Maximum in the Middle: Nonlinear Response of Microbial Plankton to Ultraviolet Radiation and Phosphorus

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Medina Sánchez, Juan Manuel ^a   Delgado Molina, José Antonio ^a   Bratbak, Gunnar ^b   Bullejos, Francisco José ^a   Villar Argaiz, Manuel ^a   Carrillo, Presentación ^c  

^a UNIVERSITY OF GRANADA   (Spain)

^b UNIVERSITY OF BERGEN   (Norway)

^c UNIVERSITY OF GRANADA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATE; PHOSPHORUS;

ABIOTIC STRESS; ARTICLE; AUTOTROPHY; BIODIVERSITY; COMPETITION; CONTROLLED STUDY; DEPLETION; DYNAMICS; ECOSYSTEM RESILIENCE; ENVIRONMENTAL ENRICHMENT; FACTORIAL DESIGN; FOOD WEB; GLOBAL CHANGE; HETEROTROPHIC MICROBIAL FOOD WEB; MESOCOSM; MICROBIAL COMMUNITY; MICROBIAL PLANKTON; NONHUMAN; NONLINEAR SYSTEM; PARASITISM; PLANKTON; PREDATION; ULTRAVIOLET RADIATION;

BACTERIA; BIODIVERSITY; BIOMASS; ECOSYSTEM; FOOD CHAIN; LAKES; PHOSPHORUS; PLANKTON; SPAIN; ULTRAVIOLET RAYS;

CILIOPHORA;

EID: 84875930820     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0060223     Document Type: Article

References (71)

1. Williamson CE, Saros JE, Schindler DW, (2009) Sentinels of change. Science 323: 887-888.
2. Catalan J, Camarero L, Felip M, Pla S, Ventura M, et al. (2006) High mountain lakes: extreme habitats and witnesses of environmental changes. Limnetica 25: 551-584.
3. Parker BR, Vinebrooke RD, Schindler DW, (2008) Recent climate extremes alter alpine lake ecosystems. Proc Natl Acad Sci U S A 105: 12927-12931.
4. Morales-Baquero R, Pulido-Villena E, Reche I, (2006) Atmospheric inputs of phosphorus and nitrogen to the southwest Mediterranean region: biogeochemical response of high mountain lakes. Limnol Oceanogr 51: 830-837.
5. Reche I, Ortega-Retuerta E, Romera O, Pulido-Villena E, Morales-Baquero R, et al. (2009) Effect of Saharan dust inputs on bacterial activity and community composition in Mediterranean lakes and reservoirs. Limnol Oceanogr 54: 869-879.
6. Nelson CE, Carlson CA, (2011) Differential response of high-elevation planktonic bacterial community structure and metabolism to experimental nutrient enrichment. PLoS One 6: e18320.
7. Häder DP, Kumar HD, Smith RC, Worrest RC, (2007) Effects of solar UV radiation on aquatic ecosystems and interactions with climate change. Photochem Photobiol Sci 6: 267-285.
8. Keil M, Jackson DR, Hort MC, (2007) The January 2006 low ozone event over the UK 2006. Atmos Chem Phys 7: 961-972.
9. McKenzie RL, Aucamp PJ, Bais AF, Bjorn LO, Ilyas M, et al. (2011) Ozone depletion and climate change: impacts on UV radiation. Photochem Photobiol Sci 10: 182-198.
10. Häder DP, Helbling EW, Williamson CE, Worrest RC, (2011) Effects of UV radiation on aquatic ecosystems and interactions with climate change. Photochem Photobiol Sci 10: 242-260.
11. Escudero M, Castillo S, Querol X, Avila A, Alarcón M, et al. (2005) Wet and dry African dust episodes over eastern Spain. J Geophys Res 110: D18S08.
12. Bullejos FJ, Carrillo P, Villar-Argaiz M, Medina-Sánchez JM, (2010) Roles of phosphorus and ultraviolet radiation in the strength of phytoplankton-zooplankton coupling in a Mediterranean high mountain lake. Limnol Oceanogr 55: 2549-2562.
13. Mladenov N, Sommaruga R, Morales-Baquero R, Laurion I, Camarero L, et al. (2011) Dust inputs and bacteria influence dissolved organic matter in clear alpine lakes. Nat Commun 2: 405.
14. Delgado-Molina JA, Carrillo P, Medina-Sánchez JM, Villar-Argaiz M, Bullejos FJ, (2009) Interactive effects of phosphorus loads and ambient ultraviolet radiation on the algal community in a high-mountain lake. J Plankton Res 31: 619-634.
15. Medina-Sánchez JM, Villar-Argaiz M, Carrillo P, (2004) Neither with nor without you: a complex algal control on bacterioplankton in a high mountain lake. Limnol Oceanogr 49: 1722-1733.
16. Straškrabová V, Bertoni R, Blazo M, Callieri C, Forsstrom L, et al. (2009). Structure of pelagic microbial assemblages in European mountain lakes during ice-free season. In: Catalan J, Curtis CJ, Kernan M, editors. Patterns and factors of biota distribution in remote European mountain lakes. Stuttgart: Schweizerbart Science Publishers. 19-53.
17. Zubkov MV, Tarran GA, (2008) High bacterivory by the smallest phytoplankton in the North Atlantic Ocean. Nature 455: 224-226.
18. Kirchman DL, Malmstrom RR, Cottrell MT, (2005) Control of bacterial growth by temperature and organic matter in the Western Arctic. Deep Sea Res Part 2 Top Stud Oceanogr 52: 3386-3395.
19. Hall EK, Cotner JB, (2007) Interactive effect of temperature and resources on carbon cycling by freshwater bacterioplankton communities. Aquat Microb Ecol 49: 35-45.
20. Weisse T, Stadler P, Lindström ES, Kimmance SA, Montagnes DJS, (2002) Interactive effect of temperature and food concentration on growth rate: a test case using the small freshwater ciliate Urotricha farcta. Limnol Oceanogr 47: 1447-1455.
21. Bergeron M, Vincent WF, (1997) Microbial food web responses to phosphorus supply and solar UV radiation in a subarctic lake. Aquat Microb Ecol 12: 239-249.
22. Rae R, Vincent WF, (1998) Effects of temperature and ultraviolet radiation on microbial food web structure: potential responses to global change. Freshw Biol 40: 747-758.
23. Bouvy M, Bettarel Y, Bouvier C, Domaizon I, Jacquet S, et al. (2011) Trophic interactions between viruses, bacteria and nanoflagellates under various nutrient conditions and simulated climate change. Environ Microbiol 13: 1842-1857.
24. Biddanda B, Ogdahl M, Cotner J, (2001) Dominance of bacterial metabolism in oligotrophic relative to eutrophic waters. Limnol Oceanogr 46: 730-739.
25. Caston CB, Nowlin WH, Gaulke A, Vanni MJ, (2009) The relative importance of heterotrophic bacteria to pelagic ecosystem dynamics varies with reservoir trophic state. Limnol Oceanogr 54: 2143-2156.
26. Miki T, Jacquet S, (2008) Complex interactions in the microbial world: underexplored key links between viruses, bacteria and protozoan grazers in aquatic environments. Aquat Microb Ecol 51: 195-208.
27. Carrillo P, Delgado-Molina JA, Medina-Sánchez JM, Bullejos FJ, Villar-Argaiz M, (2008) Phosphorus inputs unmask negative effects of ultraviolet radiation on algae in a high mountain lake. Glob Change Biol 14: 423-439.
28. Medina-Sánchez JM, Villar-Argaiz M, Carrillo P, (2006) Solar radiation-nutrient interaction enhances the resource and predation algal control on bacterioplankton: a short-term experimental study. Limnol Oceanogr 51: 913-924.
29. Intergovernmental Panel on Climate Change (2007) Climate change 2007: The physical science basis. New York: Cambridge University Press. 996 p.
30. Mostajir B, Demers S, de Mora S, Belzile C, Chanut JP, et al. (1999) Experimental test of the effect of ultraviolet-B radiation in a planktonic community. Limnol Oceanogr 44: 586-596.
31. Ferreyra GA, Mostajir B, Schloss IR, Chatila K, Ferrario ME, et al. (2006) Ultraviolet-B radiation effects on the structure and function of lower trophic levels of the marine planktonic food web. Photochem Photobiol 82: 887-897.
32. Crain CM, Kroeker K, Halpern BS, (2008) Interactive and cumulative effects of multiple human stressors in marine systems. Ecol Lett 11: 1304-1315.
33. Villar-Argaiz M, Medina-Sánchez JM, Carrillo P, (2001) Inter- and intra-annual variability in the phytoplankton community of a high mountain lake: the influence of external (atmospheric) and internal (recycled) sources of P. Freshw Biol. 46: 1017-1034.
34. American Public Health Association (1992) Standard methods for the examination of water and wastewater, 18th edn. Washington: American Public Health Association. 70 p.
35. Medina-Sánchez JM, Villar-Argaiz M, Carrillo P, (2002) Modulation of the bacterial response to spectral solar radiation by algae and limiting nutrients. Freshw Biol 47: 2191-2204.
36. Villar-Argaiz M, Medina-Sánchez JM, Carrillo P, (2002) Microbial plankton response to contrasting climatic conditions: insights from community structure, productivity and fraction stoichiometry. Aquat Microb Ecol 29: 253-266.
37. Straškrabová V, Callieri C, Carrillo P, Cruz-Pizarro L, Fott J, et al. (1999) Investigations on pelagic food webs in mountain lakes- aims and methods. J Limnol 58: 77-87.
38. Medina-Sánchez JM, Villar-Argaiz M, Sánchez-Castillo P, Cruz-Pizarro L, Carrillo P, (1999) Structure changes in a planktonic food web: biotic and abiotic controls. J Limnol 58: 213-222.
39. Bratbak G, Heldal M, Norland S, Thingstad TF, (1990) Viruses as partners in spring bloom microbial trophodynamics. Appl Environ Microbiol 56: 100-105.
40. Bratbak G, Heldal M, Thingstad TF, Riemann B, Haslund OH, (1992) Incorporation of viruses into the budget of microbial C-transfer- a 1st approach. Mar Ecol Prog Ser 83: 273-280.
41. Smith DC, Azam F, (1992) A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine. Mar Microb Food Webs 6: 107-114.
42. Carrillo P, Medina-Sánchez JM, Villar-Argaiz M, (2002) The interaction of phytoplankton and bacteria in a high mountain lake: importance of the spectral composition of solar radiation. Limnol Oceanogr 47: 1294-1306.
43. Quinn G, Keough M (2002) Experimental design and data analysis for biologists. Cambridge: Cambridge University Press. 537 p.
44. Urabe J, Kyle M, Makino W, Yoshida T, Andersen T, et al. (2002) Reduced light increases herbivore production due to stoichiometric effects of light/nutrient balance. Ecology 83: 619-627.
45. Motulsky HJ, Christopoulos A (2003) Fitting models to biological data using linear and nonlinear regression. A practical guide to curve fitting. San Diego CA: GraphPad Software Inc. 351 p.
46. Hurlbert SH, (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54: 187-211.
47. Vadstein O, Stibor H, Lippert B, Løseth K, Roederer W, et al. (2004) Moderate increase in the biomass of omnivorous copepods may ease grazing control of planktonic algae. Mar Ecol Prog Ser. 270: 199-207.
48. Duarte CM, Agustí S, Vaqué D, Agawin NSR, Felipe J, et al. (2005) Experimental test of bacteria-phytoplankton coupling in the Southern Ocean. Limnol Oceanogr 50: 1844-1854.
49. Thingstad TF, Bellerby RGJ, Bratbak G, Børsheim KY, Egge JK, et al. (2008) Counterintuitive carbon-to-nutrient coupling in an Arctic pelagic ecosystem. Nature 455: 387-390.
50. Boersma M, Elser JJ, (2006) Too much of a good thing: on stoichiometrically balanced diets and maximal growth. Ecology 87: 1325-1330.
51. Connell JH, (1978) Diversity in tropical rain forest and coral reefs. Science 199: 1302-1310.
52. Kaunzinger CMK, Morin PJ, (1998) Productivity controls food chain properties in microbial communities. Nature 395: 495-497.
53. De Castro F, Gaedke U, Boenigk J, (2009) Reverse evolution: driving forces behind the loss of acquired photosynthetic traits. PLoS One 4: e8465.
54. Tadonléké RD, Planas D, Lucotte A, (2005) Microbial food webs in boreal humic lakes and reservoirs: Ciliates as a major factor related to the dynamics of the most active bacteria. Microb Ecol 49: 325-341.
55. Carrillo P, Villar-Argaiz M, Medina-Sánchez JM, (2008) Does microorganism stoichiometry predict microbial food web interactions after a phosphorus pulse? Microb Ecol 56: 350-363.
56. Pedrós-Alió C, Calderon-Paz JI, Gasol JM, (2000) Comparative analysis shows that bacterivory, not viral lysis, controls the abundance of heterotrophic prokaryotic plankton. FEMS Microbiol Ecol 32: 157-165.
57. Wommack KE, Colwell RR, (2000) Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Biol Rev. 64: 69-114.
58. Medina-Sánchez JM, Carrillo P, Delgado-Molina JA, Bullejos FJ, Villar-Argaiz M, (2010) Patterns of resource limitation of bacteria along a trophic gradient in Mediterranean inland waters. FEMS Microbiol Ecol 74: 554-565.
59. Sinha RP, Häder DP, (2002) UV-induced DNA damage and repair: a review. Photochem Photobiol Sci 1: 225-236.
60. Sommaruga R, Sattler B, Oberleiter A, Wille A, Wograth-Sommaruga S, et al. (1999) An in situ enclosure experiment to test the solar UVB impact on plankton in a high altitude mountain lake. II. Effects on the microbial food web. J Plankton Res 21: 859-876.
61. Modenutti BE, Balseiro EG, Callieri C, Bertoni R, Queimalinos CP, (2005) Effect of UV-B and different PAR intensities on the primary production of the mixotrophic planktonic ciliate Stentor araucanus. Limnol Oceanogr 50: 864-871.
62. Helton RR, Cottrell MT, Kirchman DL, Wommack KE, (2005) Evaluation of incubation-based methods for estimating virioplankton production in estuaries. Aquat Microb Ecol 41: 209-219.
63. Hofer JS, Sommaruga R, (2001) Seasonal dynamics of viruses in an alpine lake: importance of filamentous forms. Aquat Microb Ecol 26: 1-11.
64. Säwström C, Lisle J, Anesio AM, Priscu JC, Laybourn-Parry J, (2008) Bacteriophage in polar inland waters. Extremophiles 12: 167-175.
65. Paterson H, Laybourn-Parry J, (2012) Antarctic sea ice viral dynamics over an annual cycle. Polar Biol 35: 491-497.
66. Säwström C, Pearce I, Davidson AT, Rosén P, Laybourn-Parry J, (2008) Influence of environmental conditions, bacterial activity and viability on the viral component in 10 Antarctic lakes. FEMS Microbiol Ecol 63: 12-22.
67. Paul JH, (2008) Prophages in marine bacteria: dangerous molecular time bombs or the key to survival in the seas? ISME J 2: 579-589.
68. Maranger R, Del Giorgio PA, Bird DF, (2002) Accumulation of damaged bacteria and viruses in lake water exposed to solar radiation. Aquat Microb Ecol 28: 213-227.
69. Woodward G, Perkins DM, Brown LE, (2010) Climate change and freshwater ecosystems: impacts across multiple levels of organization. Philos T R Soc B 365: 2093-2106.
70. Cotner JB, Biddanda BA, (2002) Small players, large role: Microbial influence on biogeochemical processes in pelagic aquatic ecosystems. Ecosystems 5: 105-121.
71. Thomas WH, Cho BC, Azam F, (1991) Phytoplankton and bacterial production and biomass in sub-alpine Eastern Brook Lake, Sierra-Nevada, California. I. Seasonal interrelationships between the two biotic groups. Arct Alp Res 23: 287-295.