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

Abstract

The concept of biomass growth is central to microbial carbon (C) cycling and ecosystem nutrient turnover. Microbial biomass is usually assumed to grow by cellular replication, despite microorganisms’ capacity to increase biomass by synthesizing storage compounds. Resource investment in storage allows microbes to decouple their metabolic activity from immediate resource supply, supporting more diverse microbial responses to environmental changes. Here we show that microbial C storage in the form of triacylglycerides (TAGs) and polyhydroxybutyrate (PHB) contributes significantly to the formation of new biomass, i.e. growth, under contrasting conditions of C availability and complementary nutrient supply in soil. Together these compounds can comprise a C pool 0.19 ± 0.03 to 0.46 ± 0.08 times as large as extractable soil microbial biomass and reveal 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 as a key pathway of biomass growth and an underlying mechanism for resistance and resilience of microbial communities facing environmental change.

Drought resistance and resilience of rhizosphere communities in forest soils from the cellular to ecosystem scale – insights from 13C pulse labeling

“…Consequently, the lower ratio of the 13 C signal in PLFA to that in microbial cytoplasm under drought (Fig.5) strongly suggests that rhizosphere microorganisms shifted their use of fresh rhizodeposits toward osmoregulation, storage and maintenance. These findings support those from a recent study byMason-Jones et al (2023), that microorganisms invest primarily in storage instead of replicative growth in times of reduced C supply (as under drought in our experiments). In our study, different microbial groups showed divergent drought responses regarding the ratios of the 13 C signal in PLFAs vs in microbial cytoplasm.…”

“…Incorporation of 13 C in PLFAs reflects the formation of new microbial cells and hence can serve as an indicator for the growth of rhizosphere communities (Kaiser et al, 2015). In comparison, extracted microbial biomass following chloroform fumigation mainly comprises microbial cytoplasm (Hogberg et al, 2010), which can also be used for other metabolic processes, for adjusting osmotic potentials (Karlowsky et al, 2018b), or for storage (Mason-Jones et al, 2023). In 13 C pulse labeling experiments in mountain grasslands, Fuchslueger et al (2014) observed a reduced transfer and incorporation of assimilates into bacteria after a 2-month drought, but not into associated arbuscular mycorrhizal fungi.…”

“…Since PLFAs are components of cell membrane, their weaker 13 C signal in dry soils reflects reduced formation of new cells, which is indicative of suppressed cellular replication(Kaiser et al, 2015). By comparison, microbial cytoplasm assessed as CFE-microbial biomass(Hogberg et al, 2008;Lorenz et al, 2021) consists primarily of compounds used for metabolic processes with high turnover rates(Malik et al, 2016), for regulation of osmotic potentials(Karlowsky et al, 2018a), and for storage(Mason-Jones et al, 2023). Consequently, the lower ratio of the 13 C signal in PLFA to that in microbial cytoplasm under drought (Fig.5) strongly suggests that rhizosphere microorganisms shifted their use of fresh rhizodeposits toward osmoregulation, storage and maintenance.…”

Promotion of Humic Acid Transformation by Abiotic and Biotic Fe Redox Cycling in Nontronite

“…It may be attributed to the incomplete mineralization of structurally complexed molecules such as HA. For potential intracellular OM, such as glycogen, triacylglycerides, and polyhydroxybutyrate, mineralization of these simple molecules can be more easily achieved.…”

“…It may be attributed to the incomplete mineralization of structurally complexed molecules such as HA. For potential intracellular OM, such as glycogen, triacylglycerides, and polyhydroxybutyrate, 77 mineralization of these simple molecules can be more easily achieved. Supply of HA trans increased the reduction rate (Table S2), but more importantly, it significantly increased the final reduction extent (7.9% for HA initial and 16.2% for HA trans ) by 105.5% (Figure 3A).…”