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Sugar transport systems in Kluyveromyces marxianus CCT 7735

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Abstract

The pattern of glucose repression in most Kluyveromyces marxianus strains does not correlate with fermentative behaviour; however, glucose repression and fermentative metabolism appear to be linked to the kinetics of sugar uptake. In this work, we show that lactose transport in K. marxianus CCT 7735 by lactose-grown cells is mediated by a low-affinity H+-sugar symporter. This system is glucose repressed and able to transport galactose with low affinity. We also observed the activity of a distinct lactose transporter in response to raffinose. Regarding glucose uptake, specificities of at least three low-affinity systems rely on the carbon source available in a given growth medium. Interestingly, it was observed only one high-affinity system is able to transport both glucose and galactose. We also showed that K. marxianus CCT 7735 regulates the expression of sugar transport systems in response to glucose availability.

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References

  • André B (1995) An overview of membrane transport proteins in Saccharomyces cerevisiae. Yeast 11:1575–1611

    Article  PubMed  Google Scholar 

  • Blank LM, Lehmbeck F, Sauer U (2005) Metabolic-flux and network analysis in fourteen hemiascomycetous yeasts. FEMS Yeast Res 5:545–558

    Article  CAS  PubMed  Google Scholar 

  • Carvalho-Silva M, Spencer-Martins I (1990) Modes of lactose uptake in the yeast species Kluyveromyces marxianus. Antonie Van Leeuwenhoek 57:77–81

    Article  CAS  PubMed  Google Scholar 

  • De Bruijne AW, Schuddemat J, Van den Broek PJA, Van Steveninck J (1988) Regulation of sugar transport systems of Kluyveromyces marxianus: the role of carbohydrates and their catabolism. BBA - Biomembr 939:569–576

    Article  Google Scholar 

  • de Lima LA, Diniz RHS, de Queiroz MV, Fietto LG, Silveira WB (2018) Screening of Yeasts Isolated from Brazilian Environments for the 2-Phenylethanol (2-PE) Production. Biotechnol Bioprocess Eng 23:326–332

    Article  CAS  Google Scholar 

  • de Souza CJA, Costa DA, Rodrigues MQRB, dos Santos AF, Lopes MR, Abrantes ABP, dos Santos Costa P, Silveira WB, Passos FML, Fietto LG (2012) The influence of presaccharification, fermentation temperature and yeast strain on ethanol production from sugarcane bagasse. Bioresour Technol 109:63–69

    Article  CAS  PubMed  Google Scholar 

  • Diniz RHS, Silveira WB, Fietto LG, Passos FML (2012) The high fermentative metabolism of Kluyveromyces marxianus UFV-3 relies on the increased expression of key lactose metabolic enzymes. Antonie Van Leeuwenhoek 101:541–550

    Article  CAS  PubMed  Google Scholar 

  • Diniz RHS, Rodrigues MQRB, Fietto LG, Passos FML, Silveira WB (2014) Optimizing and validating the production of ethanol from cheese whey permeate by Kluyveromyces marxianus UFV-3. Biocatal Agric Biotechnol 3:111–117

    Article  Google Scholar 

  • Ferreira PG, da Silveira FA, dos Santos RCV, Genier HLA, Diniz RHS, Ribeiro JI, Fietto LG, Passos FML, da Silveira WB (2015) Optimizing ethanol production by thermotolerant Kluyveromyces marxianus CCT 7735 in a mixture of sugarcane bagasse and ricotta whey. Food Sci Biotechnol 24:1421–1427

    Article  CAS  Google Scholar 

  • Fiechter A, Fuhrmann GF, Kappeli E (1981) Regulation of glucose metabolism in growing yeast cells. Adv Microbiol Pysiol 22:123–183

    Article  CAS  Google Scholar 

  • Flores CL, Rodríguez C, Petit T, Gancedo C (2000) Carbohydrate and energy-yielding metabolism in non-conventional yeasts. FEMS Microbiol Rev 24:507–529

    CAS  PubMed  Google Scholar 

  • Fonseca GG, Heinzle E, Wittmann C, Gombert AK (2008) The yeast Kluyveromyces marxianus and its biotechnological potential. Appl Microbiol Biotechnol 79:339–354

    Article  CAS  PubMed  Google Scholar 

  • Fonseca GG, Carvalho NMB, Gombert AK (2013) Growth of the yeast Kluyveromyces marxianus CBS 6556 on different sugar combinations as sole carbon and energy source. Appl Microbiol Biotechnol 97:5055–5067

    Article  CAS  PubMed  Google Scholar 

  • Gabardo S, Pereira GF, Rech R, Ayub MAZ (2015) The modeling of ethanol production by Kluyveromyces marxianus using whey as substrate in continuous A-stat bioreactors. J Ind Microbiol Biotechnol 42:1243–1253

    Article  CAS  PubMed  Google Scholar 

  • Gancedo JM (2008) The early steps of glucose signalling in yeast. FEMS Microbiol Rev 32:673–704

    Article  CAS  PubMed  Google Scholar 

  • Gasnier B (1987) Characterization of low- and high-affinity glucose transports in the yeast Kluyveromyces marxianus. BBA - Biomembr 903:425–433

    Article  CAS  Google Scholar 

  • González-Siso MI (1996) The biotechnological utilization of cheese whey: a review. Bioresour Technol 57:1–11

    Article  Google Scholar 

  • González-Siso MI, Freire-Picos MA, Ramil E, González-Domínguez M, Rodríguez Torres A, Cerdán ME (2000) Respirofermentative metabolism in Kluyveromyces lactis: insights and perspective. Enzyme Microbiol Technol 26:699–705

    Article  Google Scholar 

  • Guimarães PMR, Teixeira JA, Domingues L (2010) Fermentation of lactose to bio-ethanol by yeasts as part of integrated solutions for the valorisation of cheese whey. Biotechnol Adv 28:375–384

    Article  CAS  PubMed  Google Scholar 

  • Henderson CM, Block DE (2014) Examining the role of membrane lipid composition in determining the ethanol tolerance of Saccharomyces cerevisiae. Appl Environ Microbiol 80:2966–2972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Höfer M, Misra PC (1978) Evidence for a proton/sugar symport in the yeast Rhodotorula gracilis (glutinis). Biochem J 172:15–22

    Article  PubMed  PubMed Central  Google Scholar 

  • Lages F, Silva-Graça M, Lucas C (1999) Active glycerol uptake is a mechanism underlying halotolerance in yeasts: a study of 42 species. Microbiol 145:2577–2585

    Article  CAS  Google Scholar 

  • Lane MM, Morrissey JP (2010) Kluyveromyces marxianus: a yeast emerging from its sister’ s shadow. Fungal Biol Rev 24:17–26

    Article  Google Scholar 

  • Lane MM, Burke N, Karreman R, Wolfe KH, O’Byrne CP, Morrissey JP (2011) Physiological and metabolic diversity in the yeast Kluyveromyces marxianus. Antonie Van Leeuwenhoek 100:507–519

    Article  CAS  PubMed  Google Scholar 

  • Loaces I, Rodríguez C, Amarelle V, Fabiano E, Noya F (2016) Improved glycerol to ethanol conversion by E. coli using a metagenomic fragment isolated from an anaerobic reactor. J Ind Microbiol Biotechnol 43:1405–1416

    Article  CAS  PubMed  Google Scholar 

  • Loureiro-Dias MC, Peinado JM (1982) Effect of ethanol and other alkanols on the maltose transport system of Saccharomyces cerevisiae. Biotechnol Lett 4:721–724

    Article  CAS  Google Scholar 

  • Loureiro-Dias MC, Peinado JM (1984) Transport of maltose in Saccahromyces cerevisiae. Effect of pH and potassium ions. Biochem J 222:293–298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Merico A, Sulo P, Piškur J, Compagno C (2007) Fermentative lifestyle in yeasts belonging to the Saccharomyces complex. FEBS J 274:976–989

    Article  CAS  PubMed  Google Scholar 

  • Merico A, Galafassi S, Piškur J, Compagno C (2009) The oxygen level determines the fermentation pattern in Kluyveromyces lactis. FEMS Yeast Res 9:749–756

    Article  CAS  PubMed  Google Scholar 

  • O’Shea DG, Walsh PK (1996) Morphological characterization of the dimorphic yeast Kluyveromyces marxianus var. marxianus NRRLy2415 by semi-automated image analysis. Biotechnol Bioeng 51:679–690

    Article  PubMed  Google Scholar 

  • Otterstedt K, Larseon C, Bill RM, Stahlberg A, Boles E, Hohmann S, Gustafsson L (2004) Switching the mode of metabolism in the yeast Saccharomyces cerevisiae. EMBO Rep 5:532–537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ozcan S, Johnston M (1995) Three different regulatory mechanisms enable yeast hexose transporter (HXT) genes to be induced by different levels of glucose. Mol Cell Biol 15:1564–1572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Postma E, Van Den Brooek PJA (1990) Continuous-culture study of the regulation of glucose and fructose transport in Kluyveromyces marxianis CBS 6556. L. Bacteriol 172:2871–2876

    Article  CAS  Google Scholar 

  • Prazeres AR, Carvalho F, Rivas J (2012) Cheese whey management: a review. J Environ Manag 110:48–68

    Article  CAS  Google Scholar 

  • Rocha SN, Abrahao-Neto J, Cerdan ME, Gonzalez-Siso MI, Gombert AK (2010) Heterologous expression of glucose oxidase in the yeast Kluyveromyces marxianus. Microb Cell Fact 9:4. https://doi.org/10.1186/1475-2859-9-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rubio-Texeira M (2006) Endless versatility in the biotechnological applications of Kluyveromyces LAC genes. Biotechnol Adv 24:212–225

    Article  CAS  PubMed  Google Scholar 

  • Schaffrath R, Breunig KD (2000) Genetics and molecular physiology of the yeast Kluyveromyces lactis. Fungal Genet Biol 30:173–190

    Article  CAS  PubMed  Google Scholar 

  • Silveira WB, Passos FJV, Mantovani HC, Passos FML (2005) Ethanol production from cheese whey permeate by Kluyveromyces marxianus UFV-3: a flux analysis of oxido-reductive metabolism as a function of lactose concentration and oxygen levels. Enzyme Microb Technol 36:930–936

    Article  CAS  Google Scholar 

  • Silveira WB, Diniz RHS, Cerdan ME, Gonzalez-Siso MI, Souza RA, Vidigal PMP, Brustolini OJB, de Almeida Prata ERB, Medeiros AC, Paiva LC, Nascimento M, Ferreira EG, dos Santos VC, Braganca CRS, Fernandes TAR, Colombo LT, Passos FML (2014) Genomic sequence of the yeast Kluyveromyces marxianus CCT 7735 (UFV-3), a highly lactose-fermenting yeast isolated from the Brazilian dairy industry. Genome Announc 2:e01136–14

    Article  PubMed  PubMed Central  Google Scholar 

  • Suomalainen H, Nurminen T, Oura E (1973) Aspects of cytology and metabolism of yeast. Prog Ind Microbiol 12:109–167

    CAS  PubMed  Google Scholar 

  • Varela JA, Montini N, Scully D, Van der Ploeg R, Oreb M, Boles E, Hirota J, Akada R, Hoshida H, Morrissey JP (2017) Polymorphisms in the LAC12 gene explain lactose utilisation variability in Kluyveromyces marxianus strains. FEMS Yeast Res 17:1–13

    Article  CAS  Google Scholar 

  • Yadav JS, Yan S, Pilli S, Kumar L, Tyagi RD, Surampalli RY (2015) Cheese whey: a potential resource to transform into bioprotein, functional/nutritional proteins and bioactive peptides. Biotechnol Adv 33:756–774

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was supported by the Brazilian Agencies CNPq (National Science and Technology Development Council), CAPES (Coordination for the Improvement of Higher Education Personnel) and FAPEMIG (Foundation for Research Support of the State of Minas Gerais). We also would like to acknowledge Federal University of Ouro Preto, MG, Brazil for financial support (Process N. 23109.003209/2016-98 Edital PROPP 09/2016) and Federal University of Viçosa, MG, Brazil.

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Considering the involvement, explained below, we believe that it is appropriate to include the following authors in the manuscript: Silveira FA, Diniz RHS, Sampaio GSS, Brandao, RL, Silveira WB and Castro IM. IMC and WBS: Conceived of or designed study. FAS, RHSD and GMSS: Performed research. IMC, WBS and RLB: Analyzed data and discussion relative. IMC and WBS: Wrote the paper.

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Correspondence to Ieso M. Castro.

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This work has not been published previously, it is not under consideration for publication anywhere else, and its publication in Antonie van Leeuwenhoek has been approved by all co-authors, as well as by the responsible authorities at the institutes where the work has been carried out. The authors ensure that accepted principles of ethical and professional conduct has been followed and absence of conflicts of interest.

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da Silveira, F.A., Diniz, R.H.S., Sampaio, G.M.S. et al. Sugar transport systems in Kluyveromyces marxianus CCT 7735. Antonie van Leeuwenhoek 112, 211–223 (2019). https://doi.org/10.1007/s10482-018-1143-4

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