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The following article appeared in MicrobiologyOpen 2017;6:e00419; and may be found at https://doi.org/10.1002/mbo3.419 Received: 23 May 2016 | Revised: 23 September 2016 | Accepted: 28 September 2016 DOI: 10.1002/mbo3.419 ORIGINAL RESEARCH Diversification of the kinetic properties of yeast NADP- glutamate- dehydrogenase isozymes proceeds independently of their evolutionary origin Carlos Campero-Basaldua1 | Héctor Quezada2 | Lina Riego-Ruíz3 | Dariel Márquez1 | Erendira Rojas1 | James González1 | Mohammed El-Hafidi4 | Alicia González1 1Departamento de Bioquímica y Biología Estructural, Instituto de Fisiología Abstract Celular, Universidad Nacional Autónoma de In the yeast Saccharomyces cerevisiae, the ScGDH1 and ScGDH3 encoded glutamate México, Mexico City, México dehydrogenases (NADP- GDHs) catalyze the synthesis of glutamate from ammonium 2Laboratorio de Inmunología y Proteómica, Hospital Infantil de México and α- ketoglutarate (α- KG). Previous kinetic characterization showed that these Federico Gómez, Mexico City, México enzymes displayed different allosteric properties and respectively high or low rate of 3División de Biología Molecular, IPICYT, San α- KG utilization. Accordingly, the coordinated action of ScGdh1 and ScGdh3, regu- Luis Potosí, México 4Departamento de Biomedicina lated balanced α- KG utilization for glutamate biosynthesis under either fermentative Cardiovascular, Instituto Nacional de or respiratory conditions, safeguarding energy provision. Here, we have addressed the Cardiología Ignacio Chávez, Mexico City, México question of whether there is a correlation between the regulation and kinetic proper- ties of the NADP- GDH isozymes present in S. cerevisiae (ScGdh1 and ScGdh3), Correspondence Alicia González, Departamento de Kluyveromyces lactis (KlGdh1), and Lachancea kluyveri (LkGdh1) and their evolutionary Bioquímica y Biología Estructural, Instituto history. Our results show that the kinetic properties of K. lactis and L. kluyveri single de Fisiología Celular, Universidad Nacional Autónoma de México, Mexico City, México. NADP- GDHs are respectively similar to either ScGDH3 or ScGDH1, which arose from Email: [email protected] the whole genome duplication event of theS. cerevisiae lineage, although, KlGDH1 and Funding information LkGDH1 originated from a GDH clade, through an ancient interspecies hybridization Dirección General de Asuntos del Personal event that preceded the divergence between the Saccharomyces clade and the one Académico, UNAM, Grant/Award Number: IN201015; Consejo Nacional de Ciencia containing the genera Kluyveromyces, Lachancea, and Eremothecium. Thus, the kinetic y Tecnología, Grant/Award Number: properties which determine the NADP- GDHs capacity to utilize α- KG and synthesize CB-2014-239492-B glutamate do not correlate with their evolutionary origin. KEYWORDS functional diversification, glutamate dehydrogenase, kinetics, paralogous enzymes, phylogeny, yeast gene duplication 1 | INTRODUCTION glutamate and glutamine, whose amino groups are subsequently dis- tributed to other compounds. The five- carbon skeleton of these amino Two pathways determine glutamate biosynthesis in fungi: the NADP- acids derives from α- ketoglutarate (α- KG), an intermediate of the tri- dependent glutamate dehydrogenase (NADP- GDH) and the con- carboxylic acid cycle. Thus, glutamate biosynthesis represents a crucial certed action of glutamine synthetase (GS) and glutamate synthase intersection of carbon and nitrogen metabolism and, as such, its regula- (GOGAT) (Magasanik, 2003). These enzymes assimilate ammonium into tion must balance biosynthetic needs and energy production (DeLuna, This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2016 The Authors. MicrobiologyOpen published by John Wiley & Sons Ltd. MicrobiologyOpen. 2017;6:e419. www.MicrobiologyOpen.com | 1 of 18 https://doi.org/10.1002/mbo3.419 2 of 18 | CAMPERO- BASALDUA ET AL. Avendano, Riego, & Gonzalez, 2001). Redox homeostasis and defense the peculiar facultative metabolism of S. cerevisiae (Avendano et al., against oxidative stress are also influenced by glutamate biosynthesis 2005). since this amino acid is a glutathione precursor (Guillamon, van Riel, It has been proposed that in the S. cerevisiae lineage, a whole genome Giuseppin, & Verrips, 2001; Lee, Kim, Kang, Kim, & Maeng, 2012). duplication (WGD) event took place (Wolfe & Shields, 1997) and that Although the relative contribution of the two glutamate- producing a selected group of the resulting duplicated genes have been retained pathways to the biosynthesis of this amino acid varies among species in two copies among which are the paralogous ScGDH1 and ScGDH3 and growth conditions, it has been reported that NADP- GDH (1.4.1.4) genes (Seoighe & Wolfe, 1999). However, the evolutionary studies of plays a leading role in Schizosaccharomyces pombe, Aspergillus nidulans, the fungal NADP- GDHs have not addressed the characteristics of the Neurospora crassa, and Saccharomyces cerevisiae grown on ammonium pre- WGD ancestral- type genes which did not originate through WGD, as sole nitrogen source, in which inactivation of the NADP- GDH encod- and those present in the Saccharomycetes, which arose through WGD. ing genes, dramatically reduces growth rate (Fincham, 1951; Macheda, The Saccharomycetales (or Hemyascomycetes) group includes species Hynes, & Davis, 1999; Magasanik, 2003; Perysinakis, Kinghorn, & closely related to S. cerevisiae for which the genome sequence and Drainas, 1994). Modulation of NADP- GDH activity in vivo coordinates genetic manipulation resources are available, representing a valuable metabolic fluxes according to modifications in the availability of nitro- tool for functional evolutionary studies. The yeasts Kluyveromyces lac- gen and carbon sources and contributes to the maintenance of an equil- tis and Lachancea kluyveri descend from the pre- WGD ancestor, and ibrated redox state. In Candida albicans, S. pombe, and several Aspergillus have a single NADP- GDH- encoding gene, suggesting that no sporadic species, this modulation involves rate of α- ketoglutarate (KG) utilization duplications have occurred in this gene. With regard to the carbon me- through allosteric regulation and cooperative kinetics (Holmes, Collings, tabolism operating in these yeasts, it is evident that each one shows Farnden, & Shepherd, 1989; Noor & Punekar, 2005; Perysinakis et al., different levels of adaptation to the fermentative lifestyle:K. lactis me- 1994), whereas in Candida tropicalis, Candida pseudotropicalis, Candida tabolism is constitutively respiratory, for this reason, it cannot grow parapsilosis, Debaryomyces hansenii, and Aspergillus terreus, NADP- GDH anaerobically and does not produce respiratory- deficient mutants hyperbolic kinetics determines intermediate utilization (Alba- Lois et al., (Breunig et al., 2000). L. kluyveri displays an intermediate fermentative 2004; Choudhury & Punekar, 2009; Holmes et al., 1989). capacity between K. lactis and S. cerevisiae, it can grow anaerobically S. cerevisiae has two NADP- GDH isoforms namely ScGdh1 and and produce respiratory- deficient mutants on sugar- rich media, but it ScGdh3 (Avendano, Deluna, Olivera, Valenzuela, & Gonzalez, 1997). only ferments in the absence of oxygen (Moller, Olsson, & Piskur, 2001; ScGdh1 shows hyperbolic kinetics for α- KG saturation and is the pre- Moller et al., 2002), whereas in S. cerevisiae fermentative metabolism dominant isoform under exponential growth on glucose and when predominates whenever high sugar concentration is available regard- acetate plus raffinose are used as carbon sources (DeLuna et al., less of oxygen disponibility. It even represses respiratory metabolism in 2001; Tang, Sieg, & Trotter, 2011). While ScGdh3 is a cooperative the presence of high glucose or fructose concentration, through carbon enzyme displaying sigmoidal kinetics for α- KG utilization, this isoform catabolite repression (Gancedo, 1998). This yeast can grow anaerobi- contributes significantly to NADP- GDH activity during growth on cally and produce respiratory- deficient mutants (Gancedo, 1998). One ethanol as sole carbon source (Avendano et al., 2005; DeLuna et al., of the most prominent features of baker′s yeast is the rapid conversion 2001) and becomes the predominant isoform during stationary phase of sugars to ethanol and carbon dioxide under both anaerobic an aer- (Lee et al., 2012). Accordingly, transcription of the ScGDH3 gene is obic conditions; this phenomenon is called Crabtree effect (Hagman, strongly induced during growth on ethanol and is nearly absent on Säll, & Piskur, 2014) and is present in yeast species well adapted to glucose. This carbon- mediated regulation is overimposed to the tran- the fermentative life style (Pfeiffer & Morley,2014). According to this scriptional activation by low nitrogen availability (Avendano et al., classification,S. cerevisiae and L. kluyveri are Crabtree positive, whereas 2005). Although transcription of theScGDH1 gene is not repressed on K. lactis is Crabtree negative. ethanol, the relative contribution of theSc Gdh1 enzyme to the overall This work addresses the question of whether the evolutionary NADP- GDH activity is much lower than that of ScGdh3 under this origin of S. cerevisiae ScGdh1 and ScGdh3
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