Mixotrophic haptophytes are key bacterial grazers in oligotrophic coastal waters

ISME Journal

Volumn 8, Issue 1, 2014, Pages 164-176

  Unrein, Fernando ^a,b   Gasol, Josep M ^a   Not, Fabrice ^a,c   Forn, Irene ^a   Massana, Ramon ^a  

^a INSTITUT DE CIÈNCIES DEL MAR   (Spain)

^b INSTITUTO DE INVESTIGACIONES BIOTECNOLÓGICAS   (Argentina)

^c STATION BIOLOGIQUE DE ROSCOFF   (France)

Author keywords

cryptophytes; haptophytes; mixotrophic; oligotrophic coastal seawater

Indexed keywords

SEA WATER;

BACTERIUM; BACTERIVORY; COASTAL WATER; DINOFLAGELLATE; INTERSPECIFIC INTERACTION; MARINE ECOSYSTEM; MIXOTROPHY; PICOPLANKTON; QUANTITATIVE ANALYSIS;

ARTICLE; BACTERIAL PHENOMENA AND FUNCTIONS; BIODIVERSITY; ECOSYSTEM; FLUORESCENCE IN SITU HYBRIDIZATION; HAPTOPHYTA; METABOLISM; MICROBIOLOGY; SEA;

BACTERIAL PHYSIOLOGICAL PHENOMENA; BIODIVERSITY; ECOSYSTEM; HAPTOPHYTA; IN SITU HYBRIDIZATION, FLUORESCENCE; OCEANS AND SEAS; SEAWATER; WATER MICROBIOLOGY;

ALGAE; BACTERIA (MICROORGANISMS); CHLOROPHYTA; CRYPTOPHYTA; DINOPHYCEAE; HAPTOPHYCEAE; MASTIGOPHORA (FLAGELLATES); PHYTOMASTIGOPHOREA;

EID: 84891163637     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2013.132     Document Type: Article

References (72)

1. Alonso-Sáez L, Vázquez-Domínguez E, Cardelús C, Pinhassi J, Sala MM, Lekunberri I et al. (2008). Factors controlling the year-round variability in carbon flux through bacteria in a coastal marine system. Ecosystems 11: 397-409.
2. Bell EM, Laybourn-Parry J. (2003). Mixotrophy in the antarctic phytoflagellate, Pyramimonas gelidicola (Chlorophyta: Prasinophyceae). J Phycol 39: 644-649. (Pubitemid 36990704)
3. Bielewicz S, Bell E, Kong W, Friedberg I, Priscu JC, Morgan-Kiss RM. (2011). Protist diversity in a permanently ice-covered Antarctic Lake during the polar night transition. ISME J 5: 1559-1564.
4. Bird DF, Kalff J. (1986). Bacterial grazing by planktonic lake algae. Science 231: 493-495.
5. Caron DA. (2001). Protistan herbivory and bacterivory. In: Paul J (ed.) Marine Microbiology, Vol. 30, Methods in Microbiology. Academic Press: London, pp 289-315. (Pubitemid 33805850)
6. Chan Y-F, Tsai A-Y, Chiang K-P, Hsieh C-H. (2009). Pigmented nanoflagellates grazing on Synechococcus: seasonal variations and effect of flagellate size in the coastal ecosystem of Subtropical Western Pacific. Microbial Ecol 58: 548-557.
7. Cuvelier ML, Allen AE, Monier A, McCrow JP, Messié M, Tringe SG et al. (2010). Targeted metagenomics and ecology of globally important uncultured eukaryotic phytoplankton. Proc Natl Acad Sci USA 107: 14679-14684.
8. Estep KW, Davis PG, Keller MD, Sieburth JM. (1986). How important are oceanic algal nanoflagellates in bacterivory Limnol Oceanogr 31: 646-650.
9. Floder S, Hansen T, Ptacnik R. (2006). Energy-dependent bacterivory in Ochromonas minima-A strategy promoting the use of substitutable resources and survival at insufficient light supply. Protist 157: 291-302. (Pubitemid 44224238)
10. Foulon E, Not F, Jalabert F, Cariou T, Massana R, Simon N. (2008). Ecological niche partitioning in the picoplanktonic green alga Micromonas pusilla: evidence from environmental surveys using phylogenetic probes. Environmental Microbiol 10: 2433-2443.
11. Frias-Lopez J, Thompson A, Waldbauer J, Chisholm SW. (2009). Use of stable isotope-labelled cells to identify active grazers of picocyanobacteria in ocean surface waters. Environmental Microbiol 11: 512-525.
12. Fuller NJ, Tarran GA, Cummings DG, Woodward EMS, Orcutt KM, Yallop M et al. (2006). Molecular analysis of photosynthetic picoeukaryote community structure along an Arabian Sea transect. Limnol Oceanogr 51: 2502-2514. (Pubitemid 44902139)
13. Gasol JM, del Giorgio PA. (2000). Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities. Scientia Marina 64: 197-224. (Pubitemid 30615216)
14. Gasol JM, Pinhassi J, Alonso-Sáez L, Ducklow H, Herndl GJ, Koblízek M et al. (2008). Towards a better understanding of microbial carbon flux in the sea. Aquat Microbial Ecol 53: 21-38.
15. Gonzalez JM, Sherr BF, Sherr E. (1993). Digestive enzyme activity as a quantitative measure of protistan grazing: The acid lysozyme assay for bacterivory. Mar Ecol Prog Ser 100: 197-206. (Pubitemid 24416144)
16. Gutiérrez-Rodríguez A, Latasa M, Scharek R, Massana R, Vila G, Gasol JM. (2011). Growth and grazing rate dynamics of major phytoplankton groups in an oligotrophic coastal site. Estuarine Coastal Shelf Sci 95: 77-87.
17. Hartmann M, Grob C, Tarran GA, Martin AP, Burkill PH, Scanlan DJ et al. (2012). Mixotrophic basis of Atlantic oligotrophic ecosystems. Proc Natl Acad Sci USA 109: 5756-5760.
18. Havskum H, Riemann B. (1996). Ecological importance of bacterivorous, pigmented flagellates (mixotrophs) in the Bay of Aarhus, Denmark. Mar Ecol Prog Ser 137: 251-263.
19. Hitchman RB, Jones HL. (2000). The role of mixotrophic protists in the population dynamics of the microbial food web in a small artificial pond. Freshwater Biol 43: 231-241. (Pubitemid 30079134)
20. Jardillier L, Zubkov MV, Pearman J, Scanlan DJ. (2010). Significant CO2 fixation by small prymnesiophytes in the subtropical and tropical northeast Atlantic Ocean. ISME J 4: 1180-1192.
21. Kong W, Ream DC, Priscu JC, Morgan-Kiss RM. (2012). Diversity and expression of RubisCO genes in a perennially ice-covered Antarctic lake during the polar night transition. Apply Environ Microbiol 78: 4358-4366.
22. Laybourn-Parry J, Marshall WA, Marchant HJ. (2005). Flagellate nutritional versatility as a key to survival in Antarctic phytoflagellates in two contrasting saline lakes. Freshwater Biol 50: 830-838. (Pubitemid 40600375)
23. Legrand C, Johansson N, Johnsen G, Borsheim KY, Grané li E. (2001). Phagotrophy and toxicity variation in the mixotrophic Prymnesium patelliferum (Haptophyceae). Limnol Oceanogr 46: 1208-1214. (Pubitemid 32665198)
24. Liu H, Probert I, Uitz J, Claustre H, Aris-Brosou S, Frada M et al. (2009). Extreme diversity in noncalcifying haptophytes explains a major pigment paradox in open oceans. Proc Natl Acad Sci 106: 12803-12808.
25. Logares R, Audic S, Santini S, Pernice MC, de Vargas C, Massana R. (2012). Diversity patterns and activity of uncultured marine heterotrophic flagellates unveiled with pyrosequencing. ISME J 6: 1823-1833.
26. MacIsaac EA, Stoeckner JG. (1993). Enumeration of phototrophic picoplankton by autofluorescence microscopy. In: Kemp PF, Sherr BF, Sherr EB, Cole JJ (eds.) Handbook of methods in Aquatic Microbial Ecology, Vol 30. Lewis Publishers: Boca Raton, Florida, USA, pp 187-197.
27. Marshall WA, Laybourn-Parry J. (2002). The balance between photosynthesis and grazing in Antarctic mixotrophic cryptophytes during summer. Freshwater Biol 47: 2060-2070. (Pubitemid 35255392)
28. Maruyama S, Kim E. (2013). A modern descendant of early green algal phagotrophs. Curr Biol 23: 1081-1084.
29. Massana R, Terrado R, Forn I, Lovejoy C, Pedrós Alió C. (2006). Distribution and abundance of uncultured heterotrophic flagellates in the world oceans. Environ Microbiol 8: 1515-1522. (Pubitemid 44167978)
30. Massana R, Unrein F, Rodríguez-Martínez R, Forn I, Lefort T, Pinhassi J et al. (2009). Grazing rates and functional diversity of uncultured heterotrophic flagellates. ISME J 3: 588-596.
31. McDonald SM, Sarno D, Scanlan DJ, Zingone A. (2007). Genetic diversity of eukaryotic ultraphytoplankton in the Gulf of Naples during an annual cycle. Aquat Microbial Ecol 50: 75-89. (Pubitemid 351154593)
32. Medina Sánchez JM, Felip M, Casamayor EO. (2005). Catalyzed reported deposition-fluorescence in situ hybridization protocol to evaluate phagotrophy in mixotrophic protists. Appl Environ Microbiol 71: 7321-7326. (Pubitemid 43194227)
33. Menden-Deuer S, Lessard EJ. (2000). Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol Oceanogr 45: 569-579. (Pubitemid 30247467)
34. Norland S. (1993). The relationship between biomass and volume of bacteria. In: Lewis (eds). Handbook of Methods in Aquatic Microbial Ecology. Lewis Publishers: Boca Raton, pp 303-307.
35. Not F, Latasa M, Marie D, Cariou T, Vaulot D, Simon N. (2004). A single species, Micromonas pusilla (Prasinophyceae), dominates the eukaryotic picoplankton in the western English Channel. Appl Environ Microbiol 70: 4064-4072. (Pubitemid 38969749)
36. Not F, Simon N, Biegala IC, Vaulot D. (2002). Application of fluorescent in situ hybridization coupled with tyramide signal amplification (FISH-TSA) to assess eukaryotic picoplankton composition. Aquat Microbial Ecol 28: 157-166. (Pubitemid 34780560)
37. Not F, Zapata M, Pazos Y, Campan a E, Doval M, Rodríguez F. (2007). Size-fractionated phytoplankton diversity in the NW Iberian coast: a combination of microscopic, pigment and molecular analyses. Aquat Microbial Ecol 49: 255-265. (Pubitemid 351525776)
38. Novarino G. (2005). Nanoplankton protists from the western Mediterranean Sea. II. Cryptomonads (Cryptophyceae Cryptomonadea). Scientia Marina 69: 47-74. (Pubitemid 40473095)
39. Nygaard K, Tobiesen A. (1993). Bacterivory in algae: a survival strategy during nutrient limitation. Limnol Oceanogr 38: 273-279. (Pubitemid 24429402)
40. Pernthaler J, Glockner F-O, Schonhuber W, Amann R. (2001). Fluorescence in situ hybridization (FISH) with rRNA-targeted oligonucleotide probes. Methods Microbiol 30: 207-226. (Pubitemid 33287422)
41. Piwosz K, Wiktor JM, Niemi A, Tatarek A, Michel C. (2013). Mesoscale distribution and functional diversity of picoeukaryotes in the first-year sea ice of the Canadian Arctic. ISME J 7: 1461-1471.
42. Porter KG, Feig YS. (1980). The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25: 943-948.
43. Puigserver M, Chrétiennot-Dinet M-J, Nezan E. (2003). Some Prymnesiaceae (Haptophyta, Prymnesiophyceae) from the Mediterranean Sea, with the description of two new species: Chrysochromulina lanceolata sp. nov. and C. pseudolanceolata sp. nov. J Phycol 39: 762-774. (Pubitemid 37002302)
44. Palsson C, Grané li W. (2003). Diurnal and seasonal variations in grazing by bacterivorous mixotrophs in an oligotrophic clearwater lake. Archiv fur Hydrobiologie 157: 289-307. (Pubitemid 36832427)
45. Raven JA. (1997). Phagotrophy in phototrophs. Limnol Oceanogr 42: 198-205.
46. Rice JA. (1988). Mathematical statistics and data analysis. The Wadsworth & Brooks/Cole Statistics/Probability Series. Wadsworth & Brooks: Pacific Grove, CA, USA.
47. Roberts EC, Laybourn-Parry J. (2001). Mixotrophic cryptophytes and their predators in the Dry Valley lakes of Antarctica. Freshwater Biol 41: 737-746. (Pubitemid 29373253)
48. Rothhaupt KO. (1996). Laboratorary experiments with a mixotrophic chrysophyte and obligately phagotrophic and photographic competitors. Ecology 77: 716-724. (Pubitemid 126494902)
49. Sanders RW. (1991). Mixotrophic protists in marine and freshwater ecosystems. J Protozool 38: 76-81.
50. Sanders RW, Porter KG, Bennett SJ, DeBiase AE. (1989). Seasonal patterns of bacterivory by flagellates, ciliates, rotifers, and cladocerans in a freshwater planktonic community. Limnol Oceanogr 34: 673-687.
51. Schauer M, Balagué V, Pedrós Alió C, Massana R. (2003). Seasonal changes in the taxonomic composition of bacterioplankton in a coastal oligotrophic system. Aquat Microbial Ecol 31: 163-174. (Pubitemid 36391591)
52. Sherr BF, Sherr EB, Fallon RD. (1987). Use of monodispersed fluorescently labeled bacteria to estimate in situ protozoan bacterivory. Appl Environ Microbiol 53: 958-965.
53. Sherr BF, Sherr EB, Pedrós-Alió C. (1989). Simultaneous measurement of bacterioplankton production and protozoan bacterivory in estuary waters. Mar Ecol Prog Ser 54: 209-219.
54. Shi XL, Lepère C, Scanlan DJ, Vaulot D. (2011). Plastid 16S rRNA gene diversity among eukaryotic picophytoplankton sorted by flow cytometry from the South Pacific Ocean. PLoS One 6: e18979.
55. Simon M, Azam F. (1989). Protein content and protein synthesis rates of planktonic marine bacteria. Mar Ecol Prog Ser 51: 201-213.
56. Simon N, Campbell L, O rnó lfsdottir E, Groben R, Guillou L, Lange M et al. (2000). Oligonucleotide probes for the identification of three algal groups by dot blot and fluorescent whole-cell hybridization. J Eukaryotic Microbiol 47: 76-84. (Pubitemid 30063295)
57. Stibor H, Sommer U. (2003). Mixotrophy of a photosynthetic flagellate viewed from an optimal foraging perspective. Protist 154: 91-98. (Pubitemid 36684413)
58. Stoecker DK. (1999). Mixotrophy among Dinoflagellates. J Eukaryotic Microbiol 46: 397-401.
59. Sun J, Liu D. (2003). Geometric models for calculating cell biovolume and surface area for phytoplankton. J Plankton Res 25: 1331-1346. (Pubitemid 37417807)
60. Thurman J, Parry J, Hill PJ, Priscu JC, Vick TJ, Chiuchiolo A et al. (2012). Microbial dynamics and flagellate grazing during transition to winter in Lakes Hoare and Bonney, Antarctica. FEMS Microbiol Ecol 82: 449-458.
61. Tranvik LJ, Porter KG, Sieburth JM. (1989). Occurrence of bacterivory in Cryptomonas, a common freshwater phytoplankter. Oecologia 78: 473-476. (Pubitemid 20425935)
62. Treusch AH, Demir-Hilton E, Vergin KL, Worden AZ, Carlson CA, Donatz MG et al. (2012). Phytoplankton distribution patterns in the northwestern Sargasso Sea revealed by small subunit rRNA genes from plastids. ISME J 6: 481-492.
63. Tsai AY, Gong GC, Sanders RW, Chen WH, Chao CF, Chiang KP. (2011). Importance of bacterivory by pigmented and heterotrophic nanoflagellates during the warm season in a subtropical western Pacific coastal ecosystem. Aquat Microbial Ecol 63: 9-18.
64. Unrein F, Gasol JM, Massana R. (2010). Dinobryon faculiferum (Chrysophyta) in coastal Mediterranean seawater: presence and grazing impact on bacteria. J Plankton Res 32: 559-564.
65. Unrein F, Massana R, Alonso-Sáez L, Gasol JM. (2007). Significant year-round effect of small mixotrophic flagellates on bacterioplankton in an oligotrophic coastal system. Limnol Oceanogr 52: 456-469. (Pubitemid 46972154)
66. Urabe J, Gurung TB, Yoshida T, Sekino T, Nakanishi M, Maruo M et al. (2000). Diel changes in phagotrophy by Cryptomonas in Lake Biwa. Limnol Oceanogr 45: 1558-1563.
67. Vila M, Masó M. (2005). Phytoplankton functional groups and harmful algal species in anthropogenically impacted waters of the NW Mediterranean Sea. Scientia Marina 69: 31-45. (Pubitemid 40473094)
68. Vázquez-Domínguez E, Vaqué D, Gasol JM. (2007). Ocean warming enhances respiration and carbon demand of coastal microbial plankton. Global Change Biol 13: 1327-1334. (Pubitemid 47082271)
69. Worden AZ, Janouskovec J, McRose D, Engman A, Welsh RM, Malfatti S et al. (2012). Global distribution of a wild alga revealed by targeted metagenomics Curr Biol 22: 675-677.
70. Zingone A, Chrétiennot-Dinet M-J, Lange M, Medlin L. (1999). Morphological and genetic characterization of Phaeocystis cordata and P. jahnii (Prymnesiophyceae), two new species from the Mediterranean Sea. J Phycol 35: 1322-1337. (Pubitemid 30059338)
71. Zubkov MV, Tarran GA. (2008). High bacterivory by the smallest phytoplankton in the North Atlantic Ocean. Nature 455: 224-226.
72. Zubkov MV, Zollner E, Jurgens K. (2001). Digestion of bacterial macromolecules by a mixotrophic flagellate, Ochromonas sp., compared with that by two heterotrophic flagellates, Spumella pudica and Bodo saltans. Eur J Protistol 37: 155-166. (Pubitemid 32828041)