Polar Biology

, Volume 41, Issue 3, pp 537–551 | Cite as

Effects of temperature on extracellular hydrolase enzymes from soil microfungi

  • Abiramy Krishnan
  • Peter Convey
  • Marcelo Gonzalez
  • Jerzy Smykla
  • Siti Aisyah Alias
Article

Abstract

Soil microbes play important roles in global carbon and nutrient cycling. Soil microfungi are generally amongst the most important contributors. They produce various extracellular hydrolase enzymes that break down the complex organic molecules in the soil into simpler form. In this study, we investigated patterns of amylase and cellulase (which are responsible for breaking down starch and cellulose, respectively) relative activity (RA) on solid media at different culture temperatures in fungal strains from Arctic, Antarctic and tropical soils. Fungal isolates from all three regions were inoculated onto R2A media supplemented with starch for amylase and carboxymethylcellulose and trypan blue for cellulase screening. The isolates were then incubated at 4, 10, 15, 20, 25, 30, 35 and 40 °C and examined for activity after 5 and 10 days, for tropical and polar isolates, respectively. The data obtained indicate that the polar fungal strains exhibited similar patterns of amylase and cellulase RA. Both Arctic and Antarctic fungi showed highest RA for amylase and cellulase at 35 °C, while colony growth was maximised at 15 °C. Colony growth and RA of the polar isolates were negatively correlated suggesting that, as temperatures increase, the cells become stressed and have fewer resources available to invest in growth. Unlike polar isolates, tropical isolates did not exhibit any trend of colony growth with temperature, rather having idiosyncratic patterns in each isolate. The low enzyme production and RA levels in the tropical strains may suggest both a low ability to respond to temperature variation in their natural thermally stable tropical habitats, as well as a level of thermal stress limiting their enzyme production ability.

Keywords

Amylase Cellulase Soil microfungi Arctic Antarctic Tropical 

Notes

Acknowledgements

We thank the Instituto Antartico Chileno, Polish Polar Research Program and Korean Polar Research Institute for their logistic support during the Antarctic expedition in 2007 and Arctic expeditions in 2006 and 2010. We also thank Laura Gerrish, BAS Mapping and Geographic Information Centre, for the preparation of Fig. 1.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

300_2017_2215_MOESM1_ESM.docx (45 kb)
Supplementary material 1 (DOCX 44 kb)

References

  1. Addo-Bediako AS, Chown S, Gaston KJ (2000) Thermal tolerance, climatic variability and latitude. P Roy Soc Lond B 267:739–745CrossRefGoogle Scholar
  2. Aerts R (2006) The freezer defrosting: global warming and litter decomposition rates in cold biomes. J Ecol 94:713–724CrossRefGoogle Scholar
  3. Aislabie J, Fraser R, Duncan S, Farrell RL (2001) Effects of oil spills on microbial heterotrophs in Antarctic soils. Polar Biol 24:308–313CrossRefGoogle Scholar
  4. Ali SH, Alias SA, Siang HY, Smykla J, Pang KL, Guo SY, Convey P (2013) Studies on diversity of soil microfungi in the Hornsund area, Spitsbergen. Polish Polar Res 34:39–54Google Scholar
  5. Anisimov O, Fitzharris BB, Hagen JO, Jefferies B, Marchant H, Nelson F, Prowse T, Vaughan D (2001) Polar regions (Arctic and Antarctic). In: McCarthy JJ, Canziani OF, Leary NA, Dokken DJ, White KS (eds) Climate change 2001: impacts, adaptation, and vulnerability. Contribution of Working Group II to the Third Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, pp 801–841Google Scholar
  6. Anisimov OA, Vaughan DG, Callaghan TV, Furgal C, Marchant H, Prowse TD, Vilhjálmsson H, Walsh JE (2007) Polar regions (Arctic and Antarctic). In: Parry ML, Canziani OF, Palutikof JP, van der Linden PJ, Hanson CE (eds) Climate change 2007: impacts, adaptation and vulnerability. Contribution of Working Group II to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, UK, pp 653–685Google Scholar
  7. Arenz BE, Blanchette RA (2009) Investigations of fungal diversity in wooden structures and soils at historic sites on the Antarctic Peninsula. Can J Microbiol 55:46–56CrossRefPubMedGoogle Scholar
  8. Baldrian P, Voříšková J, Dobiášová P, Merhautová V, Lisá L, Valášková V (2011) Production of extracellular enzymes and degradation of biopolymers by saprotrophic microfungi from the upper layers of forest soil. Plant Soil 338:111–125CrossRefGoogle Scholar
  9. Biasi C, Meyer H, Rusalimova O, Hammerle R, Kaiser C, Baranyi C, Daims H, Lashchinsky N, Barsukov P, Richter A (2008) Initial effects of experimental warming on carbon exchange rates, plant growth and microbial dynamics of a lichen-rich dwarf shrub tundra in Siberia. Plant Soil 307:191–205CrossRefGoogle Scholar
  10. Bilal T, Malik B, Rehman R, Kumar M (2015) Influence of various parameters on cellulase and xylanase production by different strains of Trichoderma Species. Austin J Anal Pharm Chem 2:1034–1039Google Scholar
  11. Bonebrake TC, Mastrandrea MD (2010) Tolerance adaptation and precipitation changes complicate latitudinal patterns of climate change impacts. Proc Natl Acad Sci USA 107:12581–12586CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bradner JR, Gillings M, Nevalainen KHM (1999) Qualitative assessment of hydrolytic activities in Antarctic microfungi grown at different temperatures on solid media. World J Microb Biot 15:131–132CrossRefGoogle Scholar
  13. Brindha RJ, Mohan TS, Immanual G, Jeeva S, Packia Lekshmi NCJ (2011) Studies on amylase and cellulase enzyme activity of the fungal organisms causing spoilage in tomato. Eur J Exp Biol 1:90–96Google Scholar
  14. Burhan A, Nisa U, Gokhan C, Omer C, Ashabil A, Osman G (2012) Amylase production by endophytic fungi Cylindrocephalum sp. isolated from medicinal plant Alpinia calcarata (Haw.) Roscoe. Braz J Microbiol 43:1213–1221CrossRefGoogle Scholar
  15. Chaillan F, Le Flèche A, Bury E, Phantavong YH, Grimont P, Saliot A, Oudot J (2004) Identification and biodegradation potential of tropical aerobic hydrocarbon-degrading microorganisms. Res Microbiol 155:587–595CrossRefPubMedGoogle Scholar
  16. Convey P (1996) Overwintering strategies of terrestrial invertebrates in Antarctica- the significance of flexibility in extremely seasonal environments. Eur J Entomol 93:489–505Google Scholar
  17. Convey P, Chown SL, Clarke A, Barnes DKA, Cummings V, Ducklow H, Frati F, Green TGA, Gordon S, Griffiths H, Howard-Williams C, Huiskes AHL, Laybourn-Parry J, Lyons B, McMinn A, Peck LS, Quesada A, Schiaparelli S, Wall D (2014) The spatial structure of Antarctic biodiversity. Ecol Monogr 84:203–244CrossRefGoogle Scholar
  18. Convey P, Coulson SJ, Worland MR, Sjöblom A Annual and shorter term temperature patterns and variation in the upper layers of polar soils for terrestrial biota. Polar Biol. (In review)Google Scholar
  19. Coulson SJ, Hodkinson LD, Strathdee AT, Block W, Webb NR, Bale JS, Worland MR (1995) Thermal environments of Arctic soil organisms during winter. Arctic Alpine Res 27:364–370CrossRefGoogle Scholar
  20. Cunningham EL, Agard DA (2004) Disabling the folding catalyst is the last critical step in alpha-lytic protease folding. Protein Sci 13:325–331CrossRefPubMedPubMedCentralGoogle Scholar
  21. de Graaff MA, Classen AT, Castro HF, Schadt CW (2010) Labile soil carbon inputs mediate the soil microbial community composition and plant residue decomposition rates. New Phytol 188:1055–1064CrossRefPubMedGoogle Scholar
  22. Deshpande P, Nair S, Khedkar S (2009) Water hyacinth as carbon source for the production of cellulase by Trichoderma reesei. Appl Biochem Biotech 158:552–560CrossRefGoogle Scholar
  23. Deutsch CA, Tewksbury J, Huey RB, Sheldon K, Ghalambor C, Haak D, Martin PR (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proc Natl Acad Sci USA 105:6668–6672CrossRefPubMedPubMedCentralGoogle Scholar
  24. Dong Y, Somero GN (2009) Temperature adaptation of cytosolic malate dehydrogenases of limpets (genus Lottia): differences in stability and function due to minor changes in sequence correlate with biogeographic and vertical distributions. J Exp Biol 212:169–177CrossRefPubMedGoogle Scholar
  25. Duncan SM, Minasaki R, Farrell RL, Thwaites JM, Held BW, Arenz BE, Jurgens JA, Blanchette RA (2008) Screening fungi isolated from historic Discovery Hut on Ross Island, Antarctica for cellulose degradation. Antarct Sci 20:463–470CrossRefGoogle Scholar
  26. Fahnestock JT, Jones MH, Brooks PD, Walker DA, Welker JM (1998) Winter and early spring CO2 efflux from tundra communities of northern Alaska. J Geophys Res-Atmos 103:29023–29027CrossRefGoogle Scholar
  27. Feller G, Gerday C (2003) Psychrophilic enzymes: hot topics in cold adaptation. Nat Rev Microbiol 1:200–208CrossRefPubMedGoogle Scholar
  28. Ferrari BC, Zhang CD, Dorst J (2011) Recovering greater fungal diversity from pristine and diesel fuel contaminated sub-Antarctic soil through cultivation using both a high and a low nutrient media approach. Front Microbiol 2:1–14CrossRefGoogle Scholar
  29. Florczak T, Daroch M, Wilkinson MC, Bialkowska A, Bates AD, Turkiewicz M, Iwanejko LA (2013) Purification, characterisation and expression in Saccharomyces cerevisiae of LipG7 an enantioselective, cold-adapted lipase from the Antarctic filamentous fungus Geomyces sp. P7 with unusual thermostability characteristics. Enzyme Microb Technol 53:18–24CrossRefPubMedGoogle Scholar
  30. Gao B, Mao Y, Zhang L, He L, Wei D (2016) A novel saccharifying α-amylase of Antarctic psychrotolerant fungi Geomyces pannorum: gene cloning, functional expression, and characterization. Starch-Stärke 68:20–28CrossRefGoogle Scholar
  31. Gawas-Sakhalkar P, Singh SM (2011) Fungal community associated with Arctic moss, Tetraplodon mimoides and its rhizosphere: bioprospecting for production of industrially useful enzymes. Res Commun 100:1701–1705Google Scholar
  32. German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD (2011) Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem 43:1387–1397CrossRefGoogle Scholar
  33. German DP, Marcelo KB, Stone MM, Allison SD (2012) The Michaelis-Menten kinetics of soil extracellular enzymes in response to temperature: a cross-latitudinal study. Glob Change Biol 18:1468–1479CrossRefGoogle Scholar
  34. Gesheva V, Vasileva-Tonkova E (2012) Production of enzymes and antimicrobial compounds by halophilic Antarctic Nocardioides sp. grown on different carbon sources. World J Microbiol Biotechnol 28:2069–2076CrossRefPubMedGoogle Scholar
  35. Ghalambor CK, Huey RB, Martin P, Tewksbury J, Wang G (2006) Are mountain passes higher in the tropics? Janzen’s hypothesis revisited. Integr Comp Biol 46:5–17CrossRefPubMedGoogle Scholar
  36. Huestis DL, Oppert B, Marshall JL (2009) Geographic distributions of Idh-1 alleles in a cricket are linked to differential enzyme kinetic performance across thermal environments. BMC Evol Biol 9:113–124CrossRefPubMedPubMedCentralGoogle Scholar
  37. Huey RB (1976) Latitudinal pattern of between-altitude faunal similarity: mountains might be ‘‘higher” in the tropics. Am Nat 112:225–254CrossRefGoogle Scholar
  38. Hugelius G, Bockheim JG, Camill P, Elberling B, Grosse G, Harden JW, Johnson K, Jorgenson T, Koven CD, Kuhry P, Michaelson G, Mishra U, Palmtag J, Ping CL, O’Donnell J, Schirrmeister L, Schuur EAG, Sheng Y, Smith LC, Strauss J, Yu Z (2013) A new data set for estimating organic carbon storage to 3 m depth in soils of the northern circumpolar permafrost region. Earth Syst Sci Data 5:393–402CrossRefGoogle Scholar
  39. Ibrahim MF, Razak MNA, Phang LY, Hassan MA, Abd-Aziz S (2013) Crude cellulase from oil palm empty fruit bunch by Trichoderma asperellum UPM1 and Aspergillus fumigatus UPM2 for fermentable sugars production. Appl Biochem Biotechnol 170:1320–1335CrossRefPubMedGoogle Scholar
  40. Janzen DH (1967) Why mountain passes are higher in the tropics. Am Nat 101:233–249CrossRefGoogle Scholar
  41. Johns GC, Somero GN (2004) Evolutionary convergence in adaptation of proteins to temperature: a4-lactate dehydrogenases of Pacific damselfishes (Chromis spp.). Mol Biol Evol 21:314–320CrossRefPubMedGoogle Scholar
  42. Kleinteich J, Wood SA, Kuepper FC, Camacho A, Quesada A, Frickey T, Dietrich DR (2012) Temperature-related changes in polar cyanobacterial mat diversity and toxin production Nature. Clim Change 2:356–360CrossRefGoogle Scholar
  43. Koch O, Tscherko D, Kandeler E (2007) Temperature sensitivity of microbial respiration, nitrogen mineralization, and potential soil enzyme activities in organic alpine soils. Glob Biogeochem Cycles 21:1–11CrossRefGoogle Scholar
  44. Kochkina GA, Ivanushkina NE, Akimov VN, Gilichinskii DA, Ozerskaya SM (2007) Halo- and psychrotolerant Geomyces fungi from Arctic cryopegs and marine deposits. Microbiology 76:31–38CrossRefGoogle Scholar
  45. Krishnan A, Convey P, Gonzalez-Rocha G, Alias SA (2016) Production of extracellular hydrolase enzymes by fungi from King George Island. Polar Biol 39:65–76CrossRefGoogle Scholar
  46. Kurek E, Korniłłowicz-Kowalska T, Słomka A, Melke J (2007) Characteristics of soil filamentous fungi communities isolated from various micro − relief forms in the high Arctic tundra (Bellsund region, Spitsbergen). Polish Polar Res 28:57–73Google Scholar
  47. Laudelot H, Meyer J (1954) Les cycles d’elements minerales et de matière organique en forêt équatoriale Congolaise. Trans Fifth Int Congr Soil Sci 11:267–272Google Scholar
  48. Manivannan S, Kathiresan K (2007) Alkaline protease production by Penicillium fellutanum isolated from mangrove sediment. Int J Biol Chem 2:98–103Google Scholar
  49. Margesin R, Gander S, Zacke G, Gounot AM, Schinner F (2003) Hydrocarbon degradation and enzyme activities of cold-adapted bacteria and yeasts. Extremophiles 7:451–458CrossRefPubMedGoogle Scholar
  50. Marx MC, Wood M, Jarvis SC (2001) A microplate fluorimetric assay for the study of enzyme diversity in soils. Soil Biol Biochem 33:1633–1640CrossRefGoogle Scholar
  51. Minnis AM, Lindner DL (2013) Phylogenetic evaluation of Geomyces and allies reveals no close relatives of Pseudogymnoascus destructans, comb. nov., in bat hibernacula of eastern North America. Fungal Biol 117:638–649CrossRefPubMedGoogle Scholar
  52. Morita RY (1975) Psychrophilic bacteria. Bacteriol Rev 39:144–167PubMedPubMedCentralGoogle Scholar
  53. Newsham KK, Upson R, Read DJ (2009) Mycorrhizas and dark septate root endophytes in polar regions. Fungal Ecol 2:10–20CrossRefGoogle Scholar
  54. Nye PH (1961) Organic matter and nutrient cycles under moist tropical forest. Plant Soil 13:333–346CrossRefGoogle Scholar
  55. Øvstedal DO, Lewis Smith RI (2001) Lichens of Antarctica and South Georgia-a guide to their identification and ecology. Cambridge University Press, Cambridge, p 424Google Scholar
  56. Prenafeta-Boldu FX, Summerbell R, de Hoog GS (2005) Fungi growing on aromatic hydrocarbons: biotechnology’s unexpected encounter with biohazard? FEMS Microbiol Rev 30:109–130CrossRefGoogle Scholar
  57. Radwan S (2008) Microbiology of oil-contaminated desert soils and coastal areas in the Arabian Gulf region. In: Dion P, Nautiyal CS (eds) Microbiology of extreme soils. Soil Biology 13. Springer, Berlin, pp 275–298Google Scholar
  58. Rashid SS, Alam MZ, Karim MIA, Sallah MH (2009) Optimization of the nutrient supplements for cellulase production with the basal medium palm oil mill effluent. World Acad Sci Eng Technol 3:568–574Google Scholar
  59. Rinnan R, Michelsen A, Baath E, Jonasson S (2007) Mineralization and carbon turnover in subarctic heath soil as affected by warming and additional litter. Soil Biol Biochem 39:3014–3023CrossRefGoogle Scholar
  60. Robinson CH (2001) Cold adaptation in Arctic and Antarctic fungi. New Phytol 151:341–353CrossRefGoogle Scholar
  61. Shaver GR, Giblin AE, Nadelhoffer KJ, Thieler KK, Downs MR, Laundre JA, Rastetter EB (2006) Carbon turnover in Alaskan tundra soils: effects of organic matter quality, temperature, moisture and fertilizer. J Ecol 94:740–753CrossRefGoogle Scholar
  62. Singh SM, Singh SK, Yadav LS, Singh PN, Ravindra R (2012) Filamentous soil fungi from Ny-Ålesund, Spitsbergen, and screening for extracellular enzymes. Arctic 65:45–55CrossRefGoogle Scholar
  63. Sinsabaugh RL, Antibus RK, Linkins AE, Mcclaugherty CA, Rayburn L, Repert D, Weiland T (1993) Wood decomposition: nitrogen and phosphorus dynamics in relation to extracellular enzyme-activity. Ecology 74:1586–1593CrossRefGoogle Scholar
  64. Sogonov MV, Schroers HJ, Gams W, Dijksterhuis J, Summerbell RC (2005) The hyphomycete Teberdinia hygrophila gen. nov., sp. nov. and related anamorphs of Pseudeurotium species. Mycologia 97:695–709CrossRefPubMedGoogle Scholar
  65. Somero GN (2004) Adaptation of enzymes to temperature: searching for basic ‘‘strategies’’. Comp Biochem Physiol 139:321–333CrossRefGoogle Scholar
  66. Sturm M, Schimel J, Michaelson G, Welker JM, Oberbauer SF, Liston GE, Fahnestock J, Romanovsky VE (2005) Winter biological processes could help convert Arctic tundra to shrubland. Bioscience 55:17–26CrossRefGoogle Scholar
  67. Tortella GR, Rubilar O, Gianfreda L, Valenzuela E, Diez MC (2008) Enzymatic characterization of Chilean native wood-rotting fungi for potential use in the bioremediation of polluted environments with chlorophenols. World J Microbiol Biotechnol 24:2805–2818CrossRefGoogle Scholar
  68. Tveit AT, Urich T, Frenzel P, Svenning MM (2015) Metabolic and trophic interactions modulate methane production by Arctic peat microbiota in response to warming. Proc Natl Acad Sci USA 112:2507–2516CrossRefGoogle Scholar
  69. Waring BG, Weintraub SR, Sinsabaugh RL (2014) Ecoenzymatic stoichiometry of microbial nutrient acquisition in tropical soils. Biogeochemistry 117:101–113CrossRefGoogle Scholar
  70. Zeng X, Xiao X, Wang P, Wang FP (2004) Screening and characterization of psychrotrophic, lipolytic bacteria from deep sea sediments. J Microbiol Biotechnol 14:952–958Google Scholar
  71. Zonn SV, Li CK (1962) Dynamics of the breakdown of litter and humus, and seasonal changes in their ash composition, in two types of tropical biogeocoenoses. Soobshch Lab Lesoved. Moskva 6:144–152 (In Russian) Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  • Abiramy Krishnan
    • 1
    • 2
  • Peter Convey
    • 1
    • 4
  • Marcelo Gonzalez
    • 5
  • Jerzy Smykla
    • 6
  • Siti Aisyah Alias
    • 1
    • 3
  1. 1.National Antarctic Research CentreUniversity MalayaKuala LumpurMalaysia
  2. 2.Institute of Biological Science, Faculty of ScienceUniversity MalayaKuala LumpurMalaysia
  3. 3.Institute of Ocean and Earth Science, Institute of Postgraduate StudiesUniversity MalayaKuala LumpurMalaysia
  4. 4.British Antarctic Survey, NERCCambridgeUK
  5. 5.Instituto Antártico ChilenoPunta ArenasChile
  6. 6.Institute of Nature ConservationPolish Academy of SciencesKrakówPoland

Personalised recommendations