A co-culturing/metabolomics approach to investigate chemically mediated interactions of planktonic organisms reveals influence of bacteria on diatom metabolism

Metabolomics

Volumn 9, Issue 2, 2013, Pages 349-359

  Paul, Carsten ^a   Mausz, Michaela A ^a   Pohnert, Georg ^a  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

Co culture; Diatom; Metabolomics; Plankton interactions; Thalassiosira pseudonana

Indexed keywords

AMINO ACID;

ADAPTATION; ALGAL GROWTH; ARTICLE; BACTERIAL GROWTH; BACTERIUM; CELL LEVEL; COCULTURE; CONTROLLED STUDY; DINOROSEOBACTER SHIBAE; LABORATORY DEVICE; MASS FRAGMENTOGRAPHY; METABOLOMICS; MICROALGA; NONHUMAN; ORGANISMAL INTERACTION; PLANKTON; SIGNAL DETECTION; THALASSIOSIRA PSEUDONANA; UPREGULATION;

ALGAE; BACILLARIOPHYTA; BACTERIA (MICROORGANISMS); DINOROSEOBACTER SHIBAE; THALASSIOSIRA PSEUDONANA;

EID: 84875504338     PISSN: 15733882     EISSN: 15733890     Source Type: Journal    
DOI: 10.1007/s11306-012-0453-1     Document Type: Article

References (57)

1. Admiraal, W., Laane, R., & Peletier, H. (1984). Participation of diatoms in the amino acid cycle of coastal waters; uptake and excretion in cultures. Marine Ecology-Progress Series, 15(3), 303-306.
2. Admiraal, W., Peletier, H., & Laane, R. (1986). Nitrogen metabolism of marine planktonic diatoms-excretion, assimilation and cellular pools of free amino-acids in 7 species with different cell size. Journal of Experimental Marine Biology and Ecology, 98(3), 241-263.
3. Anderson, M. J., & Willis, T. J. (2003). Canonical analysis of principal coordinates: A useful method of constrained ordination for ecology. Ecology, 84(2), 511-525.
4. Armbrust, E. V., Berges, J. A., Bowler, C., Green, B. R., Martinez, D., Putnam, N. H., et al. (2004). The genome of the diatom Thalassiosira pseudonana: Ecology, evolution, and metabolism. Science, 306(5693), 79-86.
5. Bates, S. S., Douglas, D. J., Doucette, G. J., & Leger, C. (1995). Enhancement of domoic acid production by reintroducing bacteria to axenic cultures of the diatom Pseudo-nitzschia multiseries. Natural Toxins, 3(6), 428-435.
6. Beardall, J., Berman, T., Heraud, P., Omo Kadiri, M., Light, B. R., Patterson, G., et al. (2001). A comparison of methods for detection of phosphate limitation in microalgae. Aquatic Sciences-Research Across Boundaries, 63(1), 107-121.
7. Bruckner, C. G., Rehm, C., Grossart, H. P., & Kroth, P. G. (2011). Growth and release of extracellular organic compounds by benthic diatoms depend on interactions with bacteria. Environmental Microbiology, 13(4), 1052-1063.
8. Cole, J. J. (1982). Interactions between bacteria and algae in aquatic ecosystems. Annual Review of Ecology and Systematics, 13(1), 291-314.
9. Croft, M. T., Lawrence, A. D., Raux-Deery, E., Warren, M. J., & Smith, A. G. (2005). Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature, 438(7064), 90-93.
10. Field, C. B., Behrenfeld, M. J., Randerson, J. T., & Falkowski, P. (1998). Primary production of the biosphere: Integrating terrestrial and oceanic components. Science, 281(5374), 237-240.
11. Flynn, K. J., & Syrett, P. J. (1986). Utilization of l-lysine and l-arginine by the diatom Phaeodactylum tricornutum. Marine Biology, 90(2), 159-163.
12. Flynn, K. J., & Wright, C. R. N. (1986). The simultaneous assimilation of ammonium and l-arginine by the marine diatom Phaeodactylum tricornutum Bohlin. Journal of Experimental Marine Biology and Ecology, 95(3), 257-269.
13. Gehrke, C. W., & Leimer, K. (1971). Trimethylsilylation of amino acids-derivatization and chromatography. Journal of Chromatography, 57(2), 219-238.
14. Groene, T. (1995). Biogenic production and consumption of dimethylsulfide (DMS) and dimethylsulfoniopropionate (DMSP) in the marine pelagic zone-a review. Journal of Marine Systems, 6(3), 191-209.
15. Ianora, A., Bentley, M. G., Caldwell, G. S., Casotti, R., Cembella, A. D., Engstrom-Ost, J., et al. (2011). The relevance of marine chemical ecology to plankton and ecosystem function: An emerging field. Marine Drugs, 9(9), 1625-1648.
16. Ianora, A., Miralto, A., Poulet, S. A., Carotenuto, Y., Buttino, I., Romano, G., et al. (2004). Aldehyde suppression of copepod recruitment in blooms of a ubiquitous planktonic diatom. Nature, 429(6990), 403-407.
17. Jensen, A., Rystad, B., & Skoglund, L. (1972). The use of dialysis culture in phytoplankton studies. Journal of Experimental Marine Biology and Ecology, 8(3), 241-248.
18. Kobayashi, K., Takata, Y., & Kodama, M. (2009). Direct contact between Pseudo-nitzschia multiseries and bacteria is necessary for the diatom to produce a high level of domoic acid. Fisheries Science, 75(3), 771-776.
19. Kolber, Z., Zehr, J., & Falkowski, P. (1988). Effects of growth irradiance and nitrogen limitation on photosynthetic energy conversion in photosystem II. Plant Physiology, 88(3), 923.
20. Legrand, C., Rengefors, K., Fistarol, G. O., & Granéli, E. (2003). Allelopathy in phytoplankton-biochemical, ecological and evolutionary aspects. Phycologia, 42(4), 406-419.
21. Leimer, K. R., Rice, R. H., & Gehrke, C. W. (1977). Complete mass-spectra of N-trifluoroacetyl-N-butyl esters of amino acids. Journal of Chromatography, 141(2), 121-144.
22. Linares, F. (2006). Effect of dissolved free amino acids (DFAA) on the biomass and production of microphytobenthic communities. Journal of Experimental Marine Biology and Ecology, 330(2), 469-481.
23. Lippemeier, S., Hartig, P., & Colijn, F. (1999). Direct impact of silicate on the photosynthetic performance of the diatom Thalassiosira weissflogii assessed by on- and off-line PAM fluorescence measurements. Journal of Plankton Research, 21(2), 269-283.
24. Liu, S., Guo, Z., Li, T., Huang, H., & Lin, S. (2011). Photosynthetic efficiency, cell volume, and elemental stoichiometric ratios in Thalassirosira weissflogii under phosphorus limitation. Chinese Journal of Oceanology and Limnology, 29(5), 1048-1056.
25. 2+ antagonists on the movement and chemoorientation of male gametes of Ectocarpus siliculosus (Phaeophyceae). Botanica Acta, 107, 451-460.
26. Matsuo, Y., Imagawa, H., Nishizawa, M., & Shizuri, Y. (2005). Isolation of an algal morphogenesis inducer from a marine bacterium. Science, 307(5715), 1598.
27. Mayali, X., & Azam, F. (2004). Algicidal bacteria in the sea and their impact on algal blooms. Journal of Eukaryotic Microbiology, 51(2), 139-144.
28. McVeigh, I., & Brown, W. H. (1954). In vitro growth of Chlamydomonas chlamydogama Bold and Haematococcus pluvialis Flotow em. Wille in mixed cultures. Bulletin of the Torrey Botanical Club, 81(3), 218-233.
29. Myklestad, S., Holm-Hansen, O., Vårum, K. M., & Volcani, B. E. (1989). Rate of release of extracellular amino acids and carbohydrates from the marine diatom Chaetoceros affinis. Journal of Plankton Research, 11(4), 763-773.
30. Nilsson, C., & Sundback, K. (1996). Amino acid uptake in natural microphytobenthic assemblages studied by microautoradiography. Hydrobiologia, 332(2), 119-129.
31. Nylund, G. M., Persson, F., Lindegarth, M., Cervin, G., Hermansson, M., & Pavia, H. (2010). The red alga Bonnemaisonia asparagoides regulates epiphytic bacterial abundance and community composition by chemical defence. FEMS Microbiology Ecology, 71(1), 84-93.
32. Nylund, G. M., Weinberger, F., Rempt, M., & Pohnert, G. (2011). Metabolomic assessment of induced and activated chemical defence in the invasive red alga Gracilaria vermiculophylla. PLoS One, 6(12), e29359.
33. Paul, C., Barofsky, A., Vidoudez, C., & Pohnert, G. (2009). Diatom exudates influence metabolism and cell growth of co-cultured diatom species. Marine Ecology-Progress Series, 389, 61-70.
34. Paul, C., & Pohnert, G. (2011). Interactions of the algicidal bacterium Kordia algicida with diatoms: Regulated protease excretion for specific algal lysis. PLoS One, 6(6), e21032.
35. Pohnert, G. (2000). Wound-activated chemical defense in unicellular planktonic algae. Angewandte Chemie International Edition, 39(23), 4352-4354.
36. Pohnert, G. (2012). How to explore the sometimes unusual chemistry of aquatic defence chemicals. In C. Brönmark, & L. A. Hansson (Eds.), Chemical Ecology in Aquatic Systems: Oxford University Press.
37. Pohnert, G., Steinke, M., & Tollrian, R. (2007). Chemical cues, defence metabolites and the shaping of pelagic interspezific interactions. Trends in Ecology & Evolution, 22(4), 198-204.
38. Roy, S., & Legendre, L. (1979). DCMU-enhanced fluorescence as an index of photosynthetic activity in phytoplankton. Marine Biology, 55(2), 93-101.
39. Selander, E., Jakobsen, H. H., Lombard, F., & Kiorboe, T. (2011). Grazer cues induce stealth behavior in marine dinoflagellates. Proceedings of the National Academy of Sciences of the United States of America, 108(10), 4030-4034.
40. Selander, E., Thor, P., Toth, G., & Pavia, H. (2006). Copepods induce paralytic shellfish toxin production in marine dinoflagellates. Proceedings of the Royal Society B Biological Sciences, 273(1594), 1673-1680.
41. Seyedsayamdost, M. R., Case, R. J., Kolter, R., & Clardy, J. (2011). The jekyll-and-hyde chemistry of Phaeobacter gallaeciensis. Nature Chemistry, 3(4), 331-335.
42. Sieg, R. D., Poulson-Ellestad, K. L., & Kubanek, J. (2011). Chemical ecology of the marine plankton. Natural Product Reports, 28(2), 388-399.
43. Spielmeyer, A., & Pohnert, G. (2010). Direct quantification of dimethylsulfoniopropionate (DMSP) with hydrophilic interaction liquid chromatography/mass spectrometry. Journal of Chromatography B, 878(31), 3238-3242.
44. Steinke, M., Malin, G., & Liss, P. S. (2002). Trophic interactions in the sea: An ecological role for climate relevant volatiles? Journal of Phycology, 38(4), 630-638.
45. Teeling, H., Fuchs, B. M., Becher, D., Klockow, C., Gardebrecht, A., Bennke, C. M., et al. (2012). Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science, 336(6081), 608-611.
46. van Donk, E., Ianora, A., & Vos, M. (2011). Induced defences in marine and freshwater phytoplankton: A review. Hydrobiologia, 668(1), 3-19.
47. Vanelslander, B., Paul, C., Grueneberg, J., Prince, E. K., Gillard, J., Sabbe, K., et al. (2012). Daily bursts of biogenic cyanogen bromide (BrCN) control biofilm formation around a marine benthic diatom. Proceedings of the National Academy of Sciences of the United States of America, 109(7), 2412-2417.
48. Vardi, A., Formiggini, F., Casotti, R., De Martino, A., Ribalet, F., Miralto, A., et al. (2006). A stress surveillance system based on calcium and nitric oxide in marine diatoms. PLoS Biology, 4(3), 411-419.
49. Vidoudez, C., Casotti, R., Bastianini, M., & Pohnert, G. (2011). Quantification of dissolved and particulate polyunsaturated aldehydes in the Adriatic Sea. Marine Drugs, 9(4), 500-513.
50. Vidoudez, C., & Pohnert, G. (2008). Growth phase-specific release of polyunsaturated aldehydes by the diatom Skeletonema marinoi. Journal of Plankton Research, 30(11), 1305.
51. Vidoudez, C., & Pohnert, G. (2012). Comparative metabolomics of the diatom Skeletonema marinoi in different growth phases. Metabolomics, 8, 654-669.
52. Wagner, C., Sefkow, M., & Kopka, J. (2003). Construction and application of a mass spectral and retention time index database generated from plant GC/EI-TOF-MS metabolite profiles. Phytochemistry, 62(6), 887-900.
53. Wagner-Döbler, I., Ballhausen, B., Berger, M., Brinkhoff, T., Buchholz, I., Bunk, B., et al. (2010). The complete genome sequence of the algal symbiont Dinoroseobacter shibae: A hitchhiker's guide to life in the sea. ISME Journal, 4(1), 61-77.
54. Wolfe, G. V., Steinke, M., & Kirst, G. O. (1997). Grazing-activated chemical defence in a unicellular marine alga. Nature, 387(6636), 894-897.
55. Yamasaki, Y., Nagasoe, S., Matsubara, T., Shikata, T., Shimasaki, Y., Oshima, Y., et al. (2007). Allelopathic interactions between the bacillariophyte Skeletonema costatum and the raphidophyte Heterosigma akashiwo. Marine Ecology-Progress Series, 339, 83.
56. Yamasaki, Y., Shikata, T., Nukata, A., Ichiki, S., Nagasoe, S., Matsubara, T., et al. (2009). Extracellular polysaccharide-protein complexes of a harmful alga mediate the allelopathic control it exerts within the phytoplankton community. ISME Journal, 3(7), 808-817.
57. Zhang, J. Z., & Fischer, C. J. (2006). A simplified resorcinol method for direct spectrophotometric determination of nitrate in seawater. Marine Chemistry, 99(1-4), 220-226.