Massive regime shifts and high activity of heterotrophic bacteria in an ice-covered lake

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Bižić Ionescu, Mina ^a,b   Amann, Rudolf ^a   Grossart, Hans Peter ^b,c,d  

^a MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

^b LEIBNIZ INSTITUTE OF FRESHWATER ECOLOGY AND INLAND FISHERIES   (Germany)

^c UNIVERSITY OF POTSDAM   (Germany)

^d BERLIN BRANDENBURG INSTITUTE OF ADVANCED BIODIVERSITY RESEARCH BBIB   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CARBON; ICE; RNA 16S; OXYGEN;

APHANIZOMENON; AQUATIC ENVIRONMENT; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIAL OVERGROWTH; CARBON SOURCE; CLIMATE CHANGE; COMMUNITY STRUCTURE; CYANOBACTERIUM; DENATURING GRADIENT GEL ELECTROPHORESIS; FLUORESCENCE IN SITU HYBRIDIZATION; FOOD WEB; GERMANY; HETEROTROPHIC BACTERIUM; LAKE; MICROBIAL BIOMASS; MICROBIAL COMMUNITY; NONHUMAN; PHYSIOLOGICAL STRESS; PHYTOPLANKTON; PROKARYOTES BY HABITAT; PROTEIN SYNTHESIS; PYROSEQUENCING; SNOW COVER; SPECIES DIVERSITY; SPECIES DOMINANCE; WATER TEMPERATURE; WINTER; BACTERIUM; BIODIVERSITY; BIOMASS; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; ECOSYSTEM; GENETIC VARIABILITY; GENETICS; GEOGRAPHY; GROWTH, DEVELOPMENT AND AGING; HETEROTROPHY; ICE COVER; METABOLISM; MICROBIOLOGY; PH; PHYLOGENY; PROCEDURES; SEASON;

BACTERIA; BIODIVERSITY; BIOMASS; CLIMATE CHANGE; CYANOBACTERIA; ECOSYSTEM; GENETIC VARIATION; GEOGRAPHY; GERMANY; HETEROTROPHIC PROCESSES; HYDROGEN-ION CONCENTRATION; ICE COVER; LAKES; OXYGEN; PHYLOGENY; PHYTOPLANKTON; RNA, RIBOSOMAL, 16S; SEASONS; SEQUENCE ANALYSIS, DNA;

EID: 84912535594     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0113611     Document Type: Article

References (43)

1. Benson B, Magnuson J (2007) Global lake and river ice phenology database. National Snow and Ice Data Center/World Data Center for Glaciology, Boulder, CO. Digital media. http//nsidc.org/data/g01377.html.
2. Chapman WL, Walsh JE (1991) Updated 1996. Arctic and Southern Ocean Sea Ice Concentrations. Boulder, Colorado USA.
3. Dokulil MT, Herzig A (2009) An analysis of long-term winter data on phytoplankton and zooplankton in Neusiedler See, a shallow temperate lake, Austria. Aquat Ecol 43: 715-725. doi: 10.1007/s10452-009-9282-3.
4. Boetius A, Albrecht S, Bakker K, Bienhold C, Felden J, et al. (2013) Export of algal biomass from the melting Arctic sea ice. Science 339: 1430-1432. doi: 10.1126/science.1231346.
5. Bertilsson S, Burgin A, Carey CC, Fey SB, Grossart H-P, et al. (2013) The under-ice microbiome of seasonally frozen lakes. Limnol Oceanogr 58: 1998-2012. doi: 10.4319/lo.2013.58.6.1998.
6. Eiler A, Bertilsson S (2004) Composition of freshwater bacterial communities associated with cyanobacterial blooms in four Swedish lakes. Environ Microbiol 6: 1228-1243. doi: 10.1111/j.1462-2920.2004.00657.x.
7. Greenbank J (1945) Limnological conditions in ice-covered lakes, especially as related to winter-kill of fish. Ecol Monogr 15: 343-392.
8. Tulonen T, Kankaala P (1994) Factors controlling production of phytoplankton and bacteria under ice in a humic, boreal lake. J Plankton Res 16: 1411-1432.
9. Twiss MR, McKay RML, Bourbonniere RA, Bullerjahn GS, Carrick HJ, et al. (2012) Diatoms abound in ice-covered Lake Erie: An investigation of offshore winter limnology in Lake Erie over the period 2007 to 2010. J Gt Lakes 38: 18-30.
10. Newton RJ, Jones SE, Eiler A, McMahon KD, Bertilsson S (2011) A guide to the natural history of freshwater lake bacteria. Microbiol Mol Biol Rev 75: 14-49. doi: 10.1128/MMBR.00028-10.
11. Tada Y, Grossart H-P (2014) Community shifts of actively growing lake bacteria after N-acetylglucosamine addition: improving the BrdU-FACS method. ISME J 8: 441-454. doi: 10.1038/ ismej.2013.148.
12. Rösel S, Allgaier M, Grossart H-P (2012) Long-term characterization of free-living and particleassociated bacterial communities in Lake Tiefwaren reveals distinct seasonal patterns. Microb Ecol 64: 571-583. doi: 10.1007/s00248-012-0049-3.
13. Llorens-Marès T (2012) Winter to spring changes in the slush bacterial community composition of a high mountain lake (Lake Redon, Pyrenees). Environ Microbiol Rep 4: 50-56.
14. Glatz R, Lepp P, Ward B, Francis C (2006) Planktonic microbial community composition across steep physical/chemical gradients in permanently ice-covered Lake Bonney, Antarctica. Geobiology 4: 53-67.
15. IPCC 2007 (n.d.) Climate Change 2007: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Parry ML, Canziani OF, Palutikof JP, van der Linden PJ, Hanson CE, editors. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA
16. Dean WE, Gorham E (1998) Magnitude and significance of carbon burial in lakes, reservoirs, and peatlands. Geology 26: 535-538. doi: 10.1130/0091-7613(1998)026<0535: MASOCB>2.3.CO; 2.
17. Koschel R, Adams DD (2003) An approach to understanding a temperate oligotrophic lowland lake (Lake Stechlin, Germany). Adv Limnol 58: 1-9.
18. Ruttner F (1968) Fundamentals of limnology. 3rd ed. Univ of Toronto Press, Toronto.
19. Rösel S, Grossart H-P (2012) Contrasting dynamics in activity and community composition of free-living and particle-associated bacteria in spring. Aquat Microb Ecol 66: 169-181. doi: 10.3354/ame01568.
20. Pernthaler A, Pernthaler J, Amann R (2004) Sensitive multi-color fluorescence in situ hybridization for the identification of environmental microorganisms. In: Kowalchuk G, de Bruijn FJ, Head IM, Akkermans AD, van Elsas JD, editors. Molecular Microbial Ecology Manual. Dodrecht, the Netherlands: Kluwer Academic Publishers, Vol. 2nd edditi. pp. 711-726. doi: 10.1007/978-1-4020-2177-0-311.
21. Pizzetti I, Fuchs BM, Gerdts G, Wichels A, Wiltshire KH, et al. (2011) Temporal variability of coastal Planctomycetes clades at Kabeltonne station, North Sea. Appl Environ Microbiol 77: 5009-5017. doi: 10.1128/AEM.02931-10.
22. Zeder M, Ellrott A, Amann R (2011) Automated sample area definition for high-throughput microscopy. Cytom Part A 79: 306-310. doi: 10.1002/cyto.a.21034.
23. Ionescu D, Siebert C, Polerecky L, Munwes YY, Lott C, et al. (2012) Microbial and chemical characterization of underwater fresh water springs in the Dead Sea. PLoS One 7: e38319. doi: 10.1371/journal.pone.0038319.
24. Muyzer G, Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59: 695-700.
25. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4: 1-9.
26. Lane D (1991) 16S/23S rRNA sequencing. Nucleic acid techniques in bacterial systematics. John Wiley and Sons, New York, NY. pp.115-175.
27. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, et al. (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41: D590-6. doi: 10.1093/nar/gks1219.
28. Üveges V, Tapolczai K, Krienitz L, Padisák J (2012) Photosynthetic characteristics and physiological plasticity of an Aphanizomenon flos-aquae (Cyanobacteria, Nostocaceae) winter bloom in a deep oligomesotrophic lake (Lake Stechlin, Germany). Hydrobiologia 698: 263-272. doi: 10.1007/s10750-012-1103-3.
29. Cole JJ, Findlay S, Pace ML (1988) Bacterial production in fresh and saltwater ecosystems: a cross-system overview. Mar Ecol Prog Ser 43: 1-10.
30. Keto J, Tallberg P (2000) The recovery of Vesijarvi, a lake in southern Finland: water quality and phytoplankton interpretations. Boreal Environ Res 5: 15-26.
31. Kling G, Kipphut G, Miller M (1992) The flux of CO2 and CH4 from lakes and rivers in arctic Alaska. Hydrobiologia 240: 23-36.
32. Kankaala P, Huotari J, Tulonen T, Ojala A (2013) Lake-size dependent physical forcing of carbon dioxide and methane effluxes from lakes in a boreal landscape. Limnol Oceanogr 58: 1915-1930. doi: 10.4319/lo.2013.58.6.1915.
33. Karlsson J, Giesler R, Persson J, Lundin E (2013) High emission of carbon dioxide and methane during ice thaw in high latitude lakes. Geophys Res Lett 40: 1123-1127. doi: 10.1002/grl.50152.
34. Teeling H, Fuchs BM, Becher D, Klockow C, Gardebrecht A, et al. (2012) Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 336: 608-611. doi: 10.1126/science.1218344.
35. Kirchman DL (2002) The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiol Ecol 39: 91-100. doi: 10.1111/j.1574-6941.2002.tb00910.x.
36. Van Trappen S, Vandecandelaere I, Mergaert J, Swings J (2005) Flavobacterium fryxellicola sp. nov. and Flavobacterium psychrolimnae sp. nov., novel psychrophilic bacteria isolated from microbial mats in Antarctic lakes. Int J Syst Evol Microbiol 55: 769-772. doi: 10.1099/ijs.0.03056-0.
37. Tamaki H (2003) Flavobacterium limicola sp. nov., a psychrophilic, organic-polymer-degrading bacterium isolated from freshwater sediments. Int J Syst Evol Microbiol 53: 519-526. doi: 10.1099/ ijs.0.02369-0.
38. Zhu F, Wang S, Zhou P (2003) Flavobacterium xinjiangense sp. nov. and Flavobacterium omnivorum sp. nov., novel psychrophiles from the China No. 1 glacier. Int J Syst Evol Microbiol 53: 853-857. doi: 10.1099/ijs.0.02310-0.
39. Humphry DR, George A, Black GW, Cummings SP (2001) Flavobacterium frigidarium sp. nov., an aerobic, psychrophilic, xylanolytic and laminarinolytic bacterium from Antarctica. Int J Syst Evol Microbiol 51: 1235-1243.
40. Cole JJ, Caraco NF, Kling G, Kratz T (1994) Carbon dioxide supersaturation in the surface waters of lakes. Science (80-) 265: 1568-1570.
41. Cole JJ, Prairie YT, Caraco NF, McDowell WH, Tranvik LJ, et al. (2007) Plumbing the Global Carbon Cycle: Integrating Inland Waters into the Terrestrial Carbon Budget. Ecosystems 10: 172-185. doi: 10.1007/s10021-006-9013-8.
42. Straškrábová V, Izmest'yeva LR, Maksimova EA, Fietz S, Nedoma J, et al. (2005) Primary production and microbial activity in the euphotic zone of Lake Baikal (Southern Basin) during late winter. Glob Planet Change 46: 57-73. doi: 10.1016/j.gloplacha.2004.11.006.
43. Levasseur M (2013) Impact of Arctic meltdown on the microbial cycling of sulphur. Nat Geosci 6: 691-700. doi: 10.1038/ngeo1910.