Response to substrate limitation by a marine sulfate-reducing bacterium

TY - JOUR

T1 - Response to substrate limitation by a marine sulfate-reducing bacterium

AU - Marietou, Angeliki

AU - Kjeldsen, Kasper U

AU - Glombitza, Clemens

AU - Jørgensen, Bo Barker

N1 - © 2021. The Author(s), under exclusive licence to International Society for Microbial Ecology.

PY - 2022/1

Y1 - 2022/1

N2 - Sulfate-reducing microorganisms (SRM) in subsurface sediments live under constant substrate and energy limitation, yet little is known about how they adapt to this mode of life. We combined controlled chemostat cultivation and transcriptomics to examine how the marine sulfate reducer, Desulfobacterium autotrophicum, copes with substrate (sulfate or lactate) limitation. The half-saturation uptake constant (Km) for lactate was 1.2 µM, which is the first value reported for a marine SRM, while the Km for sulfate was 3 µM. The measured residual lactate concentration in our experiments matched values observed in situ in marine sediments, supporting a key role of SRM in the control of lactate concentrations. Lactate limitation resulted in complete lactate oxidation via the Wood-Ljungdahl pathway and differential overexpression of genes involved in uptake and metabolism of amino acids as an alternative carbon source. D. autotrophicum switched to incomplete lactate oxidation, rerouting carbon metabolism in response to sulfate limitation. The estimated free energy was significantly lower during sulfate limitation (-28 to -33 kJ mol-1 sulfate), suggesting that the observed metabolic switch is under thermodynamic control. Furthermore, we detected the upregulation of putative sulfate transporters involved in either high or low affinity uptake in response to low or high sulfate concentration.

AB - Sulfate-reducing microorganisms (SRM) in subsurface sediments live under constant substrate and energy limitation, yet little is known about how they adapt to this mode of life. We combined controlled chemostat cultivation and transcriptomics to examine how the marine sulfate reducer, Desulfobacterium autotrophicum, copes with substrate (sulfate or lactate) limitation. The half-saturation uptake constant (Km) for lactate was 1.2 µM, which is the first value reported for a marine SRM, while the Km for sulfate was 3 µM. The measured residual lactate concentration in our experiments matched values observed in situ in marine sediments, supporting a key role of SRM in the control of lactate concentrations. Lactate limitation resulted in complete lactate oxidation via the Wood-Ljungdahl pathway and differential overexpression of genes involved in uptake and metabolism of amino acids as an alternative carbon source. D. autotrophicum switched to incomplete lactate oxidation, rerouting carbon metabolism in response to sulfate limitation. The estimated free energy was significantly lower during sulfate limitation (-28 to -33 kJ mol-1 sulfate), suggesting that the observed metabolic switch is under thermodynamic control. Furthermore, we detected the upregulation of putative sulfate transporters involved in either high or low affinity uptake in response to low or high sulfate concentration.

KW - CONTINUOUS-CULTURE

KW - DESULFOVIBRIO-VULGARIS

KW - ENVIRONMENTAL CONTROLS

KW - ESCHERICHIA-COLI

KW - GROWTH YIELDS

KW - HYDROGEN

KW - KINETICS

KW - MICROBIAL LIFE

KW - REDUCTION

KW - SULFUR CYCLE

UR - http://www.scopus.com/inward/record.url?scp=85110823148&partnerID=8YFLogxK

U2 - 10.1038/s41396-021-01061-2

DO - 10.1038/s41396-021-01061-2

M3 - Journal article

C2 - 34285365

SN - 1751-7362

VL - 16

SP - 200

EP - 210

JO - The ISME Journal

JF - The ISME Journal

IS - 1

ER -