Methanogens: a window into ancient sulfur metabolism

Liu, Yuchen; Beer, Laura L.; Whitman, William B.

doi:10.1016/j.tim.2012.02.002

Cited by 92 publications

(82 citation statements)

References 67 publications

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“…Cysteine, thiosulfate, thiophosphate, and sulfide were previously tested as possible sulfur sources, but only sulfide supported the formation of thiolated tRNA exhibiting retarded migration in APM gels (32). The K M of Na 2 S (∼1 mM) (32) is close to the estimated intracellular concentrations of free sulfide in methanococci (∼1-3 mM) (41), suggesting that sulfide is a physiologically relevant sulfur donor. In this study, the anoxically purified M. maripaludis ThiI, which contained a [3Fe-4S] cluster, was active to produce thiolated tRNA when using M. jannaschii tRNA Cys , Na 2 S, and ATP as the substrates (Fig.…”

Section: Thii Sepcyss and The Ncs6 Homolog In Methanogenic Archaeamentioning

confidence: 97%

A [3Fe-4S] cluster is required for tRNA thiolation in archaea and eukaryotes

Liu

Vinyard

Reesbeck

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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The sulfur-containing nucleosides in transfer RNA (tRNAs) are present in all three domains of life; they have critical functions for accurate and efficient translation, such as tRNA structure stabilization and proper codon recognition. The tRNA modification enzymes ThiI (in bacteria and archaea) and Ncs6 (in archaea and eukaryotic cytosols) catalyze the formation of 4-thiouridine (s 4 U) and 2-thiouridine (s 2 U), respectively. The ThiI homologs were proposed to transfer sulfur via cysteine persulfide enzyme adducts, whereas the reaction mechanism of Ncs6 remains unknown. Here we show that ThiI from the archaeon Methanococcus maripaludis contains a [3Fe-4S] cluster that is essential for its tRNA thiolation activity. Furthermore, the archaeal and eukaryotic Ncs6 homologs as well as phosphoseryl-tRNA (Sep-tRNA):Cys-tRNA synthase (SepCysS), which catalyzes the Sep-tRNA to Cys-tRNA conversion in methanogens, also possess a [3Fe-4S] cluster similar to the methanogenic archaeal ThiI. These results suggest that the diverse tRNA thiolation processes in archaea and eukaryotic cytosols share a common mechanism dependent on a [3Fe-4S] cluster for sulfur transfer.iron-sulfur cluster | thionucleosides | tRNA modification | CTU1

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Section: Thii Sepcyss and The Ncs6 Homolog In Methanogenic Archaeamentioning

confidence: 97%

A [3Fe-4S] cluster is required for tRNA thiolation in archaea and eukaryotes

Liu

Vinyard

Reesbeck

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…A different suggestion has it that eukaryotes and archaea are directly descended from actinobacteria, but that the cause of higher sequence similarity in eukaryote-bacterial comparisons stems from cataclysmic elevation of the substitution rate in archaea, which are however suggested to have arisen about 800 My ago (33), despite evidence that archaea are far more ancient (34). De Duve argued that the host for the origin of mitochondria was a bacterium, the archaeal genes (and ribosomes) of eukaryotes having been acquired via LGT from archaea (35).…”

Section: Unexpected Bacterial Genes In Eukaryotic Genomesmentioning

confidence: 99%

Endosymbiotic gene transfer from prokaryotic pangenomes: Inherited chimerism in eukaryotes

Nelson-Sathi

Roettger

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

119

105

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Endosymbiotic theory in eukaryotic-cell evolution rests upon a foundation of three cornerstone partners-the plastid (a cyanobacterium), the mitochondrion (a proteobacterium), and its host (an archaeon)-and carries a corollary that, over time, the majority of genes once present in the organelle genomes were relinquished to the chromosomes of the host (endosymbiotic gene transfer). However, notwithstanding eukaryote-specific gene inventions, single-gene phylogenies have never traced eukaryotic genes to three single prokaryotic sources, an issue that hinges crucially upon factors influencing phylogenetic inference. In the age of genomes, single-gene trees, once used to test the predictions of endosymbiotic theory, now spawn new theories that stand to eventually replace endosymbiotic theory with descriptive, gene tree-based variants featuring supernumerary symbionts: prokaryotic partners distinct from the cornerstone trio and whose existence is inferred solely from single-gene trees. We reason that the endosymbiotic ancestors of mitochondria and chloroplasts brought into the eukaryotic-and plant and algal-lineage a genome-sized sample of genes from the proteobacterial and cyanobacterial pangenomes of their respective day and that, even if molecular phylogeny were artifact-free, sampling prokaryotic pangenomes through endosymbiotic gene transfer would lead to inherited chimerism. Recombination in prokaryotes (transduction, conjugation, transformation) differs from recombination in eukaryotes (sex). Prokaryotic recombination leads to pangenomes, and eukaryotic recombination leads to vertical inheritance. Viewed from the perspective of endosymbiotic theory, the critical transition at the eukaryote origin that allowed escape from Muller's ratchet-the origin of eukaryotic recombination, or sex-might have required surprisingly little evolutionary innovation.endosymbiosis | evolution | mitochondria | lateral gene transfer | plastids

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“…enes that function in sulfate assimilation and sulfur trafficking in aerobic organisms are often not identifiable in the genomes of methanogens and other anaerobes, suggesting that these ancient organisms may retain metabolic vestiges characteristic of life on the early earth (1). In aerobes, sulfur is imported into the cell as sulfate, which is reduced to sulfide in an ATP-dependent pathway (2).…”

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“…1, left), which is required for protein synthesis and incorporation into S-adenosylmethionine. In contrast, Cys is required for protein synthesis, plays a key role in the biosynthesis of coenzyme A and glutathione, and functions as a sulfur donor for the synthesis of a wide range of sulfur-containing compounds (1). Sulfur is mobilized from Cys by the activity of cysteine desulfurase (CD), which removes sulfane (S°) from Cys to yield a persulfide-modified Cys residue (C ␤-S-SH ) in the active site ( Fig.…”

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confidence: 99%

Efficient Sulfide Assimilation in Methanosarcina acetivorans Is Mediated by the MA1715 Protein

Rauch

Perona

2016

J Bacteriol

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Conserved genes essential to sulfur assimilation and trafficking in aerobic organisms are missing in many methanogens, most of which inhabit highly sulfidic, anaerobic environmental niches. This suggests that methanogens possess distinct pathways for the synthesis of key metabolites and intermediates, including cysteine, homocysteine, and protein persulfide groups. Prior work identified a novel tRNA-dependent two-step pathway for cysteine biosynthesis and a new metabolic transformation by which sulfur is inserted into aspartate semialdehyde to produce homocysteine. Homocysteine biosynthesis requires two of the three proteins previously identified in our laboratory by a comprehensive bioinformatics approach. Here, we show that the third protein identified in silico, the ApbE-like protein COG2122, facilitates sulfide assimilation in Methanosarcina acetivorans. Knockout strains lacking the gene encoding COG2122 are severely impaired for growth when sulfide is provided as the sole sulfur source. However, rapid growth is recovered upon supplementation with cysteine, homocysteine, or cystathionine, suggesting that COG2122 is required for efficient biosynthesis of both cysteine and homocysteine. Deletion of the gene encoding COG2122 does not influence the extent of sulfur modifications in tRNA or the prevalence of iron-sulfur clusters, indicating that the function of COG2122 could be limited to sulfide assimilation for cysteine and homocysteine biosynthesis alone. IMPORTANCEWe have found that the conserved M. acetivorans ma1715 gene, which encodes an ApbE-like protein, is required for optimal growth with sulfide as the sole sulfur source and supports both cysteine and homocysteine biosynthesis in vivo. Together with related functional-genomics studies in methanogens, these findings make a key contribution to elucidating the novel pathways of sulfide assimilation and sulfur trafficking in anaerobic microorganisms that existed before the advent of oxygenic photosynthesis. The data suggest that the MA1715 protein is particularly important to sustaining robust physiological function when ambient sulfide concentrations are low. Phylogenetic analysis shows that MA1715 and other recently discovered methanogen sulfur-trafficking proteins share an evolutionary history with enzymes in the methanogenesis pathway. The newly characterized genes thus likely formed an essential part of the core metabolic machinery of the ancestral euryarchaeote. Genes that function in sulfate assimilation and sulfur trafficking in aerobic organisms are often not identifiable in the genomes of methanogens and other anaerobes, suggesting that these ancient organisms may retain metabolic vestiges characteristic of life on the early earth (1). In aerobes, sulfur is imported into the cell as sulfate, which is reduced to sulfide in an ATP-dependent pathway (2). In turn, sulfide is incorporated directly into activated serine and homoserine derivatives to yield cysteine (Cys) and homocysteine (Hcy), respectively (Fig. 1, left) (3). Cys and Hcy can al...

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Methanogens: a window into ancient sulfur metabolism

Cited by 92 publications

References 67 publications

A [3Fe-4S] cluster is required for tRNA thiolation in archaea and eukaryotes

A [3Fe-4S] cluster is required for tRNA thiolation in archaea and eukaryotes

Endosymbiotic gene transfer from prokaryotic pangenomes: Inherited chimerism in eukaryotes

Efficient Sulfide Assimilation in Methanosarcina acetivorans Is Mediated by the MA1715 Protein

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