The role of transport proteins in the production of microbial glycolipid biosurfactants

Abstract

Several microorganisms are currently being used as production platform for glycolipid biosurfactants, providing a greener alternative to chemical biosurfactants. One of the reasons why these processes are commercially competitive is the fact that microbial producers can efficiently export their product to the extracellular environment, reaching high product titers. Glycolipid biosynthetic genes are often found in a dedicated cluster, amidst which genes encoding a dedicated transporter committed to shuttle the glycolipid to the extracellular environment are often found, as is the case for many other secondary metabolites. Knowing this, one can rely on gene clustering features to screen for novel putative transporters, as described and performed in this review. The above strategy proves to be very powerful to identify glycolipid transporters in fungi but is less valid for bacterial systems. Indeed, the genetics of these export systems are currently largely unknown, but some hints are given. Apart from the direct export of the glycolipid, several other transport systems have an indirect effect on glycolipid production. Specific importers dictate which hydrophilic and hydrophobic substrates can be used for production and influence the final yields. In eukaryotes, cellular compartmentalization allows the assembly of glycolipid building blocks in a highly specialized and efficient way. Yet, this requires controlled transport across intracellular membranes. Next to the direct export of glycolipids, the current state of the art regarding this indirect involvement of transporter systems in microbial glycolipid synthesis is summarized in this review.

Key points

• Transporters are directly and indirectly involved in microbial glycolipid synthesis.

• Yeast glycolipid transporters are found in their biosynthetic gene cluster.

• Hydrophilic and hydrophobic substrate uptake influence microbial glycolipid synthesis.

Graphical abstract

This is a preview of subscription content, access via your institution.

Fig. 1

References

  1. Abdel-Mawgoud AM, Stephanopoulos G (2018) Simple glycolipids of microbes: chemistry, biological activity and metabolic engineering. Synth Syst Biotechnol 3:3–19. https://doi.org/10.1016/j.synbio.2017.12.001

    Article  PubMed  Google Scholar 

  2. Abdel-Mawgoud AM, Lépine F, Déziel E (2010) Rhamnolipids: Diversity of structures, microbial origins and roles. Appl Microbiol Biotechnol 86:1323–1336. https://doi.org/10.1007/s00253-010-2498-2

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. Abdel-Mawgoud AM, Hausmann R, Lépine F, Müller MM, Déziel E (2011) Rhamnolipids: detection, analysis, biosynthesis, genetic regulation, and bioengineering of production. In: Biosurfactants. Springer, Berlin, Heidelberg, pp 13–55

  4. Araki N, Suzuki T, Miyauchi K, Kasai D, Masai E, Fukuda M (2011) Identification and characterization of uptake systems for glucose and fructose in Rhodococcus jostii RHA1. J Mol Microbiol Biotechnol 20:125–136. https://doi.org/10.1159/000324330

    CAS  Article  PubMed  Google Scholar 

  5. Ashby RD, Solaiman DKY (2010) The influence of increasing media methanol concentration on sophorolipid biosynthesis from glycerol-based feedstocks. Biotechnol Lett 32:1429–1437

    CAS  Article  Google Scholar 

  6. Backus KM, Boshoff HI, Barry CS, Boutureira O, Patel MK, D’Hooge F, Lee SS, Via LE, Tahlan K, Barry CE, Davis BG (2011) Uptake of unnatural trehalose analogs as a reporter for Mycobacterium tuberculosis. Nat Chem Biol 7:228–235. https://doi.org/10.1038/nchembio.539

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. Baral B (2017) Evolutionary trajectories of entomopathogenic fungi ABC transporters. Adv Genet 98:117–154. https://doi.org/10.1016/bs.adgen.2017.07.002

    CAS  Article  PubMed  Google Scholar 

  8. Barrett MP (1999) Structure and function of facilitative sugar transporters. Curr Opin Cell Biol 11:496–502

    CAS  Article  Google Scholar 

  9. Belardinelli JM, Stevens CM, Li W, Tan YZ, Jones V, Mancia F, Zgurskaya HI, Jackson M (2019) The MmpL3 interactome reveals a complex crosstalk between cell envelope biosynthesis and cell elongation and division in mycobacteria. Sci Rep 9:1–14. https://doi.org/10.1038/s41598-019-47159-8

    CAS  Article  Google Scholar 

  10. Black PN, Dirusso CC (2003) Transmembrane movement of exogenous long-chain fatty acids: proteins, enzymes and vectorial esterification. Microbiol Mol Biol Rev 67:454–472. https://doi.org/10.1128/MMBR.67.3.454

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. Boyarskiy S, Tullman-Ercek D (2015) Getting pumped: membrane efflux transporters for enhanced biomolecule production. Curr Opin Chem Biol 28:15–19. https://doi.org/10.1016/j.cbpa.2015.05.019

    CAS  Article  PubMed  Google Scholar 

  12. Brennan PJ, Nikaido H (1995) The envelope of mycobacteria. Annu Rev Biochem 64:29–63

    CAS  Article  Google Scholar 

  13. Brown NA, Ries LNA, Goldman GH (2014) How nutritional status signalling coordinates metabolism and lignocellulolytic enzyme secretion. Fungal Genet Biol 72:48–63. https://doi.org/10.1016/j.fgb.2014.06.012

    CAS  Article  PubMed  Google Scholar 

  14. Camões F, Islinger M, Guimarães SC, Kilaru S, Schuster M, Godinho LF, Steinberg G, Schrader M (2015) New insights into the peroxisomal protein inventory: Acyl-CoA oxidases and -dehydrogenases are an ancient feature of peroxisomes. Biochim Biophys Acta, Mol Cell Res 1853:111–125. https://doi.org/10.1016/j.bbamcr.2014.10.005

    CAS  Article  PubMed  Google Scholar 

  15. Canto A, Herrera CM, Rodriguez R (2017) Nectar-living yeasts of a tropical host plant community: diversity and effects on community-wide floral nectar traits. PeerJ. 2017:1–22. https://doi.org/10.7717/peerj.3517

    Article  Google Scholar 

  16. Chattopadhyay A, Singh R, Das AK, Maiti MK (2020) Characterization of two sugar transporters responsible for efficient xylose uptake in an oleaginous yeast Candida tropicalis SY005. Arch Biochem Biophys 695:108645. https://doi.org/10.1016/j.abb.2020.108645

    CAS  Article  PubMed  Google Scholar 

  17. Chen Y, Nielsen J (2013) Advances in metabolic pathway and strain engineering paving the way for sustainable production of chemical building blocks. Curr Opin Biotechnol 24:965–972

    CAS  Article  Google Scholar 

  18. Ciesielska K, Li B, Groeneboer S, Van Bogaert INA, Lin YC, Soetaert W, Van De Peer Y, Devreese B (2013) SILAC-based proteome analysis of Starmerella bombicola sophorolipid production. J Proteome Res 12:4376–4392. https://doi.org/10.1021/pr400392a

    CAS  Article  PubMed  Google Scholar 

  19. Daddaoua A, Krell T, Ramos JL (2009) Regulation of glucose metabolism in Pseudomonas. The phosphorylative branch and Entner-Doudoroff enzymes are regulated by a repressor containing a sugar isomerase domain. J Biol Chem 284:21360–21368. https://doi.org/10.1074/jbc.M109.014555

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. De Graeve M, De Maeseneire SL, Roelants SLKW, Soetaert W (2018) Starmerella bombicola, an industrially relevant, yet fundamentally underexplored yeast. FEMS Yeast Res 18:1–13. https://doi.org/10.1093/femsyr/foy072

    CAS  Article  Google Scholar 

  21. Del Castillo T, Duque E, Ramos JL (2008) A set of activators and repressors control peripheral glucose pathways in Pseudomonas putida to yield a common central intermediate. J Bacteriol 190:2331–2339. https://doi.org/10.1128/JB.01726-07

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. Dupont C, Chen Y, Xu Z, Roquet-Banères F, Blaise M, Witt A-K, Dubar F, Biot C, Guérardel Y, Maurer FP, others (2019) A piperidinol-containing molecule is active against Mycobacterium tuberculosis by inhibiting the mycolic acid flippase activity of MmpL3. J Biol Chem 294:17512–17523

  23. Faria NT, Santos MV, Fernandes P, Fonseca LL, Fonseca C, Ferreira FC (2014) Production of glycolipid biosurfactants, mannosylerythritol lipids, from pentoses and d-glucose/d-xylose mixtures by Pseudozyma yeast strains. Process Biochem 49:1790–1799. https://doi.org/10.1016/j.procbio.2014.08.004

    CAS  Article  Google Scholar 

  24. Fay A, Czudnochowski N, Rock JM, Johnson JR, Krogan NJ, Rosenberg O, Glickman MS (2019) Two accessory proteins govern MmpL3 mycolic acid transport in mycobacteria. MBio. 10:1–17. https://doi.org/10.1128/mBio.00850-19

    Article  Google Scholar 

  25. Ferreira C, van Voorst F, Martins A, Neves L, Oliveira R, Kielland-Brandt MC, Lucas C, Brandt A (2005) A member of the sugar transporter family, Stl1p is the glycerol/H+ symporter in Saccharomyces cerevisiae. Mol Biol Cell 16:2068–2076

    CAS  Article  Google Scholar 

  26. Franzetti A, Gandolfi I, Bestetti G, Smyth TJP (2010) Production and applications of trehalose lipid biosurfactants. Eur J Lipid Sci Technol 112:617–627. https://doi.org/10.1002/ejlt.200900162

    CAS  Article  Google Scholar 

  27. Freitag J, Ast J, Linne U, Stehlik T, Martorana D, Bölker M, Sandrock B (2014) Peroxisomes contribute to biosynthesis of extracellular glycolipids in fungi. Mol Microbiol 93:24–36. https://doi.org/10.1111/mmi.12642

    CAS  Article  PubMed  Google Scholar 

  28. Fukuoka T, Morita T, Konishi M, Imura T, Kitamoto D (2007) Characterization of new types of mannosylerythritol lipids as biosurfactants produced from soybean oil by a basidiomycetous yeast, Pseudozyma shanxiensis. J Oleo Sci 56:435–442. https://doi.org/10.5650/jos.56.435

  29. Gao R, Falkeborg M, Xu X, Guo Z (2013) Production of sophorolipids with enhanced volumetric productivity by means of high cell density fermentation. Appl Microbiol Biotechnol 97:1103–1111. https://doi.org/10.1007/s00253-012-4399-z

    CAS  Article  PubMed  Google Scholar 

  30. Gonçalves C, Wisecaver JH, Kominek J, Salema Oom M, Leandro MJ, Shen XX, Opulente DA, Zhou X, Peris D, Kurtzman CP, Hittinger CT, Rokas A, Gonçalves P (2018) Evidence for loss and reacquisition of alcoholic fermentation in a fructophilic yeast lineage. Elife. 7:1–28. https://doi.org/10.7554/eLife.33034

    Article  Google Scholar 

  31. Gonçalves P, Gonçalves C, Brito PH, Sampaio JP (2020) The Wickerhamiella/Starmerella clade—a treasure trove for the study of the evolution of yeast metabolism. Yeast. 37:313–320. https://doi.org/10.1002/yea.3463

  32. Goulet KM, Saville BJ (2017) Carbon acquisition and metabolism changes during fungal biotrophic plant pathogenesis: insights from Ustilago maydis. Can J Plant Pathol 39:247–266. https://doi.org/10.1080/07060661.2017.1354330

    CAS  Article  Google Scholar 

  33. Günther M, Grumaz C, Lorenz S, Stevens P, Lindemann E, Hirth T, Sohn K, Zibek S, Rupp S (2015) The transcriptomic profile of Pseudozyma aphidis during production of mannosylerythritol lipids. Appl Microbiol Biotechnol 99:1375–1388. https://doi.org/10.1007/s00253-014-6359-2

    CAS  Article  PubMed  Google Scholar 

  34. Guo J, Wang Y, Li B, Huang S, Chen Y, Guo X, Xiao D (2017) Development of a one-step gene knock-out and knock-in method for metabolic engineering of Aureobasidium pullulans. J Biotechnol 251:145–150. https://doi.org/10.1016/j.jbiotec.2017.04.029

    CAS  Article  PubMed  Google Scholar 

  35. Haskins RH (1950) Biochemistry of the Ustilaginales I. Preliminary cultural studies of Ustilago zeae. Can J Res 28c:213–223

    CAS  Article  Google Scholar 

  36. Hemamalini R, Khare S (2014) A proteomic approach to understand the role of the outer membrane porins in the organic solvent-tolerance of Pseudomonas aeruginosa PseA. PLoS One 9:e103788

    CAS  Article  Google Scholar 

  37. Henkel M, Müller MM, Kügler JH, Lovaglio RB, Contiero J, Syldatk C, Hausmann R (2012) Rhamnolipids as biosurfactants from renewable resources: concepts for next-generation rhamnolipid production. Process Biochem 47:1207–1219. https://doi.org/10.1016/j.procbio.2012.04.018

    CAS  Article  Google Scholar 

  38. Hewald S, Linne U, Scherer M, Marahiel MA, Kamper J, Bolker M (2006) Identification of a gene cluster for biosynthesis of mannosylerythritol lipids in the Basidiomycetous fungus Ustilago maydis. Appl Environ Microbiol 72:5469–5477. https://doi.org/10.1128/AEM.00506-06

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. Ichihara T, Tohata M, Hayase A, Fumikazu T (2019) Sophorolipid Highly-Productive Mutant Strain. U.S. Patent No. 10,435,684.

  40. Ito S, Inoue S (1982) Sophorolipids from Torulopsis bombicola: possible relation to alkane uptake. Appl Environ Microbiol 43:1278–1283. https://doi.org/10.1128/aem.43.6.1278-1283.1982

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. Ito S, Kinta M, Inoue S (1980) Growth of yeasts on n-alkanes: inhibition by a lactonic sophorolipid produced by Torulopsis bombicola. Agric Biol Chem 44:2221–2223. https://doi.org/10.1080/00021369.1980.10864301

  42. Jacquier N, Schneiter R (2010) Ypk1, the yeast orthologue of the human serum- and glucocorticoid-induced kinase, is required for efficient uptake of fatty acids. J Cell Sci 123:2218–2227. https://doi.org/10.1242/jcs.063073

    CAS  Article  PubMed  Google Scholar 

  43. Jezierska S (2020) Transport and metabolic engineering of the yeast Starmerella bombicola for enhanced production of fatty acids and their derivatives. Doctoral dissertation, Ghent University

  44. Jezierska S, Claus S, Van Bogaert I (2019) Biosynthesis of glycolipids and their genetic engineering. In: Microbial Biosurfactants and their Environmental and Industrial Applications, vol 19, pp 601–615. https://doi.org/10.5840/ncbq201919451

    Google Scholar 

  45. Jezierska S, Claus S, Van Bogaert I (2020) Identification and importance of mitochondrial citrate carriers and ATP citrate lyase for glycolipid production in Starmerella bombicola. Appl. Microbiol. Biotechnol. 104:6235–6248.

  46. Julsing MK, Schrewe M, Cornelissen S, Hermann I, Schmid A, Bühler B (2012) Outer membrane protein AlkL boosts biocatalytic oxyfunctionalization of hydrophobic substrates in Escherichia coli. Appl Environ Microbiol 78:5724–5733

    CAS  Article  Google Scholar 

  47. Kalscheuer R, Weinrick B, Veeraraghavan U, Besra GS, Jacobs WR (2010) Trehalose-recycling ABC transporter LpqY-SugA-SugB-SugC is essential for virulence of Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 107:21761–21766. https://doi.org/10.1073/pnas.1014642108

    Article  PubMed  PubMed Central  Google Scholar 

  48. Kell DB, Swainston N, Pir P, Oliver SG (2015) Membrane transporter engineering in industrial biotechnology and whole cell biocatalysis. Trends Biotechnol 33:237–246. https://doi.org/10.1016/j.tibtech.2015.02.001

    CAS  Article  PubMed  Google Scholar 

  49. Klein M, Islam Z, Knudsen PB, Carrillo M, Swinnen S, Workman M, Nevoigt E (2016) The expression of glycerol facilitators from various yeast species improves growth on glycerol of Saccharomyces cerevisiae. Metab Eng Commun 3:252–257

    Article  Google Scholar 

  50. Klein M, Swinnen S, Thevelein JM, Nevoigt E (2017) Glycerol metabolism and transport in yeast and fungi: established knowledge and ambiguities. Environ Microbiol 19:878–893

    CAS  Article  Google Scholar 

  51. Knoshaug EP, Franden MA, Stambuk BU, Zhang M, Singh A (2009) Utilization and transport of L-arabinose by non-Saccharomyces yeasts. Cellulose. 16:729–741. https://doi.org/10.1007/s10570-009-9319-8

    CAS  Article  Google Scholar 

  52. Konishi M, Fukuoka T, Morita T, Imura T, Kitamoto D (2008) Production of new types of sophorolipids by Candida batistae. J Oleo Sci 57:359–369. https://doi.org/10.5650/jos.57.359

    CAS  Article  PubMed  Google Scholar 

  53. Konishi M, Hatada Y, Horiuchi JI (2013) Draft genome sequence of the basidiomycetous yeast-like fungus Pseudozyma hubeiensis SY62, which produces an abundant amount of the biosurfactant mannosylerythritol lipids. Genome Announc 1:13–14. https://doi.org/10.1128/genomeA.00409-13

    Article  Google Scholar 

  54. Konishi M, Morita T, Fukuoka T, Imura T, Uemura S, Iwabuchi H, Kitamoto D (2017) Selective production of acid-form sophorolipids from glycerol by Candida floricola. J Oleo Sci 66:1365–1376

  55. Kubicki S, Bollinger A, Katzke N, Jaeger KE, Loeschcke A, Thies S (2019) Marine biosurfactants: biosynthesis, structural diversity and biotechnological applications. Mar Drugs 17:1–30. https://doi.org/10.3390/md17070408

    CAS  Article  Google Scholar 

  56. Kulakovskaya TV, Shashkov AS, Kulakovskaya EV, Golubev WI (2004) Characterization of an antifungal glycolipid secreted by the yeast Sympodiomycopsis paphiopedili. FEMS Yeast Res 5:247–252. https://doi.org/10.1016/j.femsyr.2004.07.008

    CAS  Article  PubMed  Google Scholar 

  57. Kulakovskaya TV, Shashkov AS, Kulakovskaya EV, Golubev WI (2005) Ustilagic acid secretion by Pseudozyma fusiformata strains. FEMS Yeast Res 5:919–923. https://doi.org/10.1016/j.femsyr.2005.04.006

    CAS  Article  PubMed  Google Scholar 

  58. Kulakovskaya TV, Golubev WI, Tomashevskaya MA, Kulakovskaya EV, Shashkov AS, Grachev AA, Chizhov AS, Nifantiev NE (2010) Production of antifungal cellobiose lipids by Trichosporon porosum. Mycopathologia 169:117–123. https://doi.org/10.1007/s11046-009-9236-2

  59. Kumagai Y, Hirasawa T, Hayakawa K, Nagai K, Wachi M (2005) Fluorescent phospholipid analogs as microscopic probes for detection of the mycolic acid-containing layer in Corynebacterium glutamicum: detecting alterations in the mycolic acid-containing layer following ethambutol treatment. Biosci Biotechnol Biochem 69:2051–2056

    CAS  Article  Google Scholar 

  60. Kurosawa T, Sakai K, Nakahara T, Oshima Y, Tabuchi T (1994) Extracellular accumulation of the polyol lipids, 3,5-dihydroxydecanoyl and 5-hydroxy-2-decenoyl esters of arabitol and mannitol, by Aureobasidium sp. Biosci Biotechnol Biochem 58:2057–2060. https://doi.org/10.1271/bbb.58.2057

    CAS  Article  Google Scholar 

  61. Kurosawa K, Wewetzer SJ, Sinskey AJ (2013) Engineering xylose metabolism in triacylglycerol-producing Rhodococcus opacus for lignocellulosic fuel production. Biotechnol Biofuels 6:1–13. https://doi.org/10.1186/1754-6834-6-134

    CAS  Article  Google Scholar 

  62. Kurtzman CP, Price NPJ, Ray KJ, Kuo T-M (2010) Production of sophorolipid biosurfactants by multiple species of the Starmerella (Candida) bombicola yeast clade. FEMS Microbiol Lett 311:140–146. https://doi.org/10.1111/j.1574-6968.2010.02082.x

  63. Li X, Yang H, Zhang D, Li X, Yu H, Shen Z (2015) Overexpression of specific proton motive force-dependent transporters facilitate the export of surfactin in Bacillus subtilis. J Ind Microbiol Biotechnol 42:93–103. https://doi.org/10.1007/s10295-014-1527-z

    CAS  Article  PubMed  Google Scholar 

  64. Li J, Xia C, Fang X, Xue H, Song X (2016) Identification and characterization of a long-chain fatty acid transporter in the sophorolipid-producing strain Starmerella bombicola. Appl Microbiol Biotechnol:7137–7150. https://doi.org/10.1007/s00253-016-7580-y

  65. Li W, Stevens CM, Pandya AN, Darzynkiewicz Z, Bhattarai P, Tong W, Gonzalez-Juarrero M, North EJ, Zgurskaya HI, Jackson M (2019) Direct inhibition of MmpL3 by novel antitubercular compounds. ACS Infect Dis 5:1001–1012. https://doi.org/10.1021/acsinfecdis.9b00048

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  66. Li Y, Chen Y, Tian X, Chu J (2020) Advances in sophorolipid-producing strain performance improvement and fermentation optimization technology. Appl Microbiol Biotechnol 104:10325–10337. https://doi.org/10.1007/s00253-020-10964-7

  67. Lim SP, Roongsawang N, Washio K, Morikawa M (2009) Flexible exportation mechanisms of arthrofactin in Pseudomonas sp. MIS38. J Appl Microbiol 107:157–166. https://doi.org/10.1111/j.1365-2672.2009.04189.x

  68. Linder T (2019) Taxonomic distribution of cytochrome p450 monooxygenases (Cyps) among the budding yeasts (sub-phylum Saccharomycotina). Microorganisms. 7. https://doi.org/10.3390/microorganisms7080247

  69. Liu F, Liang J, Zhang B, Gao Y, Yang X, Hu T, Yang H, Xu W, Guddat LW, Rao Z (2020) Structural basis of trehalose recycling by the ABC transporter LpqY-SugABC. Sci Adv 6:eabb9833. https://doi.org/10.1126/sciadv.abb9833

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  70. Lodens S, Roelants SLKW, Luyten G, Geys R, Coussement P, De Maeseneire SL, Soetaert W (2020) Unraveling the regulation of sophorolipid biosynthesis in Starmerella bombicola. FEMS Yeast Res 20:1–11. https://doi.org/10.1093/femsyr/foaa021

    CAS  Article  Google Scholar 

  71. Lopez JMS, Van Bogaert INA (2020) Microbial fatty acid transport proteins and their biotechnological potential. Authorea https://doi.org/10.22541/au.159493425.51365391

  72. Lorenz S, Guenther M, Grumaz C, Rupp S, Zibek S, Sohn K (2014) Genome sequence of the basidiomycetous fungus Pseudozyma aphidis DSM70725, an efficient producer of biosurfactant mannosylerythritol lipids. Genome Announc 2:13–14. https://doi.org/10.1128/genomeA.e00053-14

    Article  Google Scholar 

  73. Ma X, Meng L, Zhang H, Zhou L, Yue J, Zhu H, Yao R (2020) Sophorolipid biosynthesis and production from diverse hydrophilic and hydrophobic carbon substrates. Appl Microbiol Biotechnol 104:77–100. https://doi.org/10.1007/s00253-019-10247-w

    CAS  Article  PubMed  Google Scholar 

  74. Marisa Herrero O, Moncalián G, Alvarez HM (2016) Physiological and genetic differences amongst Rhodococcus species for using glycerol as a source for growth and triacylglycerol production. Microbiol (United Kingdom) 162:384–397. https://doi.org/10.1099/mic.0.000232

  75. Martín JF, Casqueiro J, Liras P (2005) Secretion systems for secondary metabolites: how producer cells send out messages of intercellular communication. Curr Opin Microbiol 8:282–293. https://doi.org/10.1016/j.mib.2005.04.009

    CAS  Article  PubMed  Google Scholar 

  76. Matsuoka T, Yoshida N (2019) Functional analysis of putative transporters involved in oligotrophic growth of Rhodococcus erythropolis N9T-4. Appl Microbiol Biotechnol 103:4167–4175. https://doi.org/10.1007/s00253-019-09714-1

    CAS  Article  PubMed  Google Scholar 

  77. Mattjus P (2009) Glycolipid transfer proteins and membrane interaction. Biochim Biophys Acta Biomembr 1788:267–272. https://doi.org/10.1016/j.bbamem.2008.10.003

    CAS  Article  Google Scholar 

  78. Morita T, Konishi M, Fukuoka T, Imura T, Kitamoto D (2006) Discovery of Pseudozyma rugulosa NBRC 10877 as a novel producer of the glycolipid biosurfactants, mannosylerythritol lipids, based on rDNA sequence. Appl Microbiol Biotechnol 73:305–313. https://doi.org/10.1007/s00253-006-0466-7

    CAS  Article  PubMed  Google Scholar 

  79. Morita T, Konishi M, Fukuoka T, Imura T, Kitamoto D (2007a) Microbial conversion of glycerol into glycolipid biosurfactants, mannosylerythritol lipids, by a basidiomycete yeast, Pseudozyma antarctica JCM 10317T. J Biosci Bioeng 104:78–81. https://doi.org/10.1263/jbb.104.78

    CAS  Article  PubMed  Google Scholar 

  80. Morita T, Konishi M, Fukuoka T, Imura T, Kitamoto D (2007b) Physiological differences in the formation of the glycolipid biosurfactants, mannosylerythritol lipids, between Pseudozyma antarctica and Pseudozyma aphidis. Appl Microbiol Biotechnol 74:307–315. https://doi.org/10.1007/s00253-006-0672-3

    CAS  Article  PubMed  Google Scholar 

  81. Morita T, Konishi M, Fukuoka T, Imura T, Kitamoto HK, Kitamoto D (2007c) Characterization of the genus Pseudozyma by the formation of glycolipid biosurfactants, mannosylerythritol lipids. FEMS Yeast Res 7:286–292

    CAS  Article  Google Scholar 

  82. Morita T, Konishi M, Fukuoka T (2008a) Production of glycolipid biosurfactants, mannosylerythritol lipids, by Pseudozyma siamensis CBS 9960 and their interfacial properties. J Biosci Bioeng. 105:493–502. https://doi.org/10.1263/jbb.105.493.

  83. Morita T, Konishi M, Fukuoka T, Imura T, Sakai H, Kitamoto D (2008b) Efficient production of di-and tri-acylated mannosylerythritol lipids as glycolipid biosurfactants by Pseudozyma parantarctica JCM 11752T. J Oleo Sci 57:557–565

    CAS  Article  Google Scholar 

  84. Morita T, Ogura Y, Takashima M, Hirose N, Fukuoka T, Imura T, Kondo Y, Kitamoto D (2011) Isolation of Pseudozyma churashimaensis sp. nov., a novel ustilaginomycetous yeast species as a producer of glycolipid biosurfactants, mannosylerythritol lipids. J Biosci Bioeng 112:137–144. https://doi.org/10.1016/j.jbiosc.2011.04.008

    CAS  Article  PubMed  Google Scholar 

  85. Morita T, Koike H, Koyama Y, Hagiwara H, Ito E, Fukuoka T, Imura T, Machida M, Kitamoto D (2013) Genome Sequence of the Basidiomycetous Yeast Pseudozyma antarctica T-34, a Producer of the glycolipid biosurfactants mannosylerythritol lipids. Genome Announc 1:e0006413–e00064-13. https://doi.org/10.1128/genomeA.00064-13

    Article  PubMed  Google Scholar 

  86. Moysés DN, Reis VCB, de Almeida JRM, de Moraes LMP, Torres FAG (2016) Xylose fermentation by Saccharomyces cerevisiae: challenges and prospects. Int J Mol Sci 17:1–18. https://doi.org/10.3390/ijms17030207

  87. Niderweis M (2008) Nutrient acquisition by mycobacteria. Microbiology. 154:679–692. https://doi.org/10.1099/mic.0.2007/012872-0

    CAS  Article  Google Scholar 

  88. Nogueira KMV, Mendes V, Carraro CB, Taveira IC, Oshiquiri LH, Gupta VK, Silva RN (2020) Sugar transporters from industrial fungi: key to improving second-generation ethanol production. Renew Sust Energ Rev 131:109991. https://doi.org/10.1016/j.rser.2020.109991

    CAS  Article  Google Scholar 

  89. Noordman WH, Janssen DB (2002) Rhamnolipid stimulates uptake of hydrophobic compounds by Pseudomonas aeruginosa. Appl Environ Microbiol 68:4502–4508. https://doi.org/10.1128/AEM.68.9.4502-4508.2002

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  90. Oraby A, Werner N, Sungur Z, Zibek S (2020) Factors affecting the synthesis of cellobiose lipids by sporisorium scitamineum. Front Bioeng Biotechnol 8:1280

    Article  Google Scholar 

  91. Pieuchot L, Jedd G (2012) Peroxisome assembly and functional diversity in eukaryotic microorganisms. Annu Rev Microbiol 66:237–263. https://doi.org/10.1146/annurev-micro-092611-150126

    CAS  Article  PubMed  Google Scholar 

  92. Puchkov EO, Zähringer U, Lindner B, Kulakovskaya TV, Seydel U, Wiese A (2002) The mycocidal, membrane-active complex of Cryptococcus humicola is a new type of cellobiose lipid with detergent features. Biochim Biophys Acta Biomembr 1558:161–170. https://doi.org/10.1016/S0005-2736(01)00428-X

    CAS  Article  Google Scholar 

  93. Pyatt C, Van Bogaert INA, James S, Ellistion A, Dicks J, Roberts I (2018) Genome mining for metabolic gene clusters in yeast. In: 27th conference on Intelligent Systems for Molecular Biology, Basel

  94. Rahim R, Ochsner UA, Olvera C, Graninger M, Messner P, Lam JS, Soberón-Chávez G (2001) Cloning and functional characterization of the Pseudomonas aeruginosa rhlC gene that encodes rhamnosyltransferase 2, an enzyme responsible for di-rhamnolipid biosynthesis. Mol Microbiol 40:708–718. https://doi.org/10.1046/j.1365-2958.2001.02420.x

    CAS  Article  PubMed  Google Scholar 

  95. Rainczuk AK, Klatt S, Yamaryo-Botté Y, Brammananth R, McConville XMJ, Coppel RL, Crellin XPK (2020) Mtrp, a putative methyltransferase in corynebacteria, is required for optimal membrane transport of trehalose mycolates. J Biol Chem 295:6108–6119. https://doi.org/10.1074/jbc.RA119.011688

    Article  PubMed  Google Scholar 

  96. Rau U, Nguyen LA, Roeper H, Koch H, Lang S (2005) Fed-batch bioreactor production of mannosylerythritol lipids secreted by Pseudozyma aphidis. Appl Microbiol Biotechnol 68:607–613. https://doi.org/10.1007/s00253-005-1906-5

    CAS  Article  PubMed  Google Scholar 

  97. Saier MH, Reddy VS, Tsu BV, Ahmed MS, Li C, Moreno-Hagelsieb G (2016) The Transporter Classification Database (TCDB): recent advances. Nucleic Acids Res 44:D372–D379. https://doi.org/10.1093/nar/gkv1103

    CAS  Article  PubMed  Google Scholar 

  98. Saika A, Koike H, Hori T, Fukuoka T, Sato S, Habe H, Kitamoto D, Morita T (2014) Draft genome sequence of the yeast Pseudozyma antarctica type strain JCM10317, a producer of the glycolipid biosurfactants, mannosylerythritol lipids. Genome Announc 2:4–5. https://doi.org/10.1128/genomeA.00878-14

    Article  Google Scholar 

  99. Saika A, Koike H, Fukuoka T, Yamamoto S, Kishimoto T, Morita T (2016) A gene cluster for biosynthesis of mannosylerythritol lipids consisted of 4-O-beta-D-Mannopyranosyl-(2R,3S)-Erythritol as the sugar moiety in a basidiomycetous yeast Pseudozyma tsukubaensis. PLoS One 11:1–16. https://doi.org/10.1371/journal.pone.0157858

    CAS  Article  Google Scholar 

  100. Saika A, Fukuoka T, Koike H, Yamamoto S, Sugahara T, Sogabe A, Kitamoto D, Morita T (2020) A putative transporter gene PtMMF1-deleted strain produces mono-acylated mannosylerythritol lipids in Pseudozyma tsukubaensis. Appl Microbiol Biotechnol 104:10105–10117. https://doi.org/10.1007/s00253-020-10961-w

    CAS  Article  PubMed  Google Scholar 

  101. Schuler D, Wahl R, Wippel K, Vranes M, Münsterkötter M, Sauer N, Kämper J (2015) Hxt1, a monosaccharide transporter and sensor required for virulence of the maize pathogen Ustilago maydis. New Phytol 206:1086–1100. https://doi.org/10.1111/nph.13314

  102. Shao Z (2011) Trehalolipids. In: Soberón-Chávez G (ed) Biosurfactants: From Genes to Applications. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 121–143. https://doi.org/10.1007/978-3-642-14490-5_5

    Google Scholar 

  103. Spargo BJ, Crowe LM, Ioneda T, Beaman BL, Crowe JH (1991) Cord factor (alpha, alpha-trehalose 6, 6’-dimycolate) inhibits fusion between phospholipid vesicles. Proc Natl Acad Sci 88:737–740

    CAS  Article  Google Scholar 

  104. Stasyk OG, Stasyk OV (2019) Glucose sensing and regulation in yeasts. In: Non-conventional Yeasts: from Basic Research to Application, pp 477–519. https://doi.org/10.1007/978-3-030-21110-3_14

    Google Scholar 

  105. Stephan J, Bender J, Wolschendorf F, Hoffmann C, Roth E, Mailänder C, Engelhardt H, Niederweis M (2005) The growth rate of Mycobacterium smegmatis depends on sufficient porin-mediated influx of nutrients. Mol Microbiol 58:714–730

    CAS  Article  Google Scholar 

  106. Takayama K, Wang C, Besra GS (2005) Pathway to synthesis and processing of mycolic acids in Mycobacterium tuberculosis. Clin Microbiol Rev 18:81–101. https://doi.org/10.1128/CMR.18.1.81

  107. Tanimura A, Takashima M, Sugita T, Endoh R, Ohkuma M, Kishino S, Ogawa J, Shima J (2016) Lipid production through simultaneous utilization of glucose, xylose, and l-arabinose by Pseudozyma hubeiensis: a comparative screening study. AMB Express 6:58. https://doi.org/10.1186/s13568-016-0236-6

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  108. Teichmann B, Linne U, Hewald S, Marahiel MA, Bölker M (2007) A biosynthetic gene cluster for a secreted cellobiose lipid with antifungal activity from Ustilago maydis. Mol Microbiol 66:525–533. https://doi.org/10.1111/j.1365-2958.2007.05941.x

    CAS  Article  PubMed  Google Scholar 

  109. Teichmann B, Labbé C, Lefebvre F, Bölker M, Linne U, Bélanger RR (2011) Identification of a biosynthesis gene cluster for flocculosin a cellobiose lipid produced by the biocontrol agent Pseudozyma flocculosa. Mol Microbiol 79:1483–1495. https://doi.org/10.1111/j.1365-2958.2010.07533.x

    CAS  Article  PubMed  Google Scholar 

  110. Titgemeyer F, Amon J, Parche S, Mahfoud M, Bail J, Schlicht M, Rehm N, Hillmann D, Stephan J, Walter B, Burkovski A, Niederweis M (2007) A genomic view of sugar transport in Mycobacterium smegmatis and Mycobacterium tuberculosis. J Bacteriol 189:5903–5915. https://doi.org/10.1128/JB.00257-07

  111. Tulloch AP, Spencer J, Deinema M (1968) A new hydroxy fatty acid sophoroside from Candida bogoriensis. Can J Chem 46:345–348

    CAS  Article  Google Scholar 

  112. Turner WJ, Dunlop MJ (2015) Trade-offs in improving biofuel tolerance using combinations of efflux pumps. ACS Synth Biol 4:1056–1063. https://doi.org/10.1021/sb500307w

    CAS  Article  PubMed  Google Scholar 

  113. Ung KL, Alsarraf HMAB, Kremer L, Blaise M (2020) The crystal structure of the mycobacterial trehalose monomycolate transport factor A, TtfA, reveals an atypical fold. Proteins Struct Funct Bioinforma 88:809–815. https://doi.org/10.1002/prot.25863

    CAS  Article  Google Scholar 

  114. Van Bogaert INA, Holvoet K, Roelants SLKW, Li B, Lin Y-C, Van de Peer Y, Soetaert W (2013) The biosynthetic gene cluster for sophorolipids: a biotechnological interesting biosurfactant produced by Starmerella bombicola. Mol Microbiol 88:501–509. https://doi.org/10.1111/mmi.12200

  115. Van Roermund CWT, Ijlst L, Majczak W, Waterham HR, Folkerts H, Wanders RJA, Hellingwerf KJ (2012) Peroxisomal fatty acid uptake mechanism in Saccharomyces cerevisiae. J Biol Chem 287:20144–20153. https://doi.org/10.1074/jbc.M111.332833

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  116. Van Wezel GP, Mahr K, König M, Traag BA, Pimentel-Schmitt EF, Willimek A, Titgemeyer F (2005) GlcP constitutes the major glucose uptake system of Streptomyces coelicolor A3(2). Mol Microbiol 55:624–636

  117. Velázquez F, Pflüger K, Cases I, De Eugenio LI, De Lorenzo V (2007) The phosphotransferase system formed by PtsP, PtsO, and PtsN proteins controls production of polyhydroxyalkanoates in Pseudomonas putida. J Bacteriol 189:4529–4533. https://doi.org/10.1128/JB.00033-07

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  118. Viljoen A, Dubois V, Girard-Misguich F, Blaise M, Herrmann JL, Kremer L (2017) The diverse family of MmpL transporters in mycobacteria: from regulation to antimicrobial developments. Mol Microbiol 104:889–904. https://doi.org/10.1111/mmi.13675

    CAS  Article  PubMed  Google Scholar 

  119. Villalba MS, Alvarez HM (2014) Identification of a novel ATP-binding cassette transporter involved in long-chain fatty acid import and its role in triacylglycerol accumulation in Rhodococcus jostii RHA1. Microbiol (United Kingdom) 160:1523–1532. https://doi.org/10.1099/mic.0.078477-0

    CAS  Article  Google Scholar 

  120. Wahl R, Wippel K, Goos S, Kämper J, Sauer N (2010) A novel high-affinity sucrose transporter is required for virulence of the plant pathogen Ustilago maydis. PLoS Biol 8:e1000303

    Article  Google Scholar 

  121. Williams JT, Haiderer ER, Coulson GB, Conner KN, Ellsworth E, Chen C, Alvarez-Cabrera N, Li W, Jackson M, Dick T, others (2019) Identification of new MmpL3 inhibitors by untargeted and targeted mutant screens defines MmpL3 domains with differential resistance. Antimicrob Agents Chemother 63:e00547–e00519

    CAS  Article  Google Scholar 

  122. Wittgens A, Kovacic F, Müller MM, Gerlitzki M, Santiago-Schübel B, Hofmann D, Tiso T, Blank LM, Henkel M, Hausmann R, Syldatk C, Wilhelm S, Rosenau F (2017) Novel insights into biosynthesis and uptake of rhamnolipids and their precursors. Appl Microbiol Biotechnol 101:2865–2878. https://doi.org/10.1007/s00253-016-8041-3

    CAS  Article  PubMed  Google Scholar 

  123. Wu JY, Yeh KL, Bin LW, Lin CL, Chang JS (2008) Rhamnolipid production with indigenous Pseudomonas aeruginosa EM1 isolated from oil-contaminated site. Bioresour Technol 99:1157–1164. https://doi.org/10.1016/j.biortech.2007.02.026

  124. Xue S-J, Liu G-L, Chi Z, Gao Z-C, Hu Z, Chi Z-M (2020) Genetic evidences for the core biosynthesis pathway, regulation, transport and secretion of liamocins in yeast-like fungal cells. Biochem J:887–903

  125. Yuan XZ, Ren FY, Zeng GM, Zhong H, Fu HY, Liu J, Xu XM (2007) Adsorption of surfactants on a Pseudomonas aeruginosa strain and the effect on cell surface lypohydrophilic property. Appl Microbiol Biotechnol 76:1189–1198. https://doi.org/10.1007/s00253-007-1080-z

    CAS  Article  PubMed  Google Scholar 

  126. Zambanini T, Buescher JM, Meurer G, Wierckx N, Blank LM (2016) Draft genome sequence of Ustilago trichophora RK089, a promising malic acid producer. Genome Announc 4:10–11. https://doi.org/10.1128/genomeA.00749-16.Copyright

    Article  Google Scholar 

  127. Zhang B, Li J, Yang X, Wu L, Zhang J, Yang Y, Zhao Y, Zhang L, Yang X, Yang X, Cheng X, Liu Z, Jiang B, Jiang H, Guddat LW, Yang H, Rao Z (2019) Crystal structures of membrane transporter MmpL3, an anti-TB drug target. Cell 176:636–648.e13. https://doi.org/10.1016/j.cell.2019.01.003

    CAS  Article  PubMed  Google Scholar 

  128. Zhou QH, Kosaric N (1993) Effect of lactose and olive oil on intra- and extracellular lipids of Torulopsis bombicola. Biotechnol Lett 15:477–482. https://doi.org/10.1007/BF00129322

    CAS  Article  Google Scholar 

  129. Zhou X, Xing X, Hou J, Liu J (2017) Quantitative proteomics analysis of proteins involved in alkane uptake comparing the profiling of Pseudomonas aeruginosa SJTD-1 in response to n-octadecane and n-hexadecane. PLoS One 12:1–13. https://doi.org/10.1371/journal.pone.0179842

    CAS  Article  Google Scholar 

Download references

Acknowledgements

The authors wish to thank the Research Foundation - Flanders (FWO; grant number 28930 and 1185417N), as well as the Special Research Fund of Ghent University Ghent (BOF; grant number STA011-17) for financial support.

Author information

Affiliations

Authors

Contributions

SC screened the literature and wrote the manuscript. LJS collaborated in overall writing and wrote on glycerol transport mechanisms. INAVB was involved in writing part of the text on CBL, conception, guiding, and reviewing. All authors read and approved the manuscript.

Corresponding author

Correspondence to Inge Noëlle Adrienne Van Bogaert.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Claus, S., Jenkins Sánchez, L. & Van Bogaert, I.N.A. The role of transport proteins in the production of microbial glycolipid biosurfactants. Appl Microbiol Biotechnol 105, 1779–1793 (2021). https://doi.org/10.1007/s00253-021-11156-7

Download citation

Keywords

  • Biosurfactant
  • Glycolipid
  • Transporter
  • Gene cluster
  • Yeast
  • Bacteria