A nonpyrrolysine member of the widely distributed trimethylamine methyltransferase family is a glycine betaine methyltransferase

Ticak, Tomislav; Kountz, Duncan J.; Girosky, Kimberly E.; Krzycki, Joseph A.; Ferguson, Donald J.

doi:10.1073/pnas.1409642111

Cited by 78 publications

(164 citation statements)

References 84 publications

(80 reference statements)

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“…The predicted proteins of the methyltransferase system are similar to MTI, CoP and MTII of other methyltransferase systems of bacteria and methanogenic archaea. Highest similarity is to the biochemically proven GB‐demethylating system of D. hafniense (Ticak et al ., ; Fig. ).…”

Section: Discussionmentioning

confidence: 93%

Glycine betaine metabolism in the acetogenic bacterium Acetobacterium woodii

Lechtenfeld

Heine

Sameith

et al. 2018

Environmental Microbiology

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The quarternary, trimethylated amine glycine betaine (GB) is widespread in nature but its fate under anoxic conditions remains elusive. It can be used by some acetogenic bacteria as carbon and energy source but the pathway of GB metabolism has not been elucidated. We have identified a gene cluster involved in GB metabolism and studied acetogenesis from GB in the model acetogen Acetobacterium woodii. GB is taken up by a secondary active, Na coupled transporter of the betaine-choline-carnitine (BCC) family. GB is demethylated to dimethylglycine, the end product of the reaction, by a methyltransferase system. Further conversion of the methyl group requires CO as well as Na indicating that GB metabolism involves the Wood-Ljungdahl pathway. These studies culminate in a model for the path of carbon and electrons during acetogenensis from GB and a model for the bioenergetics of acetogenesis from GB.

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Section: Discussionmentioning

confidence: 93%

Glycine betaine metabolism in the acetogenic bacterium Acetobacterium woodii

Lechtenfeld

Heine

Sameith

et al. 2018

Environmental Microbiology

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“…We also identified multiple ABC transporters for sugars and peptides (see Tables S5 and S6 in the supplemental material). No evidence of a carbon fixation capability was found, but we did identify genes involved in C 1 compound oxidation: (i) type I and type II carbon monoxide dehydrogenases, on the basis of both motif and gene neighborhood analyses (see Table S7 in the supplemental material), and (ii) part of the pathway for the tetrahydrofolate-dependent oxidation of methanol, glycine, methylamines, and, potentially, betaine (four copies of trimethylamine:corrinoid methyltransferases [39]) (see Table S8 in the supplemental material). Missing genes were present in multiple copies in the metagenomic data set, though they were not part of the Chloroflexi bins.…”

Section: Resultsmentioning

confidence: 99%

Chloroflexi CL500-11 Populations That Predominate Deep-Lake Hypolimnion Bacterioplankton Rely on Nitrogen-Rich Dissolved Organic Matter Metabolism and C ₁ Compound Oxidation

Denef

Mueller

Chiang

et al. 2016

Appl Environ Microbiol

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The Chloroflexi CL500-11 clade contributes a large proportion of the bacterial biomass in the oxygenated hypolimnia of deep lakes worldwide, including the world's largest freshwater system, the Laurentian Great Lakes. Traits that allow CL500-11 to thrive and its biogeochemical role in these environments are currently unknown. Here, we found that a CL500-11 population was present mostly in offshore waters along a transect in ultraoligotrophic Lake Michigan (a Laurentian Great Lake). It occurred throughout the water column in spring and only in the hypolimnion during summer stratification, contributing up to 18.1% of all cells. Genome reconstruction from metagenomic data suggested an aerobic, motile, heterotrophic lifestyle, with additional energy being gained through carboxidovory and methylovory. Comparisons to other available streamlined freshwater genomes revealed that the CL500-11 genome contained a disproportionate number of cell wall/capsule biosynthesis genes and the most diverse spectrum of genes involved in the uptake of dissolved organic matter (DOM) substrates, particularly peptides. In situ expression patterns indicated the importance of DOM uptake and protein/peptide turnover, as well as type I and type II carbon monoxide dehydrogenase and flagellar motility. Its location in the water column influenced its gene expression patterns the most. We observed increased bacteriorhodopsin gene expression and a response to oxidative stress in surface waters compared to its response in deep waters. While CL500-11 carries multiple adaptations to an oligotrophic lifestyle, its investment in motility, its large cell size, and its distribution in both oligotrophic and mesotrophic lakes indicate its ability to thrive under conditions where resources are more plentiful. Our data indicate that CL500-11 plays an important role in nitrogen-rich DOM mineralization in the extensive deep-lake hypolimnion habitat. Freshwater lakes are disproportionally active sites of carbon cycling relative to the surface area that they cover due to strong linkages to the surrounding land, from which they receive inorganic nutrients as well as organic carbon (1, 2). Of the estimated 1.9 Pg of terrestrial organic carbon that freshwater systems process per year, nearly half is respired by bacteria (3-5). When soil dissolved organic carbon outgassing is included, net freshwater carbon emissions are of the same order of magnitude as net oceanic uptake (2). While photochemical mineralization of organic carbon can predominate in lake habitats with high levels of photosynthetically active radiation (6), bacterial contributions to dissolved organic matter (DOM) mineralization are important as well (7).Nevertheless, linkages between the metabolism of organic carbon and specific populations remain limited, particularly in the less-studied hypolimnia of lakes, even for ubiquitous and highly abundant taxa, due to challenges with the isolation of representatives of these taxa (8). In recent years, the use of culture-independent methods has provided ins...

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“…Desulfitobacterium hafniense , a non‐acetogenic organism, has been found to employ these precursors solely for energy production through anaerobic respiration . In the case of the GB pathway, this organism uses a series of enzymes, MtgB, MtgC, and MtgA, to transfer one methyl group via Cbl to THF (Scheme ) . MtgA catalyzes methyl transfer from Cbl‐CH 3 to THF and lacks sequence identity towards solved protein structures .…”

Section: Methodsmentioning

confidence: 99%

“…Yellow box: In microbial glycine betaine (GB) metabolism, the methyl group (blue) is abstracted from GB and transferred to the N 5 atom of THF. In D. hafniense , THF‐CH 3 is formed by MtgA (pink) and further catabolized for energy production . The glutamyl‐ p ‐aminobenzoate moiety of THF is abbreviated as R.…”

Section: Methodsmentioning

confidence: 99%

Structures in Tetrahydrofolate Methylation in Desulfitobacterial Glycine Betaine Metabolism at Atomic Resolution

Badmann

Groll

2019

ChemBioChem

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Enzymes orchestrating methylation between tetrahydrofolate (THF) and cobalamin (Cbl) are abundant among all domains of life. During energy production in Desulfitobacterium hafniense, MtgA catalyzes the methyl transfer from methylcobalamin (Cbl‐CH3) to THF in the catabolism of glycine betaine (GB). Despite its lack of sequence identity with known structures, we could show that MtgA forms a homodimeric complex of two TIM barrels. Atomic crystallographic insights into the interplay of MtgA with THF as well as analysis of a trapped reaction intermediate (THF‐CH3)+ reveal conformational rearrangements during the transfer reaction. Whereas residues for THF methylation are conserved, the binding mode for the THF glutamyl‐p‐aminobenzoate moiety (THF tail) is unique. Apart from snapshots of individual reaction steps of MtgA, structure‐based mutagenesis combined with enzymatic activity assays allowed a mechanistic description of the methyl transfer between Cbl‐CH3 and THF. Altogether, the THF‐tail‐binding motion observed in MtgA is unique compared to other THF methyltransferases and therefore contributes to the general understanding of THF‐mediated methyl transfer.

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A nonpyrrolysine member of the widely distributed trimethylamine methyltransferase family is a glycine betaine methyltransferase

Cited by 78 publications

References 84 publications

Glycine betaine metabolism in the acetogenic bacterium Acetobacterium woodii

Glycine betaine metabolism in the acetogenic bacterium Acetobacterium woodii

Chloroflexi CL500-11 Populations That Predominate Deep-Lake Hypolimnion Bacterioplankton Rely on Nitrogen-Rich Dissolved Organic Matter Metabolism and C ₁ Compound Oxidation

Structures in Tetrahydrofolate Methylation in Desulfitobacterial Glycine Betaine Metabolism at Atomic Resolution

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A nonpyrrolysine member of the widely distributed trimethylamine methyltransferase family is a glycine betaine methyltransferase

Cited by 78 publications

References 84 publications

Glycine betaine metabolism in the acetogenic bacterium Acetobacterium woodii

Glycine betaine metabolism in the acetogenic bacterium Acetobacterium woodii

Chloroflexi CL500-11 Populations That Predominate Deep-Lake Hypolimnion Bacterioplankton Rely on Nitrogen-Rich Dissolved Organic Matter Metabolism and C 1 Compound Oxidation

Structures in Tetrahydrofolate Methylation in Desulfitobacterial Glycine Betaine Metabolism at Atomic Resolution

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Chloroflexi CL500-11 Populations That Predominate Deep-Lake Hypolimnion Bacterioplankton Rely on Nitrogen-Rich Dissolved Organic Matter Metabolism and C ₁ Compound Oxidation