Widespread Inter- and Intra-Domain Horizontal Gene Transfer of d-Amino Acid Metabolism Enzymes in Eukaryotes

Naranjo‐Ortiz, Miguel A.; Brock, Matthias; Brunke, Sascha; Hube, Bernhard; Marcet‐Houben, Marina; Gabaldón, Toni

doi:10.3389/fmicb.2016.02001

Cited by 20 publications

(25 citation statements)

References 91 publications

(124 reference statements)

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“…While HGT in eukaryotes has been the subject of controversy, there is an increasing number of gene families where HGT has been shown to play a role [11,55,56]. The results presented here show the evolutionary history of the nitrate assimilation pathway as a striking example of the importance that gene transfer between eukaryotes may have in the evolution of a certain metabolic pathway.…”

Section: Discussionmentioning

confidence: 77%

“…Adaptation to new environments requires metabolic remodeling, and HGT of metabolic genes between prokaryotes occurs at a higher rate than that of informational genes [8]; which may facilitate the recipients’ rapid adaptation [9]. Numerous metabolic pathways in eukaryotes are of bacterial origin [6], transferred from endosymbionts [10]; and many proposed HGTs between eukaryotes also involve metabolic genes [11–13]. Hence, patchily distributed metabolic pathways make good candidate subjects for investigation into possible events of HGT in eukaryotes.…”

Section: Introductionmentioning

confidence: 99%

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Reticulate evolution in eukaryotes: origin and evolution of the nitrate assimilation pathway

Ocaña‐Pallarès

Najle

Scazzocchio

et al. 2018

Preprint

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Genes and genomes can evolve through interchanging genetic material, this leading to reticular evolutionary patterns. However, the importance of reticulate evolution in eukaryotes, and in particular of horizontal gene transfer (HGT), remains controversial. Given that metabolic pathways with taxonomically-patchy distributions can be indicative of HGT events, the eukaryotic nitrate assimilation pathway is an ideal object of investigation, as previous results revealed a patchy distribution and suggested one crucial HGT event. We studied the evolution of this pathway through both multi-scale bioinformatic and experimental approaches. Our taxon-rich genomic screening shows this pathway to be present in more lineages than previously proposed and that nitrate assimilation is restricted to autotrophs and to distinct osmotrophic groups. Our phylogenies show a pervasive role of HGT, with three bacterial transfers contributing to the pathway origin, and at least seven well-supported transfers between eukaryotes. Our results, based on a larger dataset, differ from the previously proposed transfer of a nitrate assimilation cluster from Oomycota (Stramenopiles) to Dikarya (Fungi, Opisthokonta). We propose a complex HGT path involving at least two cluster transfers between Stramenopiles and Opisthokonta. We also found that gene fusion played an essential role in this evolutionary history, underlying the origin of the canonical eukaryotic nitrate reductase, and of a novel nitrate reductase in Ichthyosporea (Opisthokonta). We show that the ichthyosporean pathway, including this novel nitrate reductase, is physiologically active and transcriptionally co-regulated, responding to different nitrogen sources; similarly to distant eukaryotes with independent HGT-acquisitions of the pathway. This indicates that this pattern of transcriptional control evolved convergently in eukaryotes, favoring the proper integration of the pathway in the metabolic landscape. Our results highlight the importance of reticulate evolution in eukaryotes, by showing the crucial contribution of HGT and gene fusion in the evolutionary history of the nitrate assimilation pathway.

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Section: Discussionmentioning

confidence: 77%

Section: Introductionmentioning

confidence: 99%

Reticulate evolution in eukaryotes: origin and evolution of the nitrate assimilation pathway

Ocaña‐Pallarès

Najle

Scazzocchio

et al. 2018

Preprint

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“…The number of enzymes predicted to be specific for processing D-AAs annotated in plant genomes imply much more functions for these amino acids than currently known (Naranjo-Ortíz et al, 2016). However, it also raises the question about its metabolism in plants, especially how the abundance of different D-AAs is regulated.…”

Section: Introductionmentioning

confidence: 99%

AtDAT1 is a key enzyme of D-amino acid stimulated ethylene production inArabidopsis thaliana

Suárez

Hener

Lehnhardt

et al. 2019

Preprint

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Keywords: D-amino acids in plants, D-amino acid-stimulated ethylene production, D-amino acid 9 specific transaminase, D-methionine, 1-aminocyclopropane-1-carboxylic acid, ethylene, amino acid 10 malonylation 11 Manuscript type: Original research 12Abstract 15 D-enantiomers of proteinogenic amino acids (D-AAs) are found ubiquitously, but the knowledge 16 about their metabolism and functions in plants is scarce. A long forgotten phenomenon in this regard 17 is the D-AA-stimulated ethylene production in plants. As a starting point to investigate this effect the 18Arabidopsis accession Landsberg erecta (Ler) got into focus as it was found defective in 19 metabolizing D-AAs. Combining genetics and molecular biology of T-DNA lines and natural 20 variants together with biochemical and physiological approaches we could identify AtDAT1 as a 21 major D-AA transaminase in Arabidopsis. Atdat1 loss-of-function mutants and Arabidopsis 22 accessions with defective AtDAT1 alleles were not able to produce D-Ala, D-Glu and L-Met, the 23 metabolites of D-Met, anymore. This result corroborates the biochemical characterization of 24AtDAT1, which showed highest activity using D-Met as substrate. Germination of seedlings in light 25and dark led to enhanced growth inhibition of atdat1 mutants on D-Met. Ethylene measurements 26revealed an enhanced D-AA stimulated ethylene production in these mutants. According to initial 27 working models of this phenomenon D-Met is preferentially malonylated instead of the ethylene 28 precursor 1-aminocyclopropane-1-carboxylic acid (ACC). This decrease of ACC degradation should 29 then lead to the increase of ethylene production. We could observe in our studies a reciprocal relation 30 of malonylated methionine and ACC upon D-Met application and even significantly more malonyl-31 methionine in atdat1 mutants. Unexpectedly, the malonyl-ACC levels did not differ between mutants 32 and wild type in these experiments. With AtDAT1, the first central enzyme of plant D-AA 33 metabolism was characterized biochemically and physiologically. The specific effects of D-Met on 34 ACC metabolization, ethylene production and plant development of dat1 mutants unraveled the 35 impact of AtDAT1 on these processes, but they are not in full accordance to previous working 36 AtDAT1 regulates ethylene production 2 models. Instead, our results imply the influence of additional candidate factors or processes on D-37 AA-stimulated ethylene production which await to be uncovered. 38

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“…The number of enzymes predicted to be specific for processing D-AAs annotated in plant genomes implies much more functions for these AAs than currently known (Naranjo-Ortíz et al, 2016). However, it also raises the question about their metabolism in plants, especially how the abundance of different D-AAs is regulated.…”

Section: Introductionmentioning

confidence: 99%

AtDAT1 Is a Key Enzyme of D-Amino Acid Stimulated Ethylene Production in Arabidopsis thaliana

et al. 2019

View full text Add to dashboard Cite

D-Enantiomers of proteinogenic amino acids (D-AAs) are found ubiquitously, but the knowledge about their metabolism and functions in plants is scarce. A long forgotten phenomenon in this regard is the D-AA-stimulated ethylene production in plants. As a starting point to investigate this effect, the Arabidopsis accession Landsberg erecta (Ler) got into focus as it was found defective in metabolizing D-AAs. Combining genetics and molecular biology of T-DNA insertion lines and natural variants together with biochemical and physiological approaches, we could identify AtDAT1 as a major D-AA transaminase in Arabidopsis. Atdat1 loss-of-function mutants and Arabidopsis accessions with defective AtDAT1 alleles were unable to produce the metabolites of D-Met, D-Ala, D-Glu, and L-Met. This result corroborates the biochemical characterization, which showed highest activity of AtDAT1 using D-Met as a substrate. Germination of seedlings in light and dark led to enhanced growth inhibition of atdat1 mutants on D-Met. Ethylene measurements revealed an increased D-AA stimulated ethylene production in these mutants. According to initial working models of this phenomenon, D-Met is preferentially malonylated instead of the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC). This decrease of ACC degradation should then lead to the increase of ethylene production. We could observe a reciprocal relation of malonylated methionine and ACC upon D-Met application and significantly more malonyl-methionine in atdat1 mutants. Unexpectedly, the malonyl-ACC levels did not differ between mutants and wild type. With AtDAT1, the first central enzyme of plant D-AA metabolism was characterized biochemically and physiologically. The specific effects of D-Met on ACC metabolism, ethylene production, and plant development of dat1 mutants unraveled the impact of AtDAT1 on these processes; however, they are not in full accordance to previous working models. Instead, our results imply the influence of additional factors or processes on D-AA-stimulated ethylene production, which await to be uncovered.

show abstract

Widespread Inter- and Intra-Domain Horizontal Gene Transfer of d-Amino Acid Metabolism Enzymes in Eukaryotes

Cited by 20 publications

References 91 publications

Reticulate evolution in eukaryotes: origin and evolution of the nitrate assimilation pathway

Reticulate evolution in eukaryotes: origin and evolution of the nitrate assimilation pathway

AtDAT1 is a key enzyme of D-amino acid stimulated ethylene production inArabidopsis thaliana

AtDAT1 Is a Key Enzyme of D-Amino Acid Stimulated Ethylene Production in Arabidopsis thaliana

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