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Research article

Biotechnology and Bioengineering (BB)  |  Bioenergy and Biorefinery

A New Isolation and Evaluation Method for Marine-Derived Yeast spp. with Potential Applications in Industrial Biotechnology

Abdelrahman Saleh Zaky 1, 2, 3, Darren Greetham 1, Edward J. Louis 4, Greg A. Tucker 1 and Chenyu Du 1, 2*

1Division of Food Sciences, School of Biosciences, University of Nottingham, Nottingham LE12 5RD, UK, 2School of Applied Sciences, University of Huddersfield, Huddersfield HD1 3DH, UK, 3Department of Microbiology, Faculty of Agriculture, Cairo University, Giza 12613, Egypt, 4Centre for Genetic Architecture of Complex Traits, Department of Genetics, University of Leicester, Leicester LE1 7RH, UK

Received: May 25, 2016; Accepted: July 14, 2016

J. Microbiol. Biotechnol. 2016; 26(11): 1891-1907

Published November 28, 2016 https://doi.org/10.4014/jmb.1605.05074

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

Yeasts that are present in marine environments have evolved to survive hostile environments that are characterized by high exogenous salt content, high concentrations of inhibitory compounds, and low soluble carbon and nitrogen levels. Therefore, yeasts isolated from marine environments could have interesting characteristics for industrial applications. However, the application of marine yeast in research or industry is currently very limited owing to the lack of a suitable isolation method. Current methods for isolation suffer from fungal interference and/or low number of yeast isolates. In this paper, an efficient and nonlaborious isolation method has been developed and successfully isolated large numbers of yeasts without bacterial or fungal growth. The new method includes a three-cycle enrichment step followed by an isolation step and a confirmation step. Using this method, 116 marine yeast strains were isolated from 14 marine samples collected in the UK, Egypt, and the USA. These strains were further evaluated for the utilization of fermentable sugars (glucose, xylose, mannitol, and galactose) using a phenotypic microarray assay. Seventeen strains with higher sugar utilization capacity than the reference terrestrial yeast Saccharomyces cerevisiae NCYC 2592 were selected for identification by sequencing of the ITS and D1/D2 domains. These strains belonged to six species: S. cerevisiae, Candida tropicalis, Candida viswanathii, Wickerhamomyces anomalus, Candida glabrata, and Pichia kudriavzevii. The ability of these strains for improved sugar utilization using seawater-based media was confirmed and, therefore, they could potentially be utilized in fermentations using marine biomass in seawater media, particularly for the production of bioethanol and other biochemical products.

Keywords

Marine Yeast, Phenotypic microarray, Identification, Screening, Fermentation, Seawater

References

  1. Ahearn DG, Roth FJ Jr, Meyers SP. 1968. Ecology and characterization of yeasts from aquatic regions of South Florida. Mar. Biol. 1: 291-308.
    CrossRef
  2. Bieleski RL. 1982. Sugar alcohols, pp. 158-192. In Loewus F, Tanner W (eds.). Plant Carbohydrates I. Springer, BerlinHeidelberg.
  3. Burgaud G, Arzur D, Durand L, Cambon-Bonavita M-A, Barbier G. 2010. Marine culturable yeasts in deep-sea hydrothermal vents: species richness and association with fauna. FEMS Microbiol. Ecol. 73: 121-133.
    CrossRef
  4. Cadete R, Fonseca C, Rosa C. 2014. Novel yeast strains from Brazilian biodiversity: biotechnological applications in lignocellulose conversion into biofuels, pp. 255-279. In da Silva SS, Chandel AK (eds.). Biofuels in Brazil. Springer International Publishing.
  5. Cavka A, Jönsson LJ. 2014. Comparison of the growth of filamentous fungi and yeasts in lignocellulose-derived media. Biocatal. Agric. Biotechnol. 3: 197-204.
    CrossRef
  6. Chi Z, Chi Z, Zhang T, Liu G, Li J, Wang X. 2009. Production, characterization and gene cloning of the extracellular enzymes from the marine-derived yeasts and their potential applications. Biotechnol. Adv. 27: 236-255.
    Pubmed CrossRef
  7. Dinesh Kumar S, Karthik L, Gaurav Kumar, Bhaskara Rao KV. 2011. Biosynthesis of silver nanoparticles from marine yeast and their antimicrobial activity against multidrug resistant pathogens. Pharmacol. Online 3: 1100-1111.
  8. Fell JW. 2001. Collection and identification of marine yeasts, pp. 347-356. Methods in Microbiology. Academic Press, Burlington.
    CrossRef
  9. Fell J, Statzell-Tallman A, Scorzetti G, Gutiérrez M. 2011. Five new species of yeasts from fresh water and marine habitats in the Florida Everglades. Antonie Van Leeuwenhoek 99: 533-549.
    Pubmed CrossRef
  10. Foschino R, Gallina S, Andrighetto C, Rossetti L, Galli A. 2004. Comparison of cultural methods for the identification and molecular investigation of yeasts from sourdoughs for Italian sweet baked products. FEMS Yeast Res. 4: 609-618.
    Pubmed CrossRef
  11. Greetham D, Wimalasena T, Kerruish DWM, Brindley S, Ibbett RN, Linforth RL, et al. 2 01 4. D evelopment o f a phenotypic assay for characterisation of ethanologenic yeast strain sensitivity to inhibitors released from lignocellulosic feedstocks. J. Ind. Microbiol. Biotechnol. 41: 931-945.
    Pubmed CrossRef
  12. Guo F-J, Ma Y, Xu H-M, Wang X-H, Chi Z-M. 2013. A novel killer toxin produced by the marine-derived yeast Wickerhamomyces anomalus YF07b. Antonie Van Leeuwenhoek 103: 737-746.
    Pubmed CrossRef
  13. Jones EBG, Suetrong S, Sakayaroj J, Bahkali A, AbdelWahab MA, Boekhout T, Pang KL. 2015. Classification of marine Ascomycota, Basidiomycota, Blastocladiomycota and Chytridiomycota. Fungal Diver. 73: 1-72.
    CrossRef
  14. Karsten U, Barrow KD, Nixdorf O, West JA, King RJ. 1997. Characterization of mannitol metabolism in the mangrove red alga Caloglossa leprieurii (Montagne) J.Agardh. Planta 201: 173-178.
    CrossRef
  15. Khambhaty Y, Upadhyay D, Kriplani Y, Joshi N, Mody K, Gandhi MR. 2013. Bioethanol from macroalgal biomass:utilization of marine yeast for production of the same. Bioenergy Res. 6: 188-195.
    CrossRef
  16. Kohlmeyer J, Kohlmeyer E. 1979. Yeasts, pp. 556-606. In Kohlmeyer J, Kohlmeyer E (eds.). Marine Mycology Academic Press, New York.
    CrossRef
  17. Koop K, Carter RA, Newell RC. 1982. Mannitol-fermenting bacteria as evidence for export from kelp beds. Limnol. Oceanogr. 27: 950-954.
    CrossRef
  18. Kumar S, Gupta R, Kumar G, Sahoo D, Kuhad RC. 2013. Bioethanol production from Gracilaria verrucosa, a red alga, in a biorefinery approach. Bioresour. Technol. 135: 150-156.
    Pubmed CrossRef
  19. Kurtzman CP, Fell J. 2006. Yeast systematics and phylogeny — implications of molecular identification methods for studies in ecology, pp. 11-30. In Péter G, Rosa C (eds.). Biodiversity and Ecophysiology of Yeasts. Springer, BerlinHeidelberg.
  20. Kurtzman C, Piškur J. 2006. Taxonomy and phylogenetic diversity among the yeasts, pp. 29-46. In Sunnerhagen P, Piskur J (eds.). Comparative Genomics. Springer, BerlinHeidelberg.
  21. Kurtzman CP, Mateo RQ, Kolecka A, Theelen B, Robert V, Boekhout T. 2015. Advances in yeast systematics and phylogeny and their use as predictors of biotechnologically important metabolic pathways. FEMS Yeast Res. 15: fov050.
    Pubmed CrossRef
  22. Kutty SN. 2009. Marine yeasts from the slope sediments of Arabian Sea and Bay of Bengal. PhD. Cochin University of Science and Technology, India.
  23. Kutty SN, Philip R. 2008. Marine yeasts — a review. Yeast 25: 465-483.
    Pubmed CrossRef
  24. Lin CSK, Luque R, Clark JH, Webb C, Du C. 2011. A seawater-based biorefining strategy for fermentative production and chemical transformations of succinic acid. Energy Environ. Sci. 4: 1471-1479.
    CrossRef
  25. Mitchell TG, White TJ, Taylor JW. 1992. Comparison of 5.8S ribosomal DNA sequences among the basidiomycetous yeast genera Cystofilobasidium, Filobasidium and Filobasidiella. J. Med. Vet. Mycol. 30: 207-218.
    Pubmed CrossRef
  26. Nagahama T, Hamamoto M, Nakase T, Horikoshi K. 1999. Kluyveromyces nonfermentans sp. nov., a new yeast species isolated from the deep sea. Int. J. Syst. Bacteriol. 49: 1 8991905.
  27. Nasr NF, Zaky AS, Daw ZY. 2010. Microbiological quality of active dry and compressed baker’s yeast sold in Egypt. J. Pure Appl. Microbiol. 4: 455-462.
  28. Obara N, Oki N, Okai M, Ishida M, Urano N. 2015. Development of a simple isolation method for yeast Saccharomyces cerevisiae with high fermentative activities from coastal waters. Stud. Sci. Technol. 4: 71-76.
  29. Oshoma CE, Greetham D, Louis EJ, Smart KA, Phister TG, Powell C, Du C. 2015. Screening of non-Saccharomyces cerevisiae strains for tolerance to formic acid in bioethanol fermentation. PLoS One 10: e0135626.
    Pubmed PMC CrossRef
  30. Ostergaard S, Olsson L, Johnston M, Nielsen J. 2000. Increasing galactose consumption by Saccharomyces cerevisiae through metabolic engineering of the GAL gene regulatory network. Nat. Biotechnol. 18: 1283-1286.
    Pubmed CrossRef
  31. Pincus DH, Orenga S, Chatellier S. 2007. Yeast identification — past, present, and future methods. Med. Mycol. 45: 97-121.
    Pubmed CrossRef
  32. Praphailong W, Van Gestel M, Fleet GH, Heard GM. 1997. Evaluation of the Biolog system for the identification of food and beverage yeasts. Lett. Appl. Microbiol. 24: 455-459.
    Pubmed CrossRef
  33. Reed RH, Davison IR, Chudek JA, Foster R. 1985. The osmotic role of mannitol in the Phaeophyta: an appraisal. Phycologia 24: 35-47.
    CrossRef
  34. Rhishipal R , Philip R. 1 998. S election of m arine yeasts f or the generation of single cell protein from prawn-shell waste. Bioresour. Technol. 65: 255-256.
    CrossRef
  35. Sarkar S, Pramanik A, Mitra A, Mukherjee J. 2010. Bioprocessing data for the production of marine enzymes. Mar. Drugs 8: 1323-1372.
    Pubmed PMC CrossRef
  36. Seshadri R, Sieburth JM. 1975. Seaweeds as a reservoir of Candida yeasts in inshore waters. Mar. Biol. 30: 105-117.
    CrossRef
  37. Silvi S, Barghini P, Aquilanti A, Juarez-Jimenez B, Fenice M. 2013. Physiologic and metabolic characterization of a new marine isolate (BM39) of Pantoea sp. producing high levels of exopolysaccharide. Microb. Cell Fact. 12: 10.
    Pubmed PMC CrossRef
  38. Urano N, Yamazaki M, Ueno R. 2001. Distribution of halotolerant and/or fermentative yeasts in aquatic environments. J. Tokyo Univ. Fish 87: 7.
  39. Wang L, Chi Z, Wang X, Ju L, Chi Z, Guo N. 2008. Isolation and characterization of Candida membranifaciens subsp. flavinogenie W14-3, a novel riboflavin-producing marine yeast. Microbiol. Res. 163: 255-266.
    Pubmed CrossRef
  40. Wenger JW, Schwartz K, Sherlock G. 2010. Bulk segregant analysis by high-throughput sequencing reveals a novel xylose utilization gene from Saccharomyces cerevisiae. PLoS Genet. 6: e1000942.
    Pubmed PMC CrossRef
  41. White T, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics, pp. 315-322. In Innis M, Gelfand D, Shinsky J, White T (eds.). PCR Protocols: A Guide to Methods and Applications. Academic Press, New York.
    CrossRef
  42. White WL, Coveny AH, Robertson J, Clements KD. 2010. Utilisation of mannitol by temperate marine herbivorous fishes. J. Exp. Mar. Biol. Ecol. 391: 50-56.
    CrossRef
  43. Wickerham LJ. 1951. Taxonomy of yeasts. US Dept. Agric. Tech. Bull. 1029: 1-56.
  44. Wimalasena TT, Greetham D, Marvin ME, Liti G, Chandelia Y, Hart A, et al. 2014. Phenotypic characterisation of Saccharomyces spp. yeast for tolerance to stresses encountered during fermentation of lignocellulosic residues to produce bioethanol. Microb. Cell Fact. 13: 47.
    Pubmed PMC CrossRef
  45. Zaki AM, Wimalasena TT, Greetham D. 2014. Phenotypic characterisation of Saccharomyces spp. for tolerance to 1butanol. J. Ind. Microbiol. Biotechnol. 41: 1627-1636.
    Pubmed CrossRef
  46. Zaky AS, Du C. 2014. The isolation of novel marine yeasts;a new procedure. 31(Suppl. 132). New Biotechnol. DOI: 10.1016/j.nbt.2014.05.1939.
    CrossRef
  47. Zaky AS, Tucker GA, Daw ZY, Du C. 2014. Marine yeast isolation and industrial application. FEMS Yeast Res. 14: 813-825.
    Pubmed PMC CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2016; 26(11): 1891-1907

Published online November 28, 2016 https://doi.org/10.4014/jmb.1605.05074

Copyright © The Korean Society for Microbiology and Biotechnology.

A New Isolation and Evaluation Method for Marine-Derived Yeast spp. with Potential Applications in Industrial Biotechnology

Abdelrahman Saleh Zaky 1, 2, 3, Darren Greetham 1, Edward J. Louis 4, Greg A. Tucker 1 and Chenyu Du 1, 2*

1Division of Food Sciences, School of Biosciences, University of Nottingham, Nottingham LE12 5RD, UK, 2School of Applied Sciences, University of Huddersfield, Huddersfield HD1 3DH, UK, 3Department of Microbiology, Faculty of Agriculture, Cairo University, Giza 12613, Egypt, 4Centre for Genetic Architecture of Complex Traits, Department of Genetics, University of Leicester, Leicester LE1 7RH, UK

Received: May 25, 2016; Accepted: July 14, 2016

Abstract

Yeasts that are present in marine environments have evolved to survive hostile environments
that are characterized by high exogenous salt content, high concentrations of inhibitory
compounds, and low soluble carbon and nitrogen levels. Therefore, yeasts isolated from
marine environments could have interesting characteristics for industrial applications.
However, the application of marine yeast in research or industry is currently very limited
owing to the lack of a suitable isolation method. Current methods for isolation suffer from
fungal interference and/or low number of yeast isolates. In this paper, an efficient and nonlaborious
isolation method has been developed and successfully isolated large numbers of
yeasts without bacterial or fungal growth. The new method includes a three-cycle enrichment
step followed by an isolation step and a confirmation step. Using this method, 116 marine
yeast strains were isolated from 14 marine samples collected in the UK, Egypt, and the USA.
These strains were further evaluated for the utilization of fermentable sugars (glucose, xylose,
mannitol, and galactose) using a phenotypic microarray assay. Seventeen strains with higher
sugar utilization capacity than the reference terrestrial yeast Saccharomyces cerevisiae NCYC
2592 were selected for identification by sequencing of the ITS and D1/D2 domains. These
strains belonged to six species: S. cerevisiae, Candida tropicalis, Candida viswanathii, Wickerhamomyces
anomalus, Candida glabrata, and Pichia kudriavzevii. The ability of these strains for improved
sugar utilization using seawater-based media was confirmed and, therefore, they could
potentially be utilized in fermentations using marine biomass in seawater media, particularly
for the production of bioethanol and other biochemical products.

Keywords: Marine Yeast, Phenotypic microarray, Identification, Screening, Fermentation, Seawater

References

  1. Ahearn DG, Roth FJ Jr, Meyers SP. 1968. Ecology and characterization of yeasts from aquatic regions of South Florida. Mar. Biol. 1: 291-308.
    CrossRef
  2. Bieleski RL. 1982. Sugar alcohols, pp. 158-192. In Loewus F, Tanner W (eds.). Plant Carbohydrates I. Springer, BerlinHeidelberg.
  3. Burgaud G, Arzur D, Durand L, Cambon-Bonavita M-A, Barbier G. 2010. Marine culturable yeasts in deep-sea hydrothermal vents: species richness and association with fauna. FEMS Microbiol. Ecol. 73: 121-133.
    CrossRef
  4. Cadete R, Fonseca C, Rosa C. 2014. Novel yeast strains from Brazilian biodiversity: biotechnological applications in lignocellulose conversion into biofuels, pp. 255-279. In da Silva SS, Chandel AK (eds.). Biofuels in Brazil. Springer International Publishing.
  5. Cavka A, Jönsson LJ. 2014. Comparison of the growth of filamentous fungi and yeasts in lignocellulose-derived media. Biocatal. Agric. Biotechnol. 3: 197-204.
    CrossRef
  6. Chi Z, Chi Z, Zhang T, Liu G, Li J, Wang X. 2009. Production, characterization and gene cloning of the extracellular enzymes from the marine-derived yeasts and their potential applications. Biotechnol. Adv. 27: 236-255.
    Pubmed CrossRef
  7. Dinesh Kumar S, Karthik L, Gaurav Kumar, Bhaskara Rao KV. 2011. Biosynthesis of silver nanoparticles from marine yeast and their antimicrobial activity against multidrug resistant pathogens. Pharmacol. Online 3: 1100-1111.
  8. Fell JW. 2001. Collection and identification of marine yeasts, pp. 347-356. Methods in Microbiology. Academic Press, Burlington.
    CrossRef
  9. Fell J, Statzell-Tallman A, Scorzetti G, Gutiérrez M. 2011. Five new species of yeasts from fresh water and marine habitats in the Florida Everglades. Antonie Van Leeuwenhoek 99: 533-549.
    Pubmed CrossRef
  10. Foschino R, Gallina S, Andrighetto C, Rossetti L, Galli A. 2004. Comparison of cultural methods for the identification and molecular investigation of yeasts from sourdoughs for Italian sweet baked products. FEMS Yeast Res. 4: 609-618.
    Pubmed CrossRef
  11. Greetham D, Wimalasena T, Kerruish DWM, Brindley S, Ibbett RN, Linforth RL, et al. 2 01 4. D evelopment o f a phenotypic assay for characterisation of ethanologenic yeast strain sensitivity to inhibitors released from lignocellulosic feedstocks. J. Ind. Microbiol. Biotechnol. 41: 931-945.
    Pubmed CrossRef
  12. Guo F-J, Ma Y, Xu H-M, Wang X-H, Chi Z-M. 2013. A novel killer toxin produced by the marine-derived yeast Wickerhamomyces anomalus YF07b. Antonie Van Leeuwenhoek 103: 737-746.
    Pubmed CrossRef
  13. Jones EBG, Suetrong S, Sakayaroj J, Bahkali A, AbdelWahab MA, Boekhout T, Pang KL. 2015. Classification of marine Ascomycota, Basidiomycota, Blastocladiomycota and Chytridiomycota. Fungal Diver. 73: 1-72.
    CrossRef
  14. Karsten U, Barrow KD, Nixdorf O, West JA, King RJ. 1997. Characterization of mannitol metabolism in the mangrove red alga Caloglossa leprieurii (Montagne) J.Agardh. Planta 201: 173-178.
    CrossRef
  15. Khambhaty Y, Upadhyay D, Kriplani Y, Joshi N, Mody K, Gandhi MR. 2013. Bioethanol from macroalgal biomass:utilization of marine yeast for production of the same. Bioenergy Res. 6: 188-195.
    CrossRef
  16. Kohlmeyer J, Kohlmeyer E. 1979. Yeasts, pp. 556-606. In Kohlmeyer J, Kohlmeyer E (eds.). Marine Mycology Academic Press, New York.
    CrossRef
  17. Koop K, Carter RA, Newell RC. 1982. Mannitol-fermenting bacteria as evidence for export from kelp beds. Limnol. Oceanogr. 27: 950-954.
    CrossRef
  18. Kumar S, Gupta R, Kumar G, Sahoo D, Kuhad RC. 2013. Bioethanol production from Gracilaria verrucosa, a red alga, in a biorefinery approach. Bioresour. Technol. 135: 150-156.
    Pubmed CrossRef
  19. Kurtzman CP, Fell J. 2006. Yeast systematics and phylogeny — implications of molecular identification methods for studies in ecology, pp. 11-30. In Péter G, Rosa C (eds.). Biodiversity and Ecophysiology of Yeasts. Springer, BerlinHeidelberg.
  20. Kurtzman C, Piškur J. 2006. Taxonomy and phylogenetic diversity among the yeasts, pp. 29-46. In Sunnerhagen P, Piskur J (eds.). Comparative Genomics. Springer, BerlinHeidelberg.
  21. Kurtzman CP, Mateo RQ, Kolecka A, Theelen B, Robert V, Boekhout T. 2015. Advances in yeast systematics and phylogeny and their use as predictors of biotechnologically important metabolic pathways. FEMS Yeast Res. 15: fov050.
    Pubmed CrossRef
  22. Kutty SN. 2009. Marine yeasts from the slope sediments of Arabian Sea and Bay of Bengal. PhD. Cochin University of Science and Technology, India.
  23. Kutty SN, Philip R. 2008. Marine yeasts — a review. Yeast 25: 465-483.
    Pubmed CrossRef
  24. Lin CSK, Luque R, Clark JH, Webb C, Du C. 2011. A seawater-based biorefining strategy for fermentative production and chemical transformations of succinic acid. Energy Environ. Sci. 4: 1471-1479.
    CrossRef
  25. Mitchell TG, White TJ, Taylor JW. 1992. Comparison of 5.8S ribosomal DNA sequences among the basidiomycetous yeast genera Cystofilobasidium, Filobasidium and Filobasidiella. J. Med. Vet. Mycol. 30: 207-218.
    Pubmed CrossRef
  26. Nagahama T, Hamamoto M, Nakase T, Horikoshi K. 1999. Kluyveromyces nonfermentans sp. nov., a new yeast species isolated from the deep sea. Int. J. Syst. Bacteriol. 49: 1 8991905.
  27. Nasr NF, Zaky AS, Daw ZY. 2010. Microbiological quality of active dry and compressed baker’s yeast sold in Egypt. J. Pure Appl. Microbiol. 4: 455-462.
  28. Obara N, Oki N, Okai M, Ishida M, Urano N. 2015. Development of a simple isolation method for yeast Saccharomyces cerevisiae with high fermentative activities from coastal waters. Stud. Sci. Technol. 4: 71-76.
  29. Oshoma CE, Greetham D, Louis EJ, Smart KA, Phister TG, Powell C, Du C. 2015. Screening of non-Saccharomyces cerevisiae strains for tolerance to formic acid in bioethanol fermentation. PLoS One 10: e0135626.
    Pubmed KoreaMed CrossRef
  30. Ostergaard S, Olsson L, Johnston M, Nielsen J. 2000. Increasing galactose consumption by Saccharomyces cerevisiae through metabolic engineering of the GAL gene regulatory network. Nat. Biotechnol. 18: 1283-1286.
    Pubmed CrossRef
  31. Pincus DH, Orenga S, Chatellier S. 2007. Yeast identification — past, present, and future methods. Med. Mycol. 45: 97-121.
    Pubmed CrossRef
  32. Praphailong W, Van Gestel M, Fleet GH, Heard GM. 1997. Evaluation of the Biolog system for the identification of food and beverage yeasts. Lett. Appl. Microbiol. 24: 455-459.
    Pubmed CrossRef
  33. Reed RH, Davison IR, Chudek JA, Foster R. 1985. The osmotic role of mannitol in the Phaeophyta: an appraisal. Phycologia 24: 35-47.
    CrossRef
  34. Rhishipal R , Philip R. 1 998. S election of m arine yeasts f or the generation of single cell protein from prawn-shell waste. Bioresour. Technol. 65: 255-256.
    CrossRef
  35. Sarkar S, Pramanik A, Mitra A, Mukherjee J. 2010. Bioprocessing data for the production of marine enzymes. Mar. Drugs 8: 1323-1372.
    Pubmed KoreaMed CrossRef
  36. Seshadri R, Sieburth JM. 1975. Seaweeds as a reservoir of Candida yeasts in inshore waters. Mar. Biol. 30: 105-117.
    CrossRef
  37. Silvi S, Barghini P, Aquilanti A, Juarez-Jimenez B, Fenice M. 2013. Physiologic and metabolic characterization of a new marine isolate (BM39) of Pantoea sp. producing high levels of exopolysaccharide. Microb. Cell Fact. 12: 10.
    Pubmed KoreaMed CrossRef
  38. Urano N, Yamazaki M, Ueno R. 2001. Distribution of halotolerant and/or fermentative yeasts in aquatic environments. J. Tokyo Univ. Fish 87: 7.
  39. Wang L, Chi Z, Wang X, Ju L, Chi Z, Guo N. 2008. Isolation and characterization of Candida membranifaciens subsp. flavinogenie W14-3, a novel riboflavin-producing marine yeast. Microbiol. Res. 163: 255-266.
    Pubmed CrossRef
  40. Wenger JW, Schwartz K, Sherlock G. 2010. Bulk segregant analysis by high-throughput sequencing reveals a novel xylose utilization gene from Saccharomyces cerevisiae. PLoS Genet. 6: e1000942.
    Pubmed KoreaMed CrossRef
  41. White T, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics, pp. 315-322. In Innis M, Gelfand D, Shinsky J, White T (eds.). PCR Protocols: A Guide to Methods and Applications. Academic Press, New York.
    CrossRef
  42. White WL, Coveny AH, Robertson J, Clements KD. 2010. Utilisation of mannitol by temperate marine herbivorous fishes. J. Exp. Mar. Biol. Ecol. 391: 50-56.
    CrossRef
  43. Wickerham LJ. 1951. Taxonomy of yeasts. US Dept. Agric. Tech. Bull. 1029: 1-56.
  44. Wimalasena TT, Greetham D, Marvin ME, Liti G, Chandelia Y, Hart A, et al. 2014. Phenotypic characterisation of Saccharomyces spp. yeast for tolerance to stresses encountered during fermentation of lignocellulosic residues to produce bioethanol. Microb. Cell Fact. 13: 47.
    Pubmed KoreaMed CrossRef
  45. Zaki AM, Wimalasena TT, Greetham D. 2014. Phenotypic characterisation of Saccharomyces spp. for tolerance to 1butanol. J. Ind. Microbiol. Biotechnol. 41: 1627-1636.
    Pubmed CrossRef
  46. Zaky AS, Du C. 2014. The isolation of novel marine yeasts;a new procedure. 31(Suppl. 132). New Biotechnol. DOI: 10.1016/j.nbt.2014.05.1939.
    CrossRef
  47. Zaky AS, Tucker GA, Daw ZY, Du C. 2014. Marine yeast isolation and industrial application. FEMS Yeast Res. 14: 813-825.
    Pubmed KoreaMed CrossRef