1887

Abstract

The exit from dormancy and the start of growth should be preceded or at least accompanied by the uptake of nutrients. In this work we studied changes in the transport of several nutrients into conidia. Germination started with a short period of isodiametric growth (conidial swelling), followed by polarized growth (germ tube formation) after about 8 h at 26 °C. The onset of isodiametric growth required the presence of external both phosphate and nitrate. At the same time, an increased uptake of precursors of macromolecules and phospholipids (C- or H-labelled valine, uracil, -acetylglucosamine and choline) occurred. A low uptake of these precursors was observed also in non-germinating conidia. Concomitantly, this uptake developed an increased sensitivity to the uncoupler 3,3′,4′,5-tetrachlorosalicylanilide. Expression and activity of H-ATPase started after completing isodiametric growth, suggesting that the proton-motive force (PMF) generated by H-ATPase may be an accelerator of nutrient uptake and metabolism. C-valine uptake was also measured into a mutant with disrupted gene. This mutant did not form conidia. The mutant also exhibited uncoupler sensitivity of C-valine uptake. These observations showed that a PMF must have been generated by a mechanism(s) other than the H-ATPase activity in the WT before H-ATPase expression and in mycelia with disrupted H-ATPase.

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2015-06-01
2024-12-14
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References

  1. Abdel-Rahim A. M., Arbab H. A. (1985). Nutrient requirements in germination of conidiospores of Aspergillus niger V. Tieghen. Mycopathologia 92, 111113.[CrossRef] [Google Scholar]
  2. Abyzov S. S., Mitskevich I. N., Poglazova M. N., Barkov N. I., Lipenkov V. Y., Bobin N. E., Koudryashov B. B., Pashkevich V. M., Ivanov M. V. (2001). Microflora in the basal strata at Antarctic ice core above the Vostok lake. Adv Space Res 28, 701706.[CrossRef] [Google Scholar]
  3. Aitken W. B., Niederpruem D. J. (1972). Isotopic studies of carbohydrate metabolism during basidiospore germination in Schizophyllum commune. I. Uptake of radioactive glucose and sugar alcohols. Arch Mikrobiol 82, 173183.[CrossRef] [Google Scholar]
  4. Amillis S., Cecchetto G., Sophianopoulou V., Koukaki M., Scazzocchio C., Diallinas G. (2004). Transcription of purine transporter genes is activated during the isotropic growth phase of Aspergillus nidulans conidia. Mol Microbiol 52, 205216.[CrossRef] [Google Scholar]
  5. Arroyo I. (2009). The role of fungi in the deterioration of movable and immovable cultural heritage. e-conservation magazine 9, 4050. [Google Scholar]
  6. Brambl R. (1980). Mitochondrial biogenesis during fungal spore germination. Biosynthesis and assembly of cytochrome c oxidase in Botryodiplodia theobromae . J Biol Chem 255, 76737680. [Google Scholar]
  7. Burgstaller W. (1997). Transport of small lons and molecules through the plasma membrane of filamentous fungi. Crit Rev Microbiol 23, 146.[CrossRef] [Google Scholar]
  8. Burgstaller W. (2006). Thermodynamic boundary conditions suggest that a passive transport step suffices for citrate excretion in Aspergillus and Penicillium . Microbiology 152, 887893.[CrossRef] [Google Scholar]
  9. Carlile M. J., Watkinson S. C., Gooday G. W. (2001). The Fungi, 2nd edn. London: Academic Press. [Google Scholar]
  10. Chovanec P., Kalinák M., Liptaj T., Pronayová N., Jakubík T., Hudecová D., Varečka L'. (2005). Study of Trichoderma viride metabolism under conditions of the restriction of oxidative processes. Can J Microbiol 51, 853862.[CrossRef] [Google Scholar]
  11. Clegg J. S. (2001). Cryptobiosis–a peculiar state of biological organization. Comp Biochem Physiol B Biochem Mol Biol 128, 613624.[CrossRef] [Google Scholar]
  12. d'Enfert C. (1997). Fungal spore germination: insights from the molecular genetics of Aspergillus nidulans and Neurospora crassa . Fungal Genet Biol 21, 163172.[CrossRef] [Google Scholar]
  13. d'Enfert C., Bonini B. M., Zapella P. D., Fontaine T., da Silva A. M., Terenzi H. F. (1999). Neutral trehalases catalyse intracellular trehalose breakdown in the filamentous fungi Aspergillus nidulans and Neurospora crassa . Mol Microbiol 32, 471483.[CrossRef] [Google Scholar]
  14. Deák T., Kotyk A. (1968). Uphill transport of monosaccharides in Candida beverwijkii . Folia Microbiol (Praha) 13, 205211.[CrossRef] [Google Scholar]
  15. DeBusk R. M., DeBusk A. G. (1980). Physiological and regulatory properties of the general amino acid transport system of Neurospora crassa J Bacteriol 143, 188197. [Google Scholar]
  16. Döhlemann G., Berndt P., Hahn M. (2006). Trehalose metabolism is important for heat stress tolerance and spore germination of Botrytis cinerea . Microbiology 152, 26252634.[CrossRef] [Google Scholar]
  17. Eaton C. J., Cabrera I. E., Servin J. A., Wright S. J., Cox M. P., Borkovich K. A. (2012). The guanine nucleotide exchange factor RIC8 regulates conidial germination through Gα proteins in Neurospora crassa . PLoS ONE 7, e48026.[CrossRef] [Google Scholar]
  18. Eddy A. A., Hopkins P. (1988). The intrinsic as opposed to the apparent stoichiometry of the glycine-proton symport of the yeast Saccharomyces carlsbergensis . Biochem J 251, 115119. [Google Scholar]
  19. Eddy A. A., Nowacki J. A. (1971). Stoicheiometrical proton and potassium ion movements accompanying the absorption of amino acids by the yeast Saccharomyces carlsbergensis . Biochem J 122, 701711. [Google Scholar]
  20. Eddy A. A., Backen K., Nowacki J. (1970). Translocation of protons and alkali-metal cations accompanying the uptake of neutral amino acids by yeast. Biochem J 116, 34P35P. [Google Scholar]
  21. El-Akhal M. R., Colby T., Cantoral J. M., Harzen A., Schmidt J., Fernández-Acero F. J. (2013). Proteomic analysis of conidia germination in Colletotrichum acutatum . Arch Microbiol 195, 227246.[CrossRef] [Google Scholar]
  22. Gachomo E., Allen J. W., Pfeffer P. E., Govindarajulu M., Douds D. D., Jin H., Nagahashi G., Lammers P. J., Shachar-Hill Y., Bücking H. (2009). Germinating spores of Glomus intraradices can use internal and exogenous nitrogen sources for de novo biosynthesis of amino acids. New Phytol 184, 399411.[CrossRef] [Google Scholar]
  23. Goffeau A., Slayman C. W. (1981). The proton-translocating ATPase of the fungal plasma membrane. Biochim Biophys Acta 639, 197223.[CrossRef] [Google Scholar]
  24. Gordon J. A. (1991). Use of vanadate as protein-phosphotyrosine phosphatase inhibitor. Methods Enzymol 201, 477482.[CrossRef] [Google Scholar]
  25. Greer W. L., Wellman A. M. (1981). Inhibition of adenine and hypoxanthine uptake by guanosine in conidia of Neurospora crassa . Can J Biochem 59, 933936.[CrossRef] [Google Scholar]
  26. Harris S. D., Momany M. (2004). Polarity in filamentous fungi: moving beyond the yeast paradigm. Fungal Genet Biol 41, 391400.[CrossRef] [Google Scholar]
  27. Hawley E. S., Greenawalt J. W. (1975). Biogenesis of mitochondrial membranes in Neurospora crassa. Mitochondrial protein synthesis during conidial germination. Eur J Biochem 54, 585601.[CrossRef] [Google Scholar]
  28. Hayer K., Stratford M., Archer D. B. (2013). Structural features of sugars that trigger or support conidial germination in the filamentous fungus Aspergillus niger . Appl Environ Microbiol 79, 69246931.[CrossRef] [Google Scholar]
  29. Hayer K., Stratford M., Archer D. B. (2014). Germination of Aspergillus niger conidia is triggered by nitrogen compounds related to L-amino acids. Appl Environ Microbiol 80, 60466053.[CrossRef] [Google Scholar]
  30. Hillenga D. J., Versantvoort H. J., Driessen A. J., Konings W. N. (1996). Basic amino acid transport in plasma membrane vesicles of Penicillium chrysogenum . J Bacteriol 178, 39913995. [Google Scholar]
  31. Johnson J. H., Belt J. A., Dubinsky W. P., Zimniak A., Racker E. (1980). Inhibition of lactate transport in Ehrlich ascites tumor cells and human erythrocytes by a synthetic anhydride of lactic acid. Biochemistry 19, 38363840.[CrossRef] [Google Scholar]
  32. Kamauchi S., Mitsui K., Ujike S., Haga M., Nakamura N., Inoue H., Sakajo S., Ueda M., Tanaka A., Kanazawa H. (2002). Structurally and functionally conserved domains in the diverse hydrophilic carboxy-terminal halves of various yeast and fungal Na+/H+ antiporters (Nha1p). J Biochem 131, 821831.[CrossRef] [Google Scholar]
  33. Kaliňák M., Šimkovič M., Žemla P., Mat'at'a M., Molnár T., Liptaj T., Varečka L'., Hudecová D. (2014). Changes in metabolome and in enzyme activities during germination of Trichoderma atroviride conidia. FEMS Microbiol Lett 357, 201207. [Google Scholar]
  34. Konings W. N., Poolman B., Driessen A. J. M. (1992). Can the excretion of metabolites by bacteria be manipulated?FEMS Microbiol Rev 8, 93108.[CrossRef] [Google Scholar]
  35. Kotyk A. (1983). Coupling of secondary active transport with a Δμ H+ . J Bioenerg Biomembr 15, 307319.[CrossRef] [Google Scholar]
  36. Kotyk A., Höfer M. (1965). Uphill transport of sugars in the yeast Rhodotorula gracilis . Biochim Biophys Acta 102, 410422.[CrossRef] [Google Scholar]
  37. Kotyk A., Ríhová L. (1972). Energy requirement for amino acid uptake in Saccharomyces cerevisiae . Folia Microbiol (Praha) 17, 353356.[CrossRef] [Google Scholar]
  38. Kropf D. L., Caldwell J. H., Gow N. A., Harold F. M. (1984). Transcellular ion currents in the water mold Achlya. Amino acid proton symport as a mechanism of current entry. J Cell Biol 99, 486496.[CrossRef] [Google Scholar]
  39. Lakatoš B., Šimkovič M., Betina V., Varečka L'. (1999). Properties of uracil transport by vegetative mycelium of Trichoderma viride . FEMS Microbiol Lett 171, 161165.[CrossRef] [Google Scholar]
  40. Lamarre C., Sokol S., Debeaupuis J. P., Henry Ch., Lacroix C., Glaser P., Coppée J. Y., François J. M., Latgé J. P. (2008). Transcriptomic analysis of the exit from dormancy of Aspergillus fumigatus conidia. BMC Genomics 9, 417.[CrossRef] [Google Scholar]
  41. Lambou K., Pennati A., Valsecchi I., Tada R., Sherman S., Sato H., Beau R., Gadda G., Latgé J. P. (2013). Pathway of glycine betaine biosynthesis in Aspergillus fumigatus . Eukaryot Cell 12, 853863.[CrossRef] [Google Scholar]
  42. Leng W., Liu T., Li R., Yang J., Wei C., Zhang W., Jin Q. (2008). Proteomic profile of dormant Trichophyton rubrum conidia. BMC Genomics 9, 303.[CrossRef] [Google Scholar]
  43. Liu T., Zhang Q., Wang L., Yu L., Leng W., Yang J., Chen L., Peng J., Ma L., other authors. (2007). The use of global transcriptional analysis to reveal the biological and cellular events involved in distinct development phases of Trichophyton rubrum conidial germination. BMC Genomics 8, 100.[CrossRef] [Google Scholar]
  44. Magill J. M., Magill C. W. (1975). Purine base transport in Neurospora crassa . J Bacteriol 124, 149154. [Google Scholar]
  45. McEvoy J. J., Murray J. R. (1972). Amino acid transport in germinated arthrospores of Geotrichum candidum . Arch Mikrobiol 86, 101110.[CrossRef] [Google Scholar]
  46. Metz B., Seidl-Seiboth V., Haarmann T., Kopchinskiy A., Lorenz P., Seiboth B., Kubicek C. P. (2011). Expression of biomass-degrading enzymes is a major event during conidium development in Trichoderma reesei . Eukaryot Cell 10, 15271535.[CrossRef] [Google Scholar]
  47. Mukherjee M., Mukherjee P. K., Kale S. P. (2007). cAMP signalling is involved in growth, germination, mycoparasitism and secondary metabolism in Trichoderma virens . Microbiology 153, 17341742.[CrossRef] [Google Scholar]
  48. Mukhtar M., Parveen Z., Logan D. A. (1998). Isolation of RNA from the filamentous fungus Mucor circinelloides . J Microbiol Methods 33, 115118.[CrossRef] [Google Scholar]
  49. Nižňanský L'., Kryštofová S., Vargovič P., Kaliňák M., Simkovič M., Varečka L'. (2013). Glutamic acid decarboxylase gene disruption reveals signalling pathway(s) governing complex morphogenic and metabolic events in Trichoderma atroviride . Antonie van Leeuwenhoek 104, 793807.[CrossRef] [Google Scholar]
  50. Novodvorska M., Hayer K., Pullan S. T., Wilson R., Blythe M. J., Stam H., Stratford M., Archer D. B. (2013). Trancriptional landscape of Aspergillus niger at breaking of conidial dormancy revealed by RNA-sequencing. BMC Genomics 14, 246.[CrossRef] [Google Scholar]
  51. Oh Y. T., Ahn C. S., Kim J. G., Ro H. S., Lee C. W., Kim J. W. (2010). Proteomic analysis of early phase of conidia germination in Aspergillus nidulans . Fungal Genet Biol 47, 246253.[CrossRef] [Google Scholar]
  52. Olejníková P., Hudecová D., Burgstaller W., Kryštofová S., Varečka L. (2011). Transient excretion of succinate from Trichoderma atroviride submerged mycelia reveals the complex movements and metabolism of carboxylates. Antonie van Leeuwenhoek 100, 5566.[CrossRef] [Google Scholar]
  53. Olivera H., González A., Peña A. (1993). Regulation of the amino acid permeases in nitrogen-limited continuous cultures of the yeast Saccharomyces cerevisiae . Yeast 9, 10651073.[CrossRef] [Google Scholar]
  54. Osherov N., May G. S. (2001). The molecular mechanisms of conidial germination. FEMS Microbiol Lett 199, 153160.[CrossRef] [Google Scholar]
  55. Palmero Llamas D., de Cara Gonzalez M., Iglesias Gonzalez C., Ruíz Lopez G., Tello Marquina J. C. (2008). Effects of water potential on spore germination and viability of Fusarium species. J Ind Microbiol Biotechnol 35, 14111418.[CrossRef] [Google Scholar]
  56. Pendyala L., Wellman A. M. (1977). Developmental-stage-dependent adenine transport in Neurospora crassa . J Bacteriol 131, 453462. [Google Scholar]
  57. Pokorný R., Hudecová D., Burgstaller W., Varečka L. (2004). Changes in properties of glutamate transport in Trichoderma viride vegetative mycelia upon adaptation to glutamate as carbon source. FEMS Microbiol Lett 230, 123128.[CrossRef] [Google Scholar]
  58. Railey R. M., Kinsey J. A. (1976). Development of amino acid uptake activity in Neurospora . Can J Microbiol 22, 115120.[CrossRef] [Google Scholar]
  59. Robson G. D., Best L. C., Wiebe M. G., Trinci A. P. (1992). Choline transport in Fusarium graminearum A 3/5. FEMS Microbiol Lett 71, 247251. [Google Scholar]
  60. Scarborough G. A. (1976). The neurospora plasma membrane ATPase is an electrogenic pump. Proc Natl Acad Sci U S A 73, 14851488.[CrossRef] [Google Scholar]
  61. Schiltz J. R., Terry K. D. (1970). Nucleoside uptake during the germination of Neurospora crassa conidia. Biochim Biophys Acta 209, 278288.[CrossRef] [Google Scholar]
  62. Schmit J. C., Brody S. (1976). Biochemical genetics of Neurospora crassa conidial germination. Bacteriol Rev 40, 141. [Google Scholar]
  63. Serrano R. (1978). Characterization of the plasma membrane ATPase of Saccharomyces cerevisiae . Mol Cell Biochem 22, 5163.[CrossRef] [Google Scholar]
  64. Šimkovič M., Ditte P., Chovanec P., Varečka L'., Lakatoš B. (2007). Changes in growth competence of aged Trichoderma viride vegetative mycelia. Antonie van Leeuwenhoek 91, 407416.[CrossRef] [Google Scholar]
  65. Sinohara H. (1974). Amino acid transport in spores of Aspergillus oryzae . J Biochem 76, 513522. [Google Scholar]
  66. Slayman C. L., Slayman C. W. (1968). Net uptake of potassium in Neurospora. Exchange for sodium and hydrogen ions. J Gen Physiol 52, 424443.[CrossRef] [Google Scholar]
  67. Stade S., Brambl R. (1981). Mitochondrial biogenesis during fungal spore germination: respiration and cytochrome c oxidase in Neurospora crassa . J Bacteriol 147, 757767. [Google Scholar]
  68. Taubitz A., Bauer B., Heesemann J., Ebel F. (2007). Role of respiration in the germination process of the pathogenic mold Aspergillus fumigatus . Curr Microbiol 54, 354360.[CrossRef] [Google Scholar]
  69. Tazebay U. H., Sophianopoulou V., Cubero B., Scazzocchio C., Diallinas G. (1995). Post-transcriptional control and kinetic characterization of proline transport in germinating conidiospores of Aspergillus nidulans . FEMS Microbiol Lett 132, 2737.[CrossRef] [Google Scholar]
  70. Tazebay U. H., Sophianopoulou V., Scazzocchio C., Diallinas G. (1997). The gene encoding the major proline transporter of Aspergillus nidulans is upregulated during conidiospore germination and in response to proline induction and amino acid starvation. Mol Microbiol 24, 105117.[CrossRef] [Google Scholar]
  71. Teutschbein J., Albrecht D., Pötsch M., Guthke R., Aimanianda V., Clavaud C., Latgé J. P., Brakhage A. A., Kniemeyer O. (2010). Proteome profiling and functional classification of intracellular proteins from conidia of the human-pathogenic mold Aspergillus fumigatus . J Proteome Res 9, 34273442.[CrossRef] [Google Scholar]
  72. Tisdale J. H., DeBusk A. G. (1970). Developmental regulation of amino acid transport in Neurospora crassa . J Bacteriol 104, 689697. [Google Scholar]
  73. Tuduri P., Nso E., Dufour J. P., Goffeau A. (1985). Decrease of the plasma membrane H+-ATPase activity during late exponential growth of Saccharomyces cerevisiae . Biochem Biophys Res Commun 133, 917922.[CrossRef] [Google Scholar]
  74. van Leeuwen M. R., Krijgsheld P., Bleichrodt R., Menke H., Stam H., Stark J., Wösten H. A. B., Dijksterhuis J. (2013). Germination of conidia of Aspergillus niger is accompanied by major changes in RNA profiles. Stud Mycol 74, 5970.[CrossRef] [Google Scholar]
  75. Villalobo A., Boutry M., Goffeau A. (1981). Electrogenic proton translocation coupled to ATP hydrolysis by the plasma membrane Mg2+-dependent ATPase of yeast in reconstituted proteoliposomes. J Biol Chem 256, 1208112087. [Google Scholar]
  76. Vlanti A., Diallinas G. (2008). The Aspergillus nidulans FcyB cytosine–purine scavenger is highly expressed during germination and in reproductive compartments and is downregulated by endocytosis. Mol Microbiol 68, 959977.[CrossRef] [Google Scholar]
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