Different lanthanide elements induce strong gene expression changes in a lanthanide-accumulating methylotroph
ABSTRACT Lanthanides (Ln) are the most recently described life metals and are central to methylotrophy (type of metabolism in which organic substrates without carbon-carbon bonds serve as carbon and energy source) in diverse taxa. We recently characterized a novel, Ln-dependent, and Ln-accumulating...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-12-01
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| Series: | Microbiology Spectrum |
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| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.00867-23 |
| _version_ | 1797393646623916032 |
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| author | Linda Gorniak Julia Bechwar Martin Westermann Frank Steiniger Carl-Eric Wegner |
| author_facet | Linda Gorniak Julia Bechwar Martin Westermann Frank Steiniger Carl-Eric Wegner |
| author_sort | Linda Gorniak |
| collection | DOAJ |
| description | ABSTRACT Lanthanides (Ln) are the most recently described life metals and are central to methylotrophy (type of metabolism in which organic substrates without carbon-carbon bonds serve as carbon and energy source) in diverse taxa. We recently characterized a novel, Ln-dependent, and Ln-accumulating methylotroph, Beijerinckiaceae bacterium RH AL1, which requires lighter Ln (La, Ce, Nd) for methanol oxidation. Starting from two sets of incubations, one with different La concentrations (50 nM and 1 µM) and one with different Ln elements [La, Nd, or an Ln cocktail (containing Ce, Nd, Dy, Ho, Er, Yb)], we could show that La concentration and different Ln elements strongly affect gene expression and intracellular Ln accumulation. Differential gene expression analysis revealed that up to 41% of the encoded genes were differentially expressed. The effects of La concentration and Ln elements were not limited to Ln-dependent methanol oxidation but reached into many aspects of metabolism. We observed that Ln influence the flagellar and chemotactic machinery and that they affect polyhydroxyalkanoate biosynthesis. The most differentially expressed genes included lanM, coding for the well-characterized lanthanide-binding protein lanmodulin, and a glucose dehydrogenase gene linked to the conversion of β-D-glucose to D-glucono-1,5-lactone, a known potential metal chelator. Electron microscopy, together with RNAseq, suggested that Beijerinckiaceae bacterium RH AL1 can discriminate between Ln elements and that they are differently taken up and accumulated. The discrimination of Ln and links between Ln and various aspects of metabolism underline a broader physiological role for Ln in Beijerinckiaceae bacterium RH AL1. IMPORTANCE Since its discovery, Ln-dependent metabolism in bacteria attracted a lot of attention due to its bio-metallurgical application potential regarding Ln recycling and circular economy. The physiological role of Ln is mostly studied dependent on presence and absence. Comparisons of how different (utilizable) Ln affect metabolism have rarely been done. We noticed unexpectedly pronounced changes in gene expression caused by different Ln supplementation. Our research suggests that strain RH AL1 distinguishes different Ln elements and that the effect of Ln reaches into many aspects of metabolism, for instance, chemotaxis, motility, and polyhydroxyalkanoate metabolism. Our findings regarding Ln accumulation suggest a distinction between individual Ln elements and provide insights relating to intracellular Ln homeostasis. Understanding comprehensively how microbes distinguish and handle different Ln elements is key for turning knowledge into application regarding Ln-centered biometallurgy. |
| first_indexed | 2024-03-09T00:05:48Z |
| format | Article |
| id | doaj.art-097d2c882e364bb2983041688fd5db7b |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-09T00:05:48Z |
| publishDate | 2023-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-097d2c882e364bb2983041688fd5db7b2023-12-12T13:17:18ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-12-0111610.1128/spectrum.00867-23Different lanthanide elements induce strong gene expression changes in a lanthanide-accumulating methylotrophLinda Gorniak0Julia Bechwar1Martin Westermann2Frank Steiniger3Carl-Eric Wegner4Institute of Biodiversity, Aquatic Geomicrobiology, Friedrich Schiller University , Jena, GermanyInstitute of Biodiversity, Aquatic Geomicrobiology, Friedrich Schiller University , Jena, GermanyElectron Microscopy Center, Jena University Hospital , Jena, GermanyElectron Microscopy Center, Jena University Hospital , Jena, GermanyInstitute of Biodiversity, Aquatic Geomicrobiology, Friedrich Schiller University , Jena, GermanyABSTRACT Lanthanides (Ln) are the most recently described life metals and are central to methylotrophy (type of metabolism in which organic substrates without carbon-carbon bonds serve as carbon and energy source) in diverse taxa. We recently characterized a novel, Ln-dependent, and Ln-accumulating methylotroph, Beijerinckiaceae bacterium RH AL1, which requires lighter Ln (La, Ce, Nd) for methanol oxidation. Starting from two sets of incubations, one with different La concentrations (50 nM and 1 µM) and one with different Ln elements [La, Nd, or an Ln cocktail (containing Ce, Nd, Dy, Ho, Er, Yb)], we could show that La concentration and different Ln elements strongly affect gene expression and intracellular Ln accumulation. Differential gene expression analysis revealed that up to 41% of the encoded genes were differentially expressed. The effects of La concentration and Ln elements were not limited to Ln-dependent methanol oxidation but reached into many aspects of metabolism. We observed that Ln influence the flagellar and chemotactic machinery and that they affect polyhydroxyalkanoate biosynthesis. The most differentially expressed genes included lanM, coding for the well-characterized lanthanide-binding protein lanmodulin, and a glucose dehydrogenase gene linked to the conversion of β-D-glucose to D-glucono-1,5-lactone, a known potential metal chelator. Electron microscopy, together with RNAseq, suggested that Beijerinckiaceae bacterium RH AL1 can discriminate between Ln elements and that they are differently taken up and accumulated. The discrimination of Ln and links between Ln and various aspects of metabolism underline a broader physiological role for Ln in Beijerinckiaceae bacterium RH AL1. IMPORTANCE Since its discovery, Ln-dependent metabolism in bacteria attracted a lot of attention due to its bio-metallurgical application potential regarding Ln recycling and circular economy. The physiological role of Ln is mostly studied dependent on presence and absence. Comparisons of how different (utilizable) Ln affect metabolism have rarely been done. We noticed unexpectedly pronounced changes in gene expression caused by different Ln supplementation. Our research suggests that strain RH AL1 distinguishes different Ln elements and that the effect of Ln reaches into many aspects of metabolism, for instance, chemotaxis, motility, and polyhydroxyalkanoate metabolism. Our findings regarding Ln accumulation suggest a distinction between individual Ln elements and provide insights relating to intracellular Ln homeostasis. Understanding comprehensively how microbes distinguish and handle different Ln elements is key for turning knowledge into application regarding Ln-centered biometallurgy.https://journals.asm.org/doi/10.1128/spectrum.00867-23lanthanideslanthanomeRNAseqEDXTEMFFTEM |
| spellingShingle | Linda Gorniak Julia Bechwar Martin Westermann Frank Steiniger Carl-Eric Wegner Different lanthanide elements induce strong gene expression changes in a lanthanide-accumulating methylotroph Microbiology Spectrum lanthanides lanthanome RNAseq EDX TEM FFTEM |
| title | Different lanthanide elements induce strong gene expression changes in a lanthanide-accumulating methylotroph |
| title_full | Different lanthanide elements induce strong gene expression changes in a lanthanide-accumulating methylotroph |
| title_fullStr | Different lanthanide elements induce strong gene expression changes in a lanthanide-accumulating methylotroph |
| title_full_unstemmed | Different lanthanide elements induce strong gene expression changes in a lanthanide-accumulating methylotroph |
| title_short | Different lanthanide elements induce strong gene expression changes in a lanthanide-accumulating methylotroph |
| title_sort | different lanthanide elements induce strong gene expression changes in a lanthanide accumulating methylotroph |
| topic | lanthanides lanthanome RNAseq EDX TEM FFTEM |
| url | https://journals.asm.org/doi/10.1128/spectrum.00867-23 |
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