The Cellular Response to Lanthanum Is Substrate Specific and Reveals a Novel Route for Glycerol Metabolism in Pseudomonas putida KT2440

• Published in: mBio Vol. 11; no. 2; pp. e00516 - 20
• Main Authors: Wehrmann, Matthias, Toussaint, Maxime, Pfannstiel, Jens, Billard, Patrick, Klebensberger, Janosch
• Format: Journal Article
• Language: English
• Published: United States American Society for Microbiology 28-04-2020
• Subjects: Alcohol Dehydrogenase - metabolism; Bacterial Proteins; Bacteriology; Carbohydrate Metabolism; Carbon - metabolism; Gene Expression Regulation, Bacterial; Glycerol - metabolism; Lanthanum - metabolism; Life Sciences; Metalloproteins - metabolism; Metals, Rare Earth - metabolism; Microbiology and Parasitology; Molecular Biology and Physiology; PedE; PQQ; Proteomics; Pseudomonas putida; Pseudomonas putida - genetics; Pseudomonas putida - metabolism; rare earth elements; proteomics; rare earth elements; lanthanides; PQQ; GarK; PedE; alcohol dehydrogenases; metalloenzymes; dehydrogenases; glycerol metabolism; PedH; Pseudomonas putida; carbon metabolism; volatiles
• ISSN: 2161-2129; 2150-7511
• DOI: 10.1128/mbio.00516-20

Ever since the discovery of the first rare earth element (REE)-dependent enzyme, the physiological role of lanthanides has become an emerging field of research due to the environmental implications and biotechnological opportunities. In
KT2440, the two pyrroloquinoline quinone-dependent alcohol dehydrogenases (PQQ-ADHs) PedE and PedH are inversely regulated in response to REE availability. This transcriptional switch is orchestrated by a complex regulatory network that includes the PedR2/PedS2 two-component system and is important for efficient growth on several alcoholic volatiles. To study whether cellular responses beyond the REE switch exist, the differential proteomic responses that occur during growth on various model carbon sources were analyzed. Apart from the Ca
-dependent enzyme PedE, the differential abundances of most identified proteins were conditional. During growth on glycerol-and concomitant with the proteomic changes-lanthanum (La
) availability affected different growth parameters, including the onset of logarithmic growth and final optical densities. Studies with mutant strains revealed a novel metabolic route for glycerol utilization, initiated by PedE and/or PedH activity. Upon oxidation to glycerate via glyceraldehyde, phosphorylation by the glycerate kinase GarK most likely yields glycerate-2-phosphate, which is eventually channeled into the central metabolism of the cell. This new route functions in parallel with the main degradation pathway encoded by the
operon and provides a growth advantage to the cells by allowing an earlier onset of growth with glycerol as the sole source of carbon and energy.
The biological role of REEs has long been underestimated, and research has mainly focused on methanotrophic and methylotrophic bacteria. We have recently demonstrated that
, a plant growth-promoting bacterium that thrives in the rhizosphere of various food crops, possesses a REE-dependent alcohol dehydrogenase (PedH), but knowledge about REE-specific effects on physiological traits in nonmethylotrophic bacteria is still scarce. This study demonstrates that the cellular response of
to lanthanum (La
) is mostly substrate specific and that La
availability highly affects the growth of cells on glycerol. Further, a novel route for glycerol metabolism is identified, which is initiated by PedE and/or PedH activity and provides a growth advantage to this biotechnologically relevant organism by allowing a faster onset of growth. Overall, these findings demonstrate that lanthanides can affect physiological traits in nonmethylotrophic bacteria and might influence their competitiveness in various environmental niches.