Horizontal gene transfer from Bacteria to rumen Ciliates indicates adaptation to their anaerobic, carbohydrates-rich environment

Ricard, Guénola; McEwan, Neil R.; Dutilh, Bas E.; Jouany, J. P.; Machebœuf, Didier; Mitsumori, Makoto; McIntosh, Freda M.; Michałowski, Tadeusz; Nagamine, Takafumi; Nelson, Nancy L.; Newbold, C. J.; Nsabimana, E; Takénaka, Akio; Thomas, Nadine A.; Ushida, Kazunari; Hackstein, J.H.P.; Huynen, Martijn A.

doi:10.1186/1471-2164-7-22

Cited by 149 publications

(120 citation statements)

References 60 publications

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“…However, although one of the Tetrahymena genes does not possess sequence similarity to bacterial AdoMetDC in the N-terminal domain, the other two genes have N-terminal domains with strong similarity to bacterial sequences, especially from the Firmicutes phylum. This suggests that the Tetrahymena fusion protein genes have been recently acquired from bacteria by horizontal gene transfer, a relatively common occurrence in ciliates (57). The most parsimonious explanation for the origin of the SpmSyn N-terminal domain is that it was acquired after the divergence of the fungal and metazoan ancestors but before the origin of multicellularity in animals, suggesting that the N-terminal domain was eukaryotic in origin.…”

Section: Discussionmentioning

confidence: 98%

Crystal Structure of Human Spermine Synthase

Min

Zeng

et al. 2008

Journal of Biological Chemistry

105

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The crystal structures of two ternary complexes of human spermine synthase (EC 2.5.1.22), one with 5-methylthioadenosine and spermidine and the other with 5-methylthioadenosine and spermine, have been solved. They show that the enzyme is a dimer of two identical subunits. Each monomer has three domains: a C-terminal domain, which contains the active site and is similar in structure to spermidine synthase; a central domain made up of four ␤-strands; and an N-terminal domain with remarkable structural similarity to S-adenosylmethionine decarboxylase, the enzyme that forms the aminopropyl donor substrate. Dimerization occurs mainly through interactions between the N-terminal domains. Deletion of the N-terminal domain led to a complete loss of spermine synthase activity, suggesting that dimerization may be required for activity. The structures provide an outline of the active site and a plausible model for catalysis. The active site is similar to those of spermidine synthases but has a larger substrate-binding pocket able to accommodate longer substrates. Two residues (Asp 201 and Asp 276 ) that are conserved in aminopropyltransferases appear to play a key part in the catalytic mechanism, and this role was supported by the results of site-directed mutagenesis. The spermine synthase⅐5-methylthioadenosine structure provides a plausible explanation for the potent inhibition of the reaction by this product and the stronger inhibition of spermine synthase compared with spermidine synthase. An analysis to trace possible evolutionary origins of spermine synthase is also described.Polyamines are essential for normal growth and development, and the polyamine biosynthetic pathway is an important target for the design of therapeutic agents (1, 2). The predominant polyamines in mammalian cells are spermidine (SPD) 4 and spermine (SPM). These polyamines are made by the sequential addition of aminopropyl groups from decarboxylated S-adenosylmethionine (dcAdoMet). The addition of the first aminopropyl group to the diamine precursor putrescine is catalyzed by spermidine synthase (SpdSyn). The addition of a second aminopropyl group to the N-10 position 5 of SPD to form SPM is catalyzed by spermine synthase (SpmSyn) (Fig. 1). The critical importance of polyamines is demonstrated by studies using mice with gene deletions of ornithine decarboxylase (3) or S-adenosylmethionine decarboxylase (AdoMetDC) (4), both of which are lethal at the earliest stages of embryonic development. No SpdSyn knock-out mice have been described, but studies in yeast show that this gene is required for viability and that SPD plays an essential role as a precursor of hypusine formed in the post-translational modification of eukaryotic initiation factor 5A (5). SpmSyn has received relatively little attention compared with the large number of publications describing ornithine decarboxylase, AdoMetDC, and SpdSyn (1, 6 -8). The SpmSyn gene is not essential for growth of yeast (9). Mutants lacking the AdoMetDC gene, which cannot make SPD or SPM, grow normally when ...

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Section: Discussionmentioning

confidence: 98%

Crystal Structure of Human Spermine Synthase

Min

Zeng

et al. 2008

Journal of Biological Chemistry

105

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“…It would seem a strange coincidence, then, that all of the eukaryotic enzymes that function exclusively in anaerobic metabolism discussed above lack the characteristic a-proteobacterial affinity of mitochondrial proteins. Even if LGT has completely obscured the phylogenetic origins of these enzymes in eukaryotes, given that prokaryote-to-eukaryote LGT is now a well-established phenomenon [123][124][125][126], there is no strong reason to suspect they originated from the mitochondrial symbiont genome rather than some other bacterial source.…”

Section: (A) Hydrogen Hypothesismentioning

confidence: 99%

Diversity and origins of anaerobic metabolism in mitochondria and related organelles

Stairs

Leger

Roger

2015

Phil. Trans. R. Soc. B

135

172

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One contribution of 17 to a theme issue 'Eukaryotic origins: progress and challenges'. Across the diversity of life, organisms have evolved different strategies to thrive in hypoxic environments, and microbial eukaryotes ( protists) are no exception. Protists that experience hypoxia often possess metabolically distinct mitochondria called mitochondrion-related organelles (MROs). While there are some common metabolic features shared between the MROs of distantly related protists, these organelles have evolved independently multiple times across the breadth of eukaryotic diversity. Until recently, much of our knowledge regarding the metabolic potential of different MROs was limited to studies in parasitic lineages. Over the past decade, deep-sequencing studies of free-living anaerobic protists have revealed novel configurations of metabolic pathways that have been co-opted for life in low oxygen environments. Here, we provide recent examples of anaerobic metabolism in the MROs of free-living protists and their parasitic relatives. Additionally, we outline evolutionary scenarios to explain the origins of these anaerobic pathways in eukaryotes.

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“…Although the frequency of HGT is generally substantially lower in eukaryotic genomes compared to prokaryotic ones (Keeling and Palmer, 2008; Andersson, 2009), notable examples that invoke as well as showcase HGT's influence on eukaryotic evolution include the green plant radiation onto dry land (Yue et al, 2012), the repeated colonization of animal digestive tracts by microbial eukaryotes (Garcia-Vallve et al, 2000; Ricard et al, 2006), and even adaptation to life in boiling acid lakes in extremophile algae (Schönknecht et al, 2013). Elevated rates of HGT have also been coincident with the loss of typical eukaryotic traits such as sexual reproduction (Boschetti et al, 2012) and aerobic growth (Andersson et al, 2003; Loftus et al, 2005; Pombert et al, 2012).…”

Section: Genetic Nomads—gene Innovation Through Horizontal Gene Transfermentioning

confidence: 99%

Fungal metabolic gene clustersâ€”caravans traveling across genomes and environments

2015

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Metabolic gene clusters (MGCs), physically co-localized genes participating in the same metabolic pathway, are signature features of fungal genomes. MGCs are most often observed in specialized metabolism, having evolved in individual fungal lineages in response to specific ecological needs, such as the utilization of uncommon nutrients (e.g., galactose and allantoin) or the production of secondary metabolic antimicrobial compounds and virulence factors (e.g., aflatoxin and melanin). A flurry of recent studies has shown that several MGCs, whose functions are often associated with fungal virulence as well as with the evolutionary arms race between fungi and their competitors, have experienced horizontal gene transfer (HGT). In this review, after briefly introducing HGT as a source of gene innovation, we examine the evidence for HGT's involvement on the evolution of MGCs and, more generally of fungal metabolism, enumerate the molecular mechanisms that mediate such transfers and the ecological circumstances that favor them, as well as discuss the types of evidence required for inferring the presence of HGT in MGCs. The currently available examples indicate that transfers of entire MGCs have taken place between closely related fungal species as well as distant ones and that they sometimes involve large chromosomal segments. These results suggest that the HGT-mediated acquisition of novel metabolism is an ongoing and successful ecological strategy for many fungal species.

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Horizontal gene transfer from Bacteria to rumen Ciliates indicates adaptation to their anaerobic, carbohydrates-rich environment

Cited by 149 publications

References 60 publications

Crystal Structure of Human Spermine Synthase

Crystal Structure of Human Spermine Synthase

Diversity and origins of anaerobic metabolism in mitochondria and related organelles

Fungal metabolic gene clustersâ€”caravans traveling across genomes and environments

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