Glycerol enhances fungal germination at the water-activity limit for life

Environmental Microbiology

Volumn 19, Issue 3, 2017, Pages 947-967

  Stevenson, Andrew ^a   Hamill, Philip G ^a   Medina, Ángel ^b   Kminek, Gerhard ^c   Rummel, John D ^d   Dijksterhuis, Jan ^e   Timson, David J ^f   Magan, Naresh ^b   Leong, Su Lin L ^g   Hallsworth, John E ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b CRANFIELD UNIVERSITY   (United Kingdom)

^c EUROPEAN SPACE AGENCY   (Netherlands)

^d SETI INSTITUTE   (United States)

^e CBS KNAW FUNGAL BIODIVERSITY CENTRE   (Netherlands)

^f UNIVERSITY OF BRIGHTON   (United Kingdom)

^g SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCEROL; WATER;

ASPERGILLUS; ECOSYSTEM; EUROTIALES; FUNGUS; FUNGUS SPORE; METABOLISM; PHYSIOLOGY;

ASPERGILLUS; ECOSYSTEM; EUROTIALES; FUNGI; GLYCEROL; SPORES, FUNGAL; WATER;

EID: 84994033692     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.13530     Document Type: Article

References (98)

1. Andersen, A., Magan, N., Mead, A., and Chandler, D. (2006) Development of a population-based threshold model of conidial germination for analysing the effects of physiological manipulation on the stress tolerance and infectivity of insect pathogenic fungi. Environ Micobiol 8: 1625–1634.
2. Andrews, S., and Pitt, J.I. (1987) Further studies on the water relations of xerophilic fungi, including some halophiles. J Gen Microbiol 133: 233–238.
3. Arai, H. (2000) Foxing caused by fungi: twenty-five years of study. Int Biodeter Biodegr 46: 181–188.
4. Asada, S., Takano, M., and Shibasaki, I. (1979) Deoxyribonucleic acid strand breaks during drying of Escherichia coli on a hydrophobic filter membrane. Appl Environ Microbiol 37: 266–273.
5. Ball, P., and Hallsworth, J.E. (2015) Water structure and chaotropicity: their uses and abuses. Phys Chem Chem Phys 17: 8297–8305.
6. Bardavid, R.E., Khristo, P., and Oren, A. (2008) Interrelationships between Dunaliella and halophilic prokaryotes in saltern crystallizer ponds. Extremophiles 12: 5–14.
7. Basso, L.C., De Amorim, H.V., de Oliveira, A.J., Lopes, M.L. (2008) Yeast selection for fuel ethanol production in Brazil. FEMS Yeast Res 8:1155–1163.
8. Benison, K.C., and Karmanocky III, F.J. (2014) Could microorganisms be preserved in Mars gypsum? Insights from terrestrial examples. Geology 42: 615–618.
9. Bhaganna, P., Volkers, R.J.M., Bell, A.N.W., Kluge, K., Timson, D.J., McGrath, J.W., et al. (2010) Hydrophobic substances induce water stress in microbial cells. Microb Biotechnol 3: 701–716.
10. Bhaganna, P., Bielecka, A., Molinari, G., Hallsworth, J.E. (2016). Protective role of glycerol against benzene stress: insights from the Pseudomonas putida proteome. Curr Genet 62: 419–429.
11. Bonnardeaux, J. (2006) Agriculture uses of glycerine. In Glycerine Overview, Perth: Department of Agriculture and Food, Western Australia.
12. Chin, J.P., Megaw, J., Magill, C.L., Nowotarski, K., Williams, J.P., Bhaganna, P., et al. (2010) Solutes determine the temperature windows for microbial survival and growth. Proc Natl Acad Sci USA 107: 7835–7840.
13. Cray, J.A., Bell, A.N.W., Bhaganna, P., Mswaka, A.Y., Timson, D.J., and Hallsworth, J.E. (2013a) The biology of habitat dominance; can microbes behave as weeds? Microbiol Biotechnol 6: 453–492.
14. Cray, J.A., Connor, M.C., Stevenson, A., Houghton, J.D., Rangel, D.E., Cooke, L.R., and Hallsworth, J.E. (2016) Biocontrol agents promote growth of potato pathogens, depending on environmental conditions. Microbiol Biotechnol 9: 330–354.
15. Cray, J.A., Russell, J.T., Timson, D.J., Singhal, R.S., and Hallsworth, J.E. (2013b) A universal measure of chaotropicity and kosmotropicity. Environ Microbiol 15: 287–296.
16. Cray, J.A., Stevenson, A., Ball, P., Bankar, S.B., Eleutherio, E.C., Ezeji, T.C., et al. (2015a) Chaotropicity: a key factor in product tolerance of biofuel-producing microorganisms. Curr Opin Biotechnol 33: 228–259.
17. Dannemiller, K.C., Weschler, C.J., and Peccia, J. (In press) Fungal and bacterial growth in floor dust at elevated relative humidity levels. Indoor Air Doi: 10.1111/ina.12313
18. D'Hondt, S., Rutherford, S., and Spivack, A.J. (2002) Metabolic activity of subsurface life in deep-sea sediments. Science 295: 2067–2070.
19. Donkin, S.S. (2008) Glycerol from biodiesel production: the new corn for dairy cattle. R Bras Zootec 37: 280–286.
20. Duman, J. G. (2001). Antifreeze and ice nucleator proteins in terrestrial arthropods. Ann Rev Physiol 63: 327– 357.
21. Falk, M., Hartman, K.A., and Lord, R.C. (1963) Hydration of deoxyribonucleic acid. II. An infrared study. J Am Chem Soc 85: 387–391.
22. Fox-Powell, M.G., Hallsworth, J.E., Cousins, C.R., and Cockell, C.S. (2016) Ionic strength is a barrier to the habitability of Mars. Astrobiology 16: 427–442.
23. Gock, M.A., Hocking, A.D., Pitt, J.I., and Poulos, P.G. (2003) Influence of temperature, water activity and pH on growth of some xerophilic fungi. Int J Food Microbiol 81: 11–19.
24. Grant, W.D. (2004) Life at low water activity. Philos Trans R Soc Lond B Biol Sci 359: 1249–1266.
25. Hallsworth, J.E. (1998) Ethanol-induced water stress in yeast. J Ferment Bioeng 85: 125–137.
26. Hallsworth, J.E., Nomura, Y., and Iwahara, M. (1998) Ethanol-induced water stress and fungal growth. J Ferment Bioeng 86: 451–456.
27. Hallsworth, J.E., Heim, S., and Timmis, K.N. (2003b) Chaotropic solutes cause water stress in Pseudomonas putida. Environ Microbiol 5: 1270–1280.
28. Hallsworth, J.E., and Magan, N. (1994a) Improved biological control by changing polyols/trehalose in conidia of entomopathogens. In Brighton Crop Protection Council-Pests and Diseases. Farnham, UK: British Crop Protection Council 1994, pp. 1091–1096.
29. Hallsworth, J.E., and Magan, N. (1994b) Effect of carbohydrate type and concentration on polyols and trehalose in conidia of three entomopathogenic fungi. Microbiol-SGM 140: 2705–2713.
30. Hallsworth, J.E., and Magan, N. (1994c) Effects of KCl concentration on accumulation of acyclic sugar alcohols and trehalose in conidia of three entomopathogenic fungi. Lett Appl Microbiol 18: 8–11.
31. Hallsworth, J.E., and Magan, N. (1995) Manipulation of intracellular glycerol and erythritol enhances germination of conidia at low water availability. Microbiol-SGM 141: 1109–1115.
32. Hallsworth, J.E., and Magan, N. (1997) A rapid HPLC protocol for detection of polyols and trehalose. J Microbiol Methods 29: 7–13.
33. Hallsworth, J.E., and Nomura, Y. (1999) A simple method to determine the water activity of ethanol-containing samples. Biotechnol Bioeng 62: 242–245.
34. Hallsworth, J.E., Prior, B.A., Nomura, Y., Iwahara, M., and Timmis, K.N. (2003a) Compatible solutes protect against chaotrope (ethanol)-induced, nonosmotic water stress. Appl Environ Microbiol 69: 7032–7034.
35. 2-containing environments: chaotropicity defines the window. Environ Microbiol 9: 803–813.
36. Harrison, J.P., Hallsworth, J.E., and Cockell, C.S. (2015) Reduction of the temperature sensitivity of Halomonas hydrothermalis by iron starvation combined with microaerobic conditions. Appl Environ Microbiol 81: 2156–2162.
37. Hill, T.A. (1977) The Biology of Weeds. London, UK: E. Arnold.
38. Hocking, A.D. (1993) Responses in xerophilic fungi to changes in water activity. In Stress Tolerance of Fungi. Jennings D.H. (ed). New York: Marcel Dekker, Inc., pp. 233–243.
39. Houbraken, J., and Samson, R.A. (2011) Phylogeny of Penicillium and the segregation of Trichocomaceae into three families. Stud Mycol 70: 1–51.
40. Hubka, V., Kolarik, M., Kubátová, A., and Peterson, S.W. (2013) Taxonomic revision of the genus Eurotium and transfer of species to Aspergillus. Mycologia 105: 912–937.
41. Huchet, V., Pavan, S., Lochardet, A., Divanac'h, M.L., Postollec, F., and Thualt, D. (2013) Development and application of a predictive model of Aspergillus candidus growth as a tool to improve shelf life of bakery products. Food Microbiol 36: 254–259.
42. Javor, B.J. (1984) Growth potential of halophilic bacteria isolated from solar salt environments: carbon sources and salt requirements. Appl Environ Microbiol 48: 352–360.
43. Johnston, C.G., and Vestal, J.R. (1991) Photosynthetic carbon incorporation and turnover in Antarctic cryptoendolithic microbial communities—are they the slowest-growing communities on Earth? Appl Environ Microbiol 57: 2308–2311.
44. de Jong, J.C., McCormack, B.J., Smirnoff, N., and Talbot, N.J. (1997) Glycerol generates turgor in rice blast. Nature 389: 244.
45. Juarez, Z.N., Hernandez, L.R., Bach, H., Sanchez-Arreola, E., and Bach, H. (2015) Antifungal activity of essential oils extracted from Agastache mexicana ssp. xolocotziana and Porophyllum linaria against post-harvest pathogens. Ind Crops Prod 74: 178–182.
46. Kachalkin, A.V., and Yurkov, A.M. (2012) Yeast communities in Sphagnum phyllosphere along the temperature-moisture ecocline in the boreal forest-swamp ecosystem and description of Candida sphagnicola sp. nov. Anton Leeuw Int J G 102: 29–43.
47. Kis-Papo, T., Weig, A.R., Riley, R., Peršoh, D., Salamov, A., Sun, H., et al. (2014) Genomic adaptations of the halophilic Dead Sea filamentous fungus Eurotium rubrum. Nat Commun 5: 3745. Doi: 10.1038/ncomms4745
48. Kminek, G., Rummel, J.D., Cockell, C.S., Atlas, R., Barlow, N., Beaty, D., et al. (2010) Report of the COSPAR Mars special regions colloquium. Adv Space Res 46: 811–829.
49. Lages, F., Silva-Graca, M., and Lucas, C. (1999) Active glycerol uptake is a mechanism underlying halotolerance in yeasts: a study of 42 species. Microbiology 145: 2577–2585.
50. Leong, S.L.L., Lantz, H., Pettersson, O.V., Frisvad, J.C., Thrane, U., Heipieper, H.J., et al. (2015) Genome and physiology of the ascomycete filamentous fungus Xeromyces bisporus the most xerophilic organism isolated to date. Environ Microbiol 17: 496–513.
51. Lievens, B., Hallsworth, J.E., Belgacem, Z.B., Pozo, M.I., Stevenson, A., Willems, K.A., et al. (2015) Microbiology of sugar-rich environments: diversity, ecology, and system constraints. Environ Microbiol 17: 278–298.
52. de Lima Alves, F., Stevenson, A., Baxter, E., Gillion, J.L., Hejazi, F., Hayes, S., et al. (2015) Concomitant osmotic and chaotropicity-induced stresses in Aspergillus wentii: compatible solutes determine the biotic window. Curr Genet 61: 457–477.
53. Lomstein, B.A., Langerhuus, A.T., D'hondt, S., Jorgensen, B.B., and Spivack, A.J. (2012) Endospore abundance, microbial growth and necromass turnover in deep subseafloor sediment. Nature 484: 101–104.
54. Magan, N. (2001) Physiological approaches to improving the ecological fitness of fungal biocontrol agents. In Fungi as Biocontrol Agents. Butt, T. M., Jackson, C. W., and Magan, N. (eds). Oxon: CAB Publishing, pp. 239–250.
55. Mattenberger, F., Sabater-Muñoz, B., Hallsworth, J.E., and Fares, M.A. (In press) Glycerol stress in Saccharomyces cerevisiae: cellular responses and evolved adaptations. Environ Microbiol
56. Micheluz, A., Sulyok, M., Manente, S., Krska, R., Varese, G.C., and Ravagnan, G. (2016) Fungal secondary metabolite analysis applied to Cultural Heritage: the case of a contaminated library in Venice. World Mycotoxin J 9: 397–407.
57. Miskei, M., Karányi, Z., and Pócsi, I. (2009) Annotation of stress–response proteins in the aspergilli. Fungal Genet Biol 46: S105–S120.
58. Nazareth, S.W., and Gonsalves, V. (2014) Halophilic Aspergillus penicillioides from athalassohaline, thalassohaline, and polyhaline environments. Front Microbiol 5: 412.
59. Okano, K., Ose, A., Takai, M., Kaneko, M., Nishioka, C., et al. (2015). Inhibition of aflatoxin production and fungal growth on stored corn by allyl isothiocyanate vapor. Shokuhin Eiseigaku Zasshi 56: 1–7.
60. Oren, A. (1995) The role of glycerol in the nutrition of halophilic archaeal communities: a study of respiratory electron transport. FEMS Microbiol Ecol 16: 281–290.
61. Oren, A. (2010) Thoughts on the “missing link” between saltworks biology and solar salt quality. Global NEST J 12: 417–425.
62. Oren, A. (in press) Glycerol metabolism in hypersaline environments. Environ Microbiol. Doi: 10.1111/1462-2920.13493
63. Oren, A., and Gurevich, P. (1994) Production of d-lactate, acetate, and pyruvate from glycerol in communities of halophilic archaea in the Dead Sea and in saltern crystallizer ponds. FEMS Microbiol Ecol 14: 147–156.
64. Oren, A., and Hallsworth, J.E. (2014) Microbial weeds in hypersaline habitats: the enigma of the weed-like Haloferax mediterranei. FEMS Microbiol Lett 359: 134–142.
65. Parkes, R.J., Cragg, B.A., and Wellsbury, P. (2000) Recent studies on bacterial populations and processes in subseafloor sediments: a review. Hydrogeol J 8: 11–28.
66. Patiño-Vera, M., Jiménez, B., Balderas, K., Ortiz, M., Allende, R., Carrillo A., and Galindo, E. (2005) Pilot-scale production and liquid formulation of Rhodotorula minuta, a potential biocontrol agent of mango anthracnose. J Appl Microbiol 99: 540–550.
67. Paulussen, C., Hallsworth, J.E., Álvarez-Pérez, S., Nierman, W.C., Hamill, P.G., Blain, D., et al. (in press) Ecology of aspergillosis: insights into the pathogenic potency of Aspergillus fumigatus and some other Aspergillus species. Microbial Biotechnol Doi: 10.1111/1751-7915.12367
68. Pettersson, O.V., Su-Lin, L.L., Lantz, H., Rice, T., Dijksterhuis, J., Houbraken, J., et al. (2011) Phylogeny and intraspecific variation of the extreme xerophile, Xeromyces bisporus. Fungal Biol 115: 1100–1111.
69. Pitt, J.I., and Christian, J.H.B. (1968) Water relations of xerophilic fungi isolated from prunes. Appl Environ Microbiol 16: 1853–1858.
70. Pitt, J.I. (1975) Xerophilic fungi and the spoilage of foods of plant origin. In Water Relations of Foods. Duckworth, R.B. (ed.). London, UK: Academic Press, 273–307.
71. Pitt, J.I., and Hocking, A.D. (1977) Influence of solute and hydrogen ion concentration on the water relations of some xerophilic fungi. J Gen Microbiol 101: 35–40.
72. Pitt, J.I., and Hocking, A.D. (2009). Aspergillus. Fungi and Food Spoilage, 3rd edn Springer: New York, USA, 3–9.
73. Qian, P., Schoenau, J., and Urton, R. (2011) Effect of soil amendment with thin stillage and glycerol on plant growth and soil properties. J Plant Nutr 34: 2206–2221.
74. Rangel, D.E., Braga, G.U., Fernandes, ÉK., Keyser, C.A., Hallsworth, J.E., and Roberts, D.W. (2015a) Stress tolerance and virulence of insect-pathogenic fungi are determined by environmental conditions during conidial formation. Curr Genet 61: 383–404.
75. Rangel, D.E.N., Alder-Rangel, A., Dadachova, E., Finlay, R.D., Kupiec, M., Dijksterhuis et al. (2015b) Fungal stress biology: a preface to the Fungal Stress Responses special edition. Curr Genet 61: 231–238.
76. Rosso, L., and Robinson, T.P. (2001) A cardinal model to describe the effect of water activity on the growth of moulds. Int J Food Microbiol 63: 265–273.
77. Rummel, J.D., Beaty, D.W., Jones, M.A., Bakermans, C., Barlow, N.G., Boston, P., et al. (2014) A new analysis of Mars ‘Special Regions’, findings of the second MEPAG Special Regions Science Analysis Group (SR-SAG2). Astrobiology 14: 887–968.
78. Samson, R.A., and Lustgraaf, B.V.D. (1978) Aspergillus penicilloides and Eurotium halophilicum in association with house-dust mites. Mycopathologia 64: 13–16.
79. Santos, R., de Carvalho, C.C.R., Stevenson, A., Grant, I.R., and Hallsworth, J.E. (2015) Extraordinary solute-stress tolerance contributes to the environmental tenacity of mycobacteria. Environ Microbial Rep 7(5): 746–764.
80. Sformo, T., Walters, K., Jeannet, K., Wowk, B., Fahy, G.M., Barnes, B.M., and Duman, J.G. (2010) Deep supercooling, vitrification and limited survival to −100°C in the Alaskan beetle Cucujus clavipes puniceus (Coleoptera: Cucujidae) larvae. J Exp Biol 213: 502–509.
81. Snow, D. (1949) The germination of mould spores at controlled humidities. Ann Appl Biol 36: 1–13.
82. Stevenson, A., Cray, J.A., Williams, J.P., Santos, R., Sahay, R., Neuenkirchen, N., et al. (2015a) Is there a common water-activity limit for the three domains of life?. ISME J 9: 1333–1351.
83. Stevenson, A., Burkhardt, J., Cockell, C.S., Cray, J.A., Dijksterhuis, J., Fox-Powell, M., et al. (2015b) Multiplication of microbes below 0.690 water activity: implications for terrestrial and extraterrestrial life. Environ Microbiol 2: 257–277.
84. Stevenson, A., and Hallsworth, J.E. (2014) Water and temperature relations of soil Actinobacteria. Environ Microbiol Rep 6: 744–755.
85. Stevenson, A., Hamill, P.G., Dijksterhuis, J., Leong, S.L., and Hallsworth, J.E. (in press) Water-, pH- and temperature relations of germination for the extreme xerophiles Xeromyces bisporus (FRR 0025), Aspergillus penicillioides (JH06THJ), and Eurotium halophilicum (FRR 2471). Microbiol Biotechnol. doi: 10.1111/1751-7915.12406
86. Sun, H.J., and Friedmann, E.I. (1999) Growth on geological time scales in the Antarctic cryptoendolithic microbial community. Geomicrobiol J 16: 193–202.
87. Tassou, C.C., Panagou, E.Z., Natskoulis, P., and Magan, N. (2007) Modelling the effect of temperature and water activity on the growth of two ochratoxigenic strains of Aspergillus carbonarius from Greek wine grapes. J Appl Microbiol 103: 2267–2276.
88. Vilhelmsson, O., and Miller, K.J. (2002) Humectant permeability influences growth and compatible solute uptake by Staphylococcus aureus subjected to osmotic stress. J Food Prot 65: 1008–1015.
89. Wang, Z.X., Zhugea, J., Fanga, H., and Prior, B.A (2001) Glycerol production by microbial fermentation: A review. Biotechnol Adv 19: 201–223.
90. Wei, M., Yu, Z.S., Zhang, H.X. (2015). Molecular characterization of microbial communities in bioaerosols of a coal mine by 454 pyrosequencing and real-time PCR. J Environ Sci 30: 241–251.
91. Wheeler, K.A., and Hocking, A.D. (1988) Water relations of Paecilomyces variotii, Eurotium amstelodami, Aspergillus candidus and Aspergillus sydowii, xerophilic fungi isolated from Indonesian dried fish. Int J Food Microbiol 7: 73–78.
92. Williams, J.P., and Hallsworth, J.E. (2009) Limits of life in hostile environments; no limits to biosphere function? Environ Microbiol 11: 3292–3308.
93. Winston, P.W., and Bates, P.S. (1960) Saturated salt solutions for the control of humidity in biological research. Ecology 41: 232–237.
94. Wyatt, T.T., Golovina, E.A., Leeuwen, R., Hallsworth, J.E., Wösten, H.A., and Dijksterhuis, J. (2015) A decrease in bulk water and mannitol and accumulation of trehalose and trehalose-based oligosaccharides define a two-stage maturation process towards extreme stress resistance in ascospores of Neosartorya fischeri (Aspergillus fischeri). Environ Microbiol 17: 383–394.
95. Yakimov, M.M., Lo Cono, V., La Spada, G., Bortoluzzi, G., Messina, E., Smedile, F., et al. (2015) Microbial community of seawater-brine interface of the deep-sea brine Lake Kryos as revealed by recovery of mRNA are active below the chaotropicity limit of life. Environ Microbiol 17: 364–382.
96. Zajc, J., Džeroski, S., Kocev, D., Oren, A., Sonjak, S., Tkavc, R., et al. (2014) Chaophilic or chaotolerant fungi: a new category of extremophiles? Front Microbiol 5: 708.
97. Zhang, X.Y., Zhang, Y., Xu, X.Y., Qi, S.H. (2013). Diverse deep-sea fungi from the South China Sea and their antimicrobial activity. Curr Microbiol 67: 525–530.
98. Zhao, S., et al. (2014). Bio-organic fertilizer application significantly reduces the Fusarium oxysporum population and alters the composition of fungi communities of watermelon Fusarium wilt rhizosphere soil. Biol Fert Soils 50: 765–774.