Cold-adaptation in Sea-water-borne Signal Proteins: Sequence and NMR Structure of the Pheromone En-6 from the Antarctic Ciliate Euplotes nobilii

Pedrini, Bill; Placzek, William J.; Koculi, Eda; Alimenti, Claudio; Terza, Antonietta La; Luporini, Pierangelo; Wüthrich, Kurt

doi:10.1016/j.jmb.2007.06.046

Cited by 24 publications

(22 citation statements)

References 41 publications

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“…3A). However, despite this low extent of amino acid sequence identity, close homology among the three-dimensional NMR solution structures of the three Antarctic pheromones was previously established (20)(21)(22). We have now investigated that this structural homology extends to the pheromones of the Arctic strains, by purifying the pheromone En-A1 from the strain 4Pyrm4 (which can be grown in large cultures more easily than any of the other Arctic strains) and by determining its NMR structure in solution (Table S4).…”

Section: Resultsmentioning

confidence: 99%

“…The horizontal lines at the top indicate the disulfide bonds, which are common to both groups of pheromones. The boxes identify the locations of helical secondary structures in the four pheromones for which three-dimensional structures are available (20)(21)(22). (B) Ribbon presentations of the previously determined En-1, En-2 and En-6 pheromone solution NMR structures from the Antartic E. nobilii strains AC-1 and AC-4 (20,21).…”

Section: Discussionmentioning

confidence: 99%

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Antarctic and Arctic populations of the ciliate Euplotes nobilii show common pheromone-mediated cell-cell signaling and cross-mating

Giuseppe

Erra

Dini

et al. 2011

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

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Wild-type strains of the protozoan ciliate Euplotes collected from different locations on the coasts of Antarctica, Tierra del Fuego and the Arctic were taxonomically identified as the morpho-species Euplotes nobilii, based on morphometric and phylogenetic analyses. Subsequent studies of their sexual interactions revealed that mating combinations of Antarctic and Arctic strains form stable pairs of conjugant cells. These conjugant pairs were isolated and shown to complete mutual gene exchange and cross-fertilization. The biological significance of this finding was further substantiated by demonstrating that close homology exists among the threedimensional structures determined by NMR of the water-borne signaling pheromones that are constitutively secreted into the extracellular space by these interbreeding strains, in which these molecules trigger the switch between the growth stage and the sexual stage of the life cycle. The fact that Antarctic and Arctic E. nobilii populations share the same gene pool and belong to the same biological species provides new support to the biogeographic model of global distribution of eukaryotic microorganisms, which had so far been based exclusively on studies of morphological and phylogenetic taxonomy.ciliate mating types and sexual interactions | microbial ecology | NMR structures | polar biology | signaling by water-borne pheromones

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Antarctic and Arctic populations of the ciliate Euplotes nobilii show common pheromone-mediated cell-cell signaling and cross-mating

Giuseppe

Erra

Dini

et al. 2011

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

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“…All of them were obtained by a PCR strategy based on: (i) the knowledge of the sequence of the pheromone gene en-ant6 that, as reported elsewhere [13], was cloned earlier using a genetic approach developed in relation to the structural characterization of the pheromone En-6 specified by this gene [10]; (ii) the assumption that the sequences of the E. nobilii pheromone genes, like those of the E. octocarinatus pheromone genes [14,15] equivalent to the sub-telomeric sequences of the known pheromone gene en-ant6.…”

Section: Pheromone Gene Identification and Cloningmentioning

confidence: 99%

“…Previously we determined the conformations of a set of these E. nobilii pheromones by analysis of nuclear magnetic resonance of native protein preparations, and showed the relationships of structural homology that make these molecules able to bind their target cell receptors in competition with one another [10,11]. Now we have determined the full-length sequences of the functional genes that, in form of individual and multiple "gene-sized DNA molecules" [12, as a review], develop from the chromosomic locus mat of the micronucleus and determine the synthesis of these pheromones in the transcriptionally active genome of the somatic nucleus (macronucleus).…”

Section: Introductionmentioning

confidence: 99%

“…Three genes (designated en-ant1, en-ant2 and en-ant6) encode the pheromones En-1, En-2, and En-6 of Antarctic origin, that have already been isolated from preparations of culture supernatant and structurally characterized [10,11]; the four other genes (designated en-arc1, en-arc2, en-arc3, and en-arc4) specify the pheromones En-A1, En-A2, En-A3, and En-A4 of Arctic origin, that have not yet been purified and analyzed chemically. …”

Section: Introductionmentioning

confidence: 99%

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Characterization of the pheromone gene family of an Antarctic and Arctic protozoan ciliate, Euplotes nobilii

Vallesi¹,

Alimenti²,

Terza³

et al. 2009

Marine Genomics

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Allelic genes encoding water-borne signal proteins (pheromones) were amplified and sequenced from the somatic (macronuclear) sub-chromosomic genome of Antarctic and Arctic strains of the marine ciliate, Euplotes nobilii. Their open reading frames appeared to be specific for polypeptide sequences of 83 to 94 amino acids identifiable with cytoplasmic pheromone precursors (pre-pro-pheromones), requiring two proteolytic steps to remove the pre-and pro-segments and secrete the mature pheromones. Differently from most of the macronuclear genes that have so far been characterized from Euplotes and other hypotrich ciliates, the 5' and 3' non-coding regions of all the seven E. nobilii pheromone genes are much longer than the coding regions (621 to 700 versus 214 to 285 nucleotides), and the 5' regions in particular show nearly identical sequences across the whole set of pheromone genes. These structural peculiarities of the non-coding regions are likely due to the presence of intron sequences and provide presumptive evidence that they are site of basic, conserved activities in the mechanism that regulates the expression of the E. nobilii pheromone genes. AbstractAllelic genes encoding water-borne signal proteins (pheromones) were amplified and sequenced from the somatic (macronuclear) sub-chromosomic genome of Antarctic and Arctic strains of the marine ciliate, Euplotes nobilii. Their open reading frames appeared to be specific for polypeptide sequences of 83 to 94 amino acids identifiable with cytoplasmic pheromone precursors (pre-propheromones), requiring two proteolytic steps to remove the pre-and pro-segments and secrete the mature pheromones. Differently from most of the macronuclear genes that have so far been characterized from Euplotes and other hypotrich ciliates, the 5' and 3' non-coding regions of all the seven E. nobilii pheromone genes are much longer than the coding regions (621 to 700 versus 214 to 285 nucleotides), and the 5' regions in particular show nearly identical sequences across the whole set of pheromone genes. These structural peculiarities of the non-coding regions are likely due to the presence of intron sequences and provide presumptive evidence that they are site of basic, conserved activities in the mechanism that regulates the expression of the E. nobilii pheromone genes.3

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Molecular cold‐adaptation: Comparative analysis of two homologous families of psychrophilic and mesophilic signal proteins of the protozoan ciliate, Euplotes

et al. 2009

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SummaryUnique opportunities are provided by phylogenetically closely related organisms thriving in stably cold, or temperate milieus to study adaptive modifications of structurally homologous molecules. These modifications are of keen interest in basic science as well as in biotechnology. This review highlights structural and functional specificities that differentiate two homologous families of psychrophilic and mesophilic water-borne proteins (designated as pheromones) that signal mitotic growth and sexual mating in two marine species of the protozoan ciliate Euplotes, i.e., E. nobilii, which is distributed in Antarctic and Arctic waters, and E. raikovi, which inhabits temperate waters. The two protein families show strict conservation of a common three-helix bundle in a compact core of the molecular structure, which provides long-lasting integrity and biological activity to these molecules in their natural environment. In the psychrophilic pheromone family, cold-adaptation appears to have been achieved by superimposing an integrated complex of structural modifications on this conserved scaffold. Functionally most relevant appear to be extensions of polypeptide segments devoid of regular secondary structures, a specific distribution of polar and hydrophobic amino acids, the presence of solvent-exposed clusters of negatively charged amino acid side chains, and a unique role of aromatic residues in anchoring the molecular architecture. Due to these modifications, the psychrophilic pheromones are an example of an elegant combination of high stability of the three-dimensional structures with sufficient structural plasticity for efficient functioning at their physiologically low temperatures.2009 IUBMB IUBMB Life, 61(8): 838-845, 2009

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Cold-adaptation in Sea-water-borne Signal Proteins: Sequence and NMR Structure of the Pheromone En-6 from the Antarctic Ciliate Euplotes nobilii

Cited by 24 publications

References 41 publications

Antarctic and Arctic populations of the ciliate Euplotes nobilii show common pheromone-mediated cell-cell signaling and cross-mating

Antarctic and Arctic populations of the ciliate Euplotes nobilii show common pheromone-mediated cell-cell signaling and cross-mating

Characterization of the pheromone gene family of an Antarctic and Arctic protozoan ciliate, Euplotes nobilii

Molecular cold‐adaptation: Comparative analysis of two homologous families of psychrophilic and mesophilic signal proteins of the protozoan ciliate, Euplotes

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