Evolution of the Oligopeptide Transporter Family

Authors: Kenny M Gomolplitinant Milton H Saier

Publish Date: 2011/02/24

Volume: 240, Issue: 2, Pages: 89-110

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Abstract

The oligopeptide transporter OPT family of peptide and ironsiderophore transporters includes members from both prokaryotes and eukaryotes but with restricted distribution in the latter domain Eukaryotic members were found only in fungi and plants with a single slime mold homologue clustering with the fungal proteins All functionally characterized eukaryotic peptide transporters segregate from the known ironsiderophore transporters on a phylogenetic tree Prokaryotic members are widespread deriving from many different phyla Although they belong only to the ironsiderophore subdivision genome context analyses suggest that many of them are peptide transporters OPT family proteins have 16 or occasionally 17 transmembranespanning αhelical segments TMSs We provide statistical evidence that the 16TMS topology arose via three sequential duplication events followed by a genefusion event for proteins with a seventeenth TMS The proposed pathway is as follows 2 TMSs → 4 TMSs → 8 TMSs → 16 TMSs → 17 TMSs The seventeenth Cterminal TMS which probably arose just once is found in just one phylogenetic group of these homologues Analyses for orthology revealed that a few phylogenetic clusters consist exclusively of orthologues but most have undergone intermixing suggestive of horizontal transfer It appears that in this family horizontal gene transfer was frequent among prokaryotes rare among eukaryotes and largely absent between prokaryotes and eukaryotes as well as between plants and fungi These observations provide guides for future structural and functional analyses of OPT family membersTransport proteins have been classified in the Transporter Classification Database TCDB wwwtcdborg Saier 2000a b Saier et al 2006 2009 The first class is composed of channels/pores which catalyze facilitated diffusion by an energyindependent process Electrochemical potential–driven transporters comprising the second class are stereospecific carriers catalyzing uniport antiport and/or symport Saier 2000c Busch and Saier 2004 Primary active transporters class 3 utilize a primary source of energy chemical electrical and/or solar to drive transport of a solute against a concentration gradient Saier 2000a Group translocators class 4 utilize a primary energy source to chemically alter a substrate in a process coupled to transport across a membrane Mitchell and Moyle 1958The oligopeptide transporter OPT TC 2A67 family consists of electrochemical potential–driven transporters class 2 All functionally characterized members of this family catalyze uptake of their solutes by a cationsolute symport mechanism Hauser et al 2001 Lubkowitz 2006 Yen et al 2001 Functionally characterized members consist of transporters specific for oligopeptides three to eight amino acids and ironsiderophores Yen et al 2001 Characterized peptide transporters transport oligopeptides glutathione and glutathione conjugates Kaur et al 2009 Lubkowitz et al 1998 Characterized “yellow stripe” YS homologues on the other hand mediate the uptake of metalchelating phytosiderophores including ironnicotinamine and complexes of iron with secondary amino acid derivatives such as mugineic acid and deoxymugineic acid Kaur et al 2009 The biochemical and physiological characteristics of several OPT homologues have been studied Lubkowitz 2006 Osawa et al 2006 Stacey et al 2008 Thakur et al 2008 Two highly conserved motifs NPG and KIPPR have been found in many OPT family proteins Koh et al 2002 The OPT family is not to be confused with the protondependent oligopeptide transporter POT or PTR TC 2A17 family Paulsen and Skurray 1994 the peptide transporters PepTs of the ATPbinding cassette ABC TC 3A15 superfamily Saier 2000a Busch and Saier 2004 or the peptide/acetylCoA transporters PATs of the major facilitator superfamily MFS TC 2A125 Pao et al 1998Oligopeptide transport plays important roles in nitrogen storage and mobilization quorum sensing differentiation sexual induction mating and pheromone sensing One of the yeast homologues is the sexual differentiation process ISP4 protein of Schizosaccharomyces pombe In yeast OPT family homologues transport oligopeptides which are commonly tri tetra and/or pentapeptides Wiles et al 2006 Recently it has been found that highaffinity Saccharomyces cerevisiae and Sc pombe glutathione transporters Hgt1p and OPT1 respectively belong to the OPT family Dworeck et al 2009 Kaur et al 2009In Candida albicans eight OPT genes have been identified encoding putative OPTs Almost all are represented by polymorphic alleles Reuss and Morschhauser 2006 OPT123∆ triple mutants were found to have a severe growth defect which could be rescued by reintroduction of a single copy of OPT1 OPT2 or OPT3 The various transporters differ in their substrate preferences as shown by the ability of strains expressing specific OPT genes to grow on peptides of defined length and sequence Reuss and Morschhauser 2006In plants many OPTs appear to be plasma membrane–embedded proteins that import substrates from the apoplasm the aqueous phase of the cell wall and the external environment They may play roles in plant growth and development Lubkowitz 2006 Unlike many other OPTs which function in longdistance transport of peptides or metals YS1 an Fe3+phytosiderophore uptake system of Zea mays is known to translocate substrates from the rhizosphere the region of the soil that is directly influenced by root secretions and associated with soil microbes Yen et al 2001 Curie et al 2001 Expression of the YS1 gene is increased in roots and shoots under irondeficient conditions Curie et al 2001 When YS1 is expressed in mutant yeast lacking its native iron uptake system it is able to correct the defect specifically in Fe3+ phytosiderophore–containing mediaIn Arabidopsis nine OPT paralogues have been identified Koh et al 2002 seven of which mediate transport of tetra and pentapeptides Cagnac et al 2004 showed that AtOPT6 can mediate uptake of glutathione derivatives and metal complexes which led them to suggest that it may also be involved in stress resistance

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