such as during drought conditions.…”

Life history strategies and niches of soil bacteria emerge from interacting thermodynamic, biophysical, and metabolic traits

“…is a volumetric length, p Am is the maximum assimilation flux and m * E represents the ratio of assimilation and mobilization fluxes, i.e., the reserve capacity of the organism that is reached at long exposure to high substrate concentrations. The reserve pool buffers between environmental substrate uptake and microbial cell metabolism [54]. The standard DEB literature assumes that the relaxation time of reserve density dynamics is proportional to cell length [55].…”