Rare Earth Element (REE)-Dependent Growth of Pseudomonas putida KT2440 Relies on the ABC-Transporter PedA1A2BC and Is Influenced by Iron Availability

Wehrmann, Matthias; Berthelot, Charlotte; Billard, Patrick; Klebensberger, Janosch

doi:10.3389/fmicb.2019.02494

Cited by 22 publications

(14 citation statements)

References 97 publications

(89 reference statements)

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“…In Pseudomona putida KT2440, growth in the absence of the analogous Ln-ABC transporter still occurs if exogenous Ln 3+ concentrations are high (100 µM) and/or Fe 2+/3+ concentrations are low. These results suggest that in P. putida KT2440, Ln are in competition with metals such as Fe 3+ and can be transported by other metal (Fe 3+ ) transport systems when in excess 48 . Intriguingly, Gu and Semrau saw differential expression of multiple genes encoding ABC-type and TonB-dependent transporters in the methanotroph, Methylosinus trichosporium OB3b, when cerium was added to the growth medium 50 .…”

Section: Discussionmentioning

confidence: 83%

“…An analogous system in P. putida KT2440 exists where expression of the pedH and pedE genes, which encode Ln- and Ca-dependent ADHs respectively, are differentially regulated by Ln through the PedS2/R2 two-component system 10 . Unlike M. extorquens , Ln-ABC transport mutants of P. putida KT2440 express pedH when Ln are present, suggesting periplasmic Ln are enough to facilitate pedH expression 48 .…”

Section: Discussionmentioning

confidence: 99%

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Gene products and processes contributing to lanthanide homeostasis and methanol metabolism in Methylorubrum extorquens AM1

Roszczenko-Jasińska

Subuyuj

et al. 2020

Sci Rep

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Lanthanide elements have been recently recognized as “new life metals” yet much remains unknown regarding lanthanide acquisition and homeostasis. In Methylorubrum extorquens AM1, the periplasmic lanthanide-dependent methanol dehydrogenase XoxF1 produces formaldehyde, which is lethal if allowed to accumulate . This property enabled a transposon mutagenesis study and growth studies to confirm novel gene products required for XoxF1 function. The identified genes encode an MxaD homolog , an ABC-type transporter, an aminopeptidase, a putative homospermidine synthase, and two genes of unknown function annotated as orf6 and orf7 . Lanthanide transport and trafficking genes were also identified. Growth and lanthanide uptake were measured using strains lacking individual lanthanide transport cluster genes, and transmission electron microscopy was used to visualize lanthanide localization. We corroborated previous reports that a TonB-ABC transport system is required for lanthanide incorporation to the cytoplasm. However, cells were able to acclimate over time and bypass the requirement for the TonB outer membrane transporter to allow expression of xoxF1 and growth. Transcriptional reporter fusions show that excess lanthanides repress the gene encoding the TonB-receptor. Using growth studies along with energy dispersive X-ray spectroscopy and transmission electron microscopy, we demonstrate that lanthanides are stored as cytoplasmic inclusions that resemble polyphosphate granules.

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Section: Discussionmentioning

confidence: 83%

Section: Discussionmentioning

confidence: 99%

Gene products and processes contributing to lanthanide homeostasis and methanol metabolism in Methylorubrum extorquens AM1

Roszczenko-Jasińska

Subuyuj

et al. 2020

Sci Rep

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“…To date, two transporters have been experimentally verified as required for lanthanide transport: the outer membrane siderophore-associated TonB-dependent transporter (Ochsner et al 2019) and the periplasmic ABC-type transporter (Wehrmann et al 2019). We identified two transport proteins not previously associated with XoxF systems, NRAMP and the mechanosensitive ion channel (MscS).…”

Section: Discussionmentioning

confidence: 99%

Do lanthanide-dependent microbial metabolisms drive the release of REEs from weathered granites?

Voutsinos

West-Roberts

Sachdeva

et al. 2022

Preprint

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Prior to soil formation, phosphate liberated by rock weathering is often sequestered into highly insoluble lanthanide phosphate minerals. Dissolution of these minerals is critical for the release of phosphate to the biosphere, yet the microorganisms involved, and the genes required for lanthanide metabolism, are poorly understood. Here, we sampled weathered granite and associated soil to identify the zones of lanthanide phosphate mineral solubilization and genomically define the organisms implicated in lanthanide utilisation. We reconstructed 136 genomes from 11 bacterial phyla and found gene clusters implicated in lanthanide-based metabolism of methanol (primarily XoxF3 and XoxF5) are surprisingly common in microbial communities in moderately weathered granite where lanthanide phosphate minerals are dissolving. Notably, XoxF3 systems were found in Verrucomicrobia for the first time, and in Acidobacteria, Gemmatimonadetes, and Alphaproteobacteria. The XoxF-containing gene clusters are shared by diverse Acidobacteria and Gemmatimonadetes, and include conserved hypothetical proteins and transporters not associated with the few well studied XoxF systems. Given that siderophore-like molecules that strongly bind lanthanides may be required to solubilize lanthanide phosphates, it is notable that candidate siderophore biosynthesis systems were most prevalent in bacteria in moderately weathered rock, especially in Acidobacteria with lanthanide-based systems. We conclude that the confluence in the zone of moderate weathering of phosphate mineral dissolution, lanthanide utilisation, and methanol oxidation (thus carbonic acid production) may be important during the conversion of granitic rock to soil.

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“…It further indicates that this regulatory system is functional under all tested conditions. The only other two proteins (PedH and PP_2673) that showed differential abundance under more than one set of culture conditions are encoded by genes within the ped gene cluster, which encodes several crucial elements for regulation and function of PedE and PedH (13,43,47). Notably, the carbon sources provided under the conditions in which these proteins were identified either represent substrates of PedE and PedH (2-phenylethanol and glycerol) or can be converted by an enzyme depending on the same PQQ cofactor, namely, the glucose dehydrogenase Gcd (glucose).…”

Section: Discussionmentioning

confidence: 99%

“…The aforementioned observations suggest that apart from the inverse transcriptional regulation of PQQ-ADHs, which has been described in detail for different organisms, including P. putida (12,13,20,28,(39)(40)(41)(42)(43), additional cellular responses to REEs exist and could depend on the specific organism and/or environmental context. To investigate the existence of such conditional responses in the nonmethylotrophic organism P. putida KT2440, we used a differential proteomic approach during growth on various model carbon sources that reflect the metabolic diversity of the rhizosphere.…”

mentioning

confidence: 92%

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

Wehrmann

Toussaint

Pfannstiel

et al. 2020

mBio

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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 Pseudomonas putida 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 Ca2+-dependent enzyme PedE, the differential abundances of most identified proteins were conditional. During growth on glycerol—and concomitant with the proteomic changes—lanthanum (La3+) 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 glpFKRD 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. IMPORTANCE The biological role of REEs has long been underestimated, and research has mainly focused on methanotrophic and methylotrophic bacteria. We have recently demonstrated that P. putida, 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 P. putida to lanthanum (La3+) is mostly substrate specific and that La3+ 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.

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Rare Earth Element (REE)-Dependent Growth of Pseudomonas putida KT2440 Relies on the ABC-Transporter PedA1A2BC and Is Influenced by Iron Availability

Cited by 22 publications

References 97 publications

Gene products and processes contributing to lanthanide homeostasis and methanol metabolism in Methylorubrum extorquens AM1

Gene products and processes contributing to lanthanide homeostasis and methanol metabolism in Methylorubrum extorquens AM1

Do lanthanide-dependent microbial metabolisms drive the release of REEs from weathered granites?

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

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