Diversity, cold active enzymes and adaptation strategies of bacteria inhabiting glacier cryoconite holes of High Arctic

Extremophiles

Volumn 18, Issue 2, 2014, Pages 229-242

  Singh, Purnima ^a   Singh, Shiv M ^b   Dhakephalkar, Prashant ^c  

^a BIRLA INSTITUTE OF TECHNOLOGY AND SCIENCE   (India)

^b NATIONAL CENTRE FOR ANTARCTIC AND OCEAN RESEARCH   (India)

^c AGHARKAR RESEARCH INSTITUTE   (India)

Author keywords

Bacteria; Biotechnological potentials; Diversity; Svalbard Glacier

Indexed keywords

BACTERIAL PROTEIN; ENZYME;

ADAPTATION; ARCTIC; ARTICLE; BACTERIUM; GENETICS; ICE COVER; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MICROFLORA; PHENOTYPE;

ADAPTATION, PHYSIOLOGICAL; ARCTIC REGIONS; BACTERIA; BACTERIAL PROTEINS; ENZYMES; ICE COVER; MICROBIOTA; PHENOTYPE;

EID: 84896808925     PISSN: 14310651     EISSN: 14334909     Source Type: Journal    
DOI: 10.1007/s00792-013-0609-6     Document Type: Article

References (74)

1. Abyzov S, Mitskevich I, Poglazova M (1998) Microflora of the deep glacier horizons of Central Antarctica. Microbiol 67: 66-73.
2. Anesio AM, Mindl B, Laybourn-Parry J, Hodson AJ, Sattler B (2007) Viral dynamics in cryoconite holes on a high Arctic glacier (Svalbard). J Geophys Res 112: G04S31.
3. Anesio AM, Hodson AJ, Fritz A, Psenner R, Sattler B (2009) High microbial activity on glaciers: importance to the global carbon cycle. Global Change Biol 15: 955-960.
4. Annous BA, Becker LA, Bayles DO, Labeda DP, Wilkinson BJ (1997) Critical role of anteiso-C15: 0 fatty acid in the growth of Listeria monocytogenes at low temperatures. Appl Environ Microbiol 63: 3887-3894.
5. Bagshaw EA, Tranter M, Wadham JL, Fountain AG, Mowlem M (2011) High-resolution monitoring reveals dissolved oxygen dynamics in an Antarctic cryoconite hole. Hydrol Process 25: 2868-2877.
6. Bakermans C, Tsapin AI, Souza-Egipsy V, Gilichinsky DA, Nealson KH (2003) Reproduction and metabolism at -10°C of bacteria isolated from Siberian permafrost. Environ Microbiol 5: 321-326.
7. Bauer AW, Kirby MM, Sherris JC, Truck M (1966) Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 45: 493-496.
8. Cameron KA, Hodson AJ, Osborn AM (2011) Structure and diversity of bacterial, eukaryotic and Archaeal communities in glacial cryoconite holes from the Arctic and the Antarctic. FEMS Microbiol Ecol 82: 254-267. doi: 10. 1111/j. 1574-6941. 2011. 01277. x.
9. Chintalapati S, Kiran MD, Shivaji S (2004) Role of membrane lipid fatty acids in cold adaptation. Cell Mol Biol (Noisy-le-grand) 50: 631-642.
10. Christner BC, Kvitko BH, Reeve JN (2003) Molecular identification of Bacteria and Eukarya inhabiting an Antarctic cryoconite hole. Extremophiles 7: 177-183.
11. Donderski W, Mudryk Z, Walczak M (1998) Utilization of low molecular weight organic compounds by marine neustonic and planktonic bacteria. Pol J Environ Stud 7: 279-283.
12. Edwards A, Anesio AM, Rassner SM, Sattler B, Hubbard B, Perkins WT, Young M, Griffith GW (2011) Possible interactions between bacterial diversity, microbial activity and supraglacial hydrology of cryoconite holes in Svalbard. ISME J 5: 150-160.
13. Edwards A, Rassner SME, Anesio AM, Worgan HJ, Irvine-Fynn TDL, Williams HW, Sattler B, Griffith GW (2013) Contrasts between the cryoconite and ice-marginal bacterial communities of Svalbard glaciers. Polar Res 32: 19468. doi: 10. 3402/polar. v32i0. 19468.
14. Feller G, Gerday C (2003) Psychrophilic enzymes: hot topics in cold adaptation. Nat Rev Microbiol 1: 200-208.
15. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783-791.
16. Foreman CM, Sattler B, Mikucki JA, Porazinska DL, Priscu JC (2007) Metabolic activity and diversity of cryoconites in the Taylor Valley, Antarctica. J Geophys Res 112: G04S32. doi: 10. 1029/. 2006JG000358.
17. Fountain AG, Nylen TH, Tranter M, Bagshaw E (2008) Temporal variations in physical and chemical features of cryoconite holes on Canada Glacier, McMurdo Dry Valleys, Antarctica. J Geophys Res 113: G01S92. doi: 10. 1029/2007JG000430.
18. Gerdel RW, Drouet F (1960) The cryoconite of the Thule Area, Greenland. Trans Am Microsc Soc 79: 256-272.
19. Groudieva T, Kambourova M, Yusef H, Royter M, Grote R, Trinks H, Antranikian G (2004) Diversity and cold-active hydrolytic enzymes of culturable bacteria associated with Arctic sea ice, Spitzbergen. Extremophiles 8: 475-488.
20. Hagen JO, Satrang A (1991) Radio-echo soundings of sub-polar glaciers with low-frequency radar. Polar Res 9: 99-107.
21. Hagen JO, Kohler J, Melvold K, Winther JG (2003) Glaciers in Svalbard: mass balance, runoff and freshwater flux. Polar Res 22: 145-159.
22. Hammer O, Harper DAT, Ryan PD (2001) PAST: paleontological Statistics software package for education and data analysis. Palaeontol Electron 4: 1-9.
23. Harding T, Jungblut AD, Lovejoy C, Vincent WF (2011) Microbes in high Arctic snow and implications for the cold biosphere. Appl Environ Microbiol 77: 3234-3243. doi: 10. 1128/AEM. 02611-10.
24. Hodson A, Anesio AM, Ng F, Watson R, Quirk J, Irvine-Fynn T., Dye A, Clark C, McCloy P, Kohler J, Sattler B (2007) A glacier respires: quantifying the distribution and respiration CO2 flux of cryoconite across an entire Arctic supraglacial ecosystem. J Geophys Res 112: G04S36. doi: 10. 1029/2007JG000452.
25. Hodson A, Anesio AM, Tranter M, Fountain A, Osborn M, Priscu J, Laybourn-Parry J, Sattler B (2008) Glacial ecosystems. Ecol Monogr 78: 41-67.
26. Hodson A, Cameron K, Bøggild C, Irvine-fynn T, Langford H, Pearce D, Banwart S (2010) The structure, biological activity and biogeochemistry of cryoconite aggregates upon an Arctic valley glacier: Longyearbreen, Svalbard. J Glaciol 56: 349-361.
27. Jiang HL, Tay STL, Maszenan AM, Tay JH (2006) Physiological traits of bacterial strains isolated from phenol-degrading aerobic granules. FEMS Microbiol Ecol 57: 182-191.
28. Kastovska K, Elster J, Stibal M, Santruckova H (2005) Microbial assemblages in soil microbial succession after glacial retreat in Svalbard (High Arctic). Microbial Ecol 50: 396-407.
29. Konieczna I, Wojtasik B, Kwinkowski M, Burska D, Nowinski K, Żarnowiec P, Kaca W (2011) Analysis of cultivable aerobic bacteria isolated from bottom sediments in the Wijdefjorden region, Spitsbergen. Pol Polar Res 32: 181-195.
30. Kuwae T, Hosokawa Y (1999) Determination of abundance and biovolume of bacteria in sediments by dual staining with 4′, 6-diamidino-2-phenylindole and Acridine Orange: relationship to dispersion treatment and sediment characteristics. Appl Environ Microbiol 65: 3407-3412.
31. Lee YM, Kim S-Y, Jung J, Kim EH, Cho KH, Schinner F, Margesin R, Hong SG, Lee HK (2011) Cultured bacterial diversity and Human impact on Alpine glacier Cryoconite. J Microbiol 49: 355-362.
32. Leslie A (1879) The Arctic Voyages of A E Nordenskjöld. MacMillan and Co., London.
33. Martinez JL (2012) Natural antibiotic resistance and contamination by antibiotic resistance determinants: the two ages in the evolution of resistance to antimicrobials. Front Microbiol 3: 1. doi: 10. 3389/fmicb. 2012. 00001.
34. McIntyre NF (1984) Cryoconite hole thermodynamics. Can J Earth Sci 21: 152-156.
35. Mudryk ZJ, Podgórska B, Dwulit M (2005) Bacterial utilization of amino acids and carbohydrates in a marine beach. Baltic Coast Zone 9: 29-41.
36. Mueller DR, Pollard WH (2004) Gradient analysis of cryoconite ecosystems from two polar glaciers. Polar Biol 27: 66-74.
37. Mueller DR, Vincent WF, Pollard WH, Fritsen CH (2001) Glacial cryoconite ecosystems: a bipolar comparison of algal communities and habitats. Nova Hedwig Beih 123: 173-197.
38. Nishida I, Murata N (1996) Chilling sensitivity in plants and cyanobacteria: the crucial contribution of membrane lipids. Annu Rev Plant Physiol Plant Mol Biol 47: 541-568.
39. Paul EA, Clark FE (1989) Soil microbiology and biochemistry. Elsevier, New York.
40. Porazinska DL, Fountain AG, Nylen TH, Tranter M, Virginia RA, Wall DH (2004) The biodiversity and biogeochemistry of cryoconite holes from McMurdo Dry Valley glaciers, Antarctica. Arctic Antarctic Alpine Res 36: 84-91.
41. Reddy GSN, Aggarwal RK, Matsumoto GI, Shivaji S (2000) Arthrobacter flavus sp. nov., a psychrophilic bacterium isolated from a pond in McMurdo Dry Valley, Antarctica. Int J Syst Evol Microbiol 50: 1553-1561.
42. Reddy PVV, Rao SSSN, Pratibha MS, Sailaja B, Kavya B, Manorama RR, Singh SM, Srinivas TNR, Shivaji S (2009) Bacterial diversity and bioprospecting for cold-active enzymes from culturable bacteria associated with sediment from a melt water stream of Midre Lovénbreen glacier, an Arctic glacier. Res Microbiol 160: 538-546.
43. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
44. Sala MM, Arin L, Balagué V, Felipe J, Guadayol Ò, Vaqué D (2005) Functional diversity of bacterioplankton assemblages in western Antarctic seawaters during late spring. Mar Ecol Prog Ser 292: 13-21.
45. Sala MM, Terrado R, Lovejoy C, Unrein F, Pedros-Alio C (2008) Metabolic diversity of heterotrophic bacterioplankton over winter and spring in the coastal Arctic Ocean. Environ Microbiol 10: 942-949.
46. Sala MM, Arrieta JM, Boras JA, Duarte CM, Vaqué D (2010) The impact of ice melting on bacterioplankton in the Arctic Ocean. Polar Biol 33: 1683-1694. doi: 10. 1007/s00300-010-0808-x.
47. Säwström C, Mumford P, Marshall W, Hodson A, Laybourn-parry J (2002) The microbial communities and primary productivity of cryoconite holes in Arctic glacier (Svalbard 79°N). Polar Biol 25: 591-596.
48. Segawa T, Takeuchi N, Rivera A, Yamada A, Yoshimura Y, Barcaza G, Shinbori K, Motoyama H, Kohshima S, Ushida K (2012) Distribution of antibiotic resistance genes in glacier environments. Environ Microbiol Rep 5: 127-134. doi: 10. 1111/1758-2229. 12011.
49. Shivaji S, Kiran MD, Chintalapati S (2007) Perception and Transduction of Low Temperature in Bacteria. In: Gerday C, Glansdorff N (eds) Physiology and biochemistry of extremophiles. ASM Press, Washington, DC, pp 194-207.
50. Shivaji S, Begum Z, Rao SSSN, Reddy PVV, Manasa P, Sailaja B, Prathiba MS, Thamban M, Krishnan KP, Singh SM, Srinivas TN (2013) Antarctic ice core samples: culturable bacterial diversity. Res Microbiol 164: 70-82. doi: 10. 1016/j. resmic. 2012. 09. 001.
51. Singh P, Singh SM (2011) Characterization of yeast and filamentous fungi isolated from cryoconite holes of Svalbard, Arctic. Polar Biol 35: 575-583.
52. Singh SM, Sharma J, Gawas-Sakhalkar P, Upadhyay AK, Pedneker SM, Ravindra R (2012) Atmospheric deposition studies of heavy metals in Arctic by comparative analysis of lichens and cryoconite. Environ Monit Assess 185: 1367-1376. doi: 10. 1007/s10661-012-2638-5.
53. Sjolund M, Bonnedahl J, Hernandez J, Bengtsson S, Cederbrant G, Pinhassi J, Kahlmeter G, Olsen B (2008) Dissemination of multidrug-resistant bacteria into the Arctic. Emerg Infect Dis 14: 70-72.
54. Smibert RM, Krieg NR (1994) Phenotypic characterisation. In: Gerhardt P, Murray GGE, Wood WA, Krieg NR (eds) Methods for general and molecular bacteriology. American Society for Microbiology, Washington, DC, pp 607-654.
55. Srinivas TNR, Rao SSSN, Reddy PVV, Pratibha MS, Sailaja B, Kavya B, Kishore KH, Begum Z, Singh SM, Shivaji S (2009) Bacterial diversity and bioprospecting for cold-active lipases, amylases and proteases, from culturable bacteria of Kongsfjorden and Ny-Alesund, Svalbard, Arctic. Curr Microbiol 59: 537-547.
56. Steven B, Briggs G, McKay CP, Pollard WH, Greer CW, Whyte LG (2007) Characterization of the microbial diversity in a permafrost sample from the Canadian high Arctic using culture-dependent and culture-independent methods. FEMS Microbiol Ecol 59: 513-523.
57. Stibal M, Šabacká M, Kaštovská K (2006) Microbial communities on glacier surfaces in Svalbard: impact of physical and chemical properties on abundance and structure of cyanobacteria and algae. Microb Ecol 52: 644-654.
58. Stibal M, Tranter M, Benning LG, Rehák J (2008) Microbial primary production on an Arctic glacier is insignificant in comparison with allochthonous organic carbon input. Environ Microbiol 10: 2172-2178.
59. Stibal M, Šabackà M, Žàrský J (2012) Biological processes on glacier and ice sheet surfaces. Nat Geosci 5: 771-774. doi: 10. 1038/ngeo1611.
60. Takeuchi N, Kohshima S, Goto-Azuma K, Korner RM (2001) Biological characteristics of dark coloured material (cryoconite) on Canadian Arctic glaciers (Devon and Penny ice caps). Mem Natl Inst Polar Res 54: 495-505.
61. Takeuchi N, Nishiyama H, Li Z (2010) Structure and formation process of cryoconite granules on Ürümqi glacier No. 1, Tien Shan, China. Ann Glaciol 51: 9-14.
62. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10: 512-526.
63. Tamura K, Dudley J, Nei M, Kumar S (2007) Molecular evolutionary genetics analysis (MEGA) software version 4. 0. Mol Biol Evol 24: 1596-1599.
64. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739. doi: 10. 1093/molbev/msr121.
65. Teather RM, Wood PJ (1982) Use of Congo red-polysaccharide interactions in enumeration and characterisation of cellulolytic bacteria from bovine rumen. Appl Environ Microbiol 43: 777-780.
66. Tranter M, Fountain AG, Fritsen CH, Lyons WB, Priscu JC, Statham PJ, Welch KA (2004) Extreme hydrochemical conditions in natural microcosms entombed within Antarctic ice. Hydrol Process 18: 379-387.
67. Vincent WF, Howard-Williams C (1994) Nitrate-rich inland waters of the Ross Ice Shelf region, Antarctica. Antarct Sci 87: 339-346.
68. Wharton RA Jr, McKay CP, Simmons GM Jr, Parker BC (1985) Cryoconite holes on glaciers. Bioscience 35: 499-503.
69. Xiang S, Yao T, An L, Xu B, Wang J (2005) 16S rRNA sequences and differences in bacteria isolated Muztag Ata Glacier at increasing depths. Appl Environ Microbiol 71: 4619-4627.
70. Xu Y, Simpson AJ, Eyles N, Simpson MJ (2010) Sources and molecular composition of cryoconite organic matter from the Athabasca Glacier, Canadian Rocky Mountains. Org Geochem 41: 177-186.
71. Yallop ML, Anesio AM (2010) Benthic diatom flora in supraglacial habitats: a generic-level comparison. Ann Glaciol 51: 15-22.
72. Yu Y, Li HR, Zeng YX, Chen B (2009) Extracellular enzymes of cold-adapted bacteria from Arctic sea ice, Canada Basin. Polar Biol 32: 1539-1547.
73. Yumoto I, Yamazaki K, Hishinuma M, Nodasaka Y, Suemori A, Nakajima K, Inoue N, Kawasaki K (2001) Pseudomonas alcaliphila sp. nov., a novel facultatively psychrophilic alkaliphile isolated from seawater. Int J Syst Evol Microbiol 51: 349-355.
74. Zhang XF, Yao TD, Tian LD, Xu SJ, An LZ (2008) Phylogenetic and physiological diversity of bacteria isolated from Puruogangri ice core. Microb Ecol 55: 476-488.