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

Kyle Mason-Jones; Andreas Breidenbach; Jens Dyckmans; Callum C. Banfield; Michaela A. Dippold

doi:10.1038/s41467-023-37713-4

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

Kyle Mason-Jones^* (Corresponding author), Andreas Breidenbach, Jens Dyckmans, Callum C. Banfield, Michaela A. Dippold^* (Corresponding author)

^*Corresponding author for this work

NIOO - Terrestrial Ecology (TE)

Research output: Contribution to journal/periodical › Article › Scientific › peer-review

1 Citation (Scopus)

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.

Original language	English
Article number	2240
Journal	Nature Communications
DOIs	https://doi.org/10.1038/s41467-023-37713-4
Publication status	Published - 19 Apr 2023

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title = "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{\textquoteright} 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.",

author = "Kyle Mason-Jones and Andreas Breidenbach and Jens Dyckmans and Banfield, {Callum C.} and Dippold, {Michaela A.}",

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doi = "10.1038/s41467-023-37713-4",

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T1 - Intracellular carbon storage by microorganisms is an overlooked pathway of biomass growth

AU - Mason-Jones, Kyle

AU - Breidenbach, Andreas

AU - Dyckmans, Jens

AU - Banfield, Callum C.

AU - Dippold, Michaela A.

N1 - Data archiving: no NIOO data

PY - 2023/4/19

Y1 - 2023/4/19

N2 - 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.

AB - 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.

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DO - 10.1038/s41467-023-37713-4

M3 - Article

SN - 2041-1723

JO - Nature Communications

JF - Nature Communications

M1 - 2240

ER -

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

Abstract

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