E3 Ubiquitin Ligase SPL2 Is a Lanthanide-Binding Protein

Tracz, Michał; Górniak, Ireneusz; Szczepaniak, Andrzej; Białek, Wojciech

doi:10.3390/ijms22115712

Cited by 10 publications

(7 citation statements)

References 57 publications

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“…We meanwhile know three more: the periplasmic Ln-binding protein LutD; supposed to be associated with the LutAEF ABC transporter (27), a ubiquitin ligase from plant chloroplasts (30), and most recently lanpepsy (31) from Methylobacillus flagellatus.…”

Section: Discussionmentioning

confidence: 99%

“…Lanmodulin was the first known lanthanide-binding protein (except PQQ ADHs) (26). We meanwhile know three more: the periplasmic Ln-binding protein LutD; supposed to be associated with the LutAEF ABC transporter (27), a ubiquitin ligase from plant chloroplasts (30), and most recently lanpepsy (31) from Methylobacillus flagellatus . Lanmodulin is not essential for lanthanide-dependent methylotrophy in M. extorquens (25).…”

Section: Discussionmentioning

confidence: 99%

“…LanM is a homolog of the wellcharacterized calcium-binding protein calmodulin (26), which features high affinities for lanthanides and application potential for lanthanide detection and recovery (27)(28)(29). Few other lanthanide-binding proteins have been identified, including most recently lanpepsy from Methylobacillus flagellatus (27,30,31). Intracellular accumulation of lanthanides was shown for M. extorquens AM1 (25) and Beijerinckiaceae bacterium RH AL1 (32).…”

Section: Introductionmentioning

confidence: 99%

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Different lanthanide elements induce strong gene expression changes in a lanthanide-accumulating methylotroph

Gorniak

Bechwar

Westermann

et al. 2023

Preprint

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Lanthanides are the most recently described life metals and are central to methylotrophy in diverse taxa. We recently characterized a novel, lanthanide-dependent, and lanthanide-accumulating methylotroph, Beijerinckiaceae bacterium RH AL1, that utilizes lighter lanthanides (La, Ce, Nd) for methanol oxidation. We show that lanthanum concentration and different lanthanide (Ln) elements strongly affect gene expression and intracellular lanthanide accumulation. Differential gene expression analysis based on incubations with either La (50 nM or 1 µM), Nd (1 µM), or a lanthanide cocktail ([La, Ce, Nd, Dy, Ho, Er, Yb], equimolarly pooled, 1 µM), revealed that up to 41% of the encoded genes were differentially expressed. The effects of lanthanum concentration and Ln elements were not limited to lanthanide-dependent methanol oxidation but reached into many aspects of metabolism. We observed that lanthanides control the flagellar and chemotactic machinery and that they affect polyhydroxyalkanoate (PHA) biosynthesis. Secretion and various uptake systems, and carbohydrate metabolism were highly responsive. The most differentially expressed genes encode various unknown or hypothetical proteins, but alsolanM, coding for the well-characterized lanthanide-binding protein lanmodulin, and a glucose dehydrogenase gene linked to the conversion of β-D-glucose to gluconolactone, a known metal chelator. Electron microscopy, together with RNAseq, suggested different and potentially selective mechanisms for the uptake and accumulation of individual Ln elements. Mechanisms for discriminating lanthanides and links between lanthanides and various aspects of metabolism underline a broader functional role for lanthanides, possibly by functioning as calcium complements or antagonists.ImportanceSince its discovery, lanthanide-dependent metabolism in bacteria attracted a lot of attention due to its bio-metallurgical application potential regarding lanthanide recycling and circular economy. The physiological role of lanthanides is mostly studied dependent on presence and absence. Comparisons of how different (utilizable) lanthanides affect metabolism have rarely been done. Our research shows that strain RH AL1 distinguishes different lanthanide elements and that the effect of lanthanides reaches into many aspects of physiology, for instance, motility and polyhydroxyalkanoate metabolism. Numerous differentially expressed genes coding for unknown or hypothetical proteins might hide so far unknown lanthanide-binding proteins. Our findings regarding lanthanide accumulation suggest different mechanisms for dealing with individual lanthanide elements and provide insights relating to intracellular lanthanide homeostasis. Understanding comprehensively how microbes distinguish and handle different lanthanide elements is key for turning knowledge into application regarding lanthanide-centered biometallurgy.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Different lanthanide elements induce strong gene expression changes in a lanthanide-accumulating methylotroph

Gorniak

Bechwar

Westermann

et al. 2023

Preprint

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“…Notably, a crucial role for SP1 and the CHLORAD pathway has been discovered in the regulation of fruit ripening in tomato plants [ 33 ]. In view of this, two evolutionarily conserved chloroplast SP1 homologues have been studied: SPL1 and SPL2, whose roles are still largely unknown [ 37 , 40 ]. Knockdown expression analysis of SP1 and SPL2 demonstrated delays in leaf senescence and fruit ripening while the opposite effect was apparent in the overexpression analysis of SP1.…”

Section: Regulation Of Chloroplast Function By E3 Ubiquitin Ligasesmentioning

confidence: 99%

The Role of E3 Ubiquitin Ligases in Chloroplast Function

Hand

Shabek

2022

IJMS

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Chloroplasts are ancient organelles responsible for photosynthesis and various biosynthetic functions essential to most life on Earth. Many of these functions require tightly controlled regulatory processes to maintain homeostasis at the protein level. One such regulatory mechanism is the ubiquitin-proteasome system whose fundamental role is increasingly emerging in chloroplasts. In particular, the role of E3 ubiquitin ligases as determinants in the ubiquitination and degradation of specific intra-chloroplast proteins. Here, we highlight recent advances in understanding the roles of plant E3 ubiquitin ligases SP1, COP1, PUB4, CHIP, and TT3.1 as well as the ubiquitin-dependent segregase CDC48 in chloroplast function.

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“…Notably, a crucial role for SP1 and the CHLORAD pathway has been discovered in the regulation of fruit ripening in tomato plants [32]. In view of this, two evolutionarily conserved chloroplast SP1 homologues have been studied: SPL1 and SPL2, whose roles are still largely unknown [36,39]. Knockdown expression analysis of SP1 and SPL2 demonstrated delays in leaf senescence and fruit ripening while the opposite effect was apparent in the overexpression analysis of SP1.…”

Section: Sp1 a Chloroplast-localized Ring-type E3 Ligasementioning

confidence: 99%