Trichodesmium-derived dissolved organic matter is a source of nitrogen capable of supporting the growth of toxic red tide Karenia brevis

Marine Ecology Progress Series

Volumn 483, Issue , 2013, Pages 31-45

  Sipler, Rachel E ^a,b   Bronk, Deborah A ^b   Seitzinger, Sybil P ^a,c   Lauck, Ronald J ^a   McGuinness, Lora R ^a   Kirkpatrick, Gary J ^d   Heil, Cynthia A ^e   Kerkhof, Lee J ^a   Schofield, Oscar M ^a  

^a RUTGERS UNIVERSITY   (United States)

^b VIRGINIA INSTITUTE OF MARINE SCIENCE   (United States)

^c ROYAL SWEDISH ACADEMY OF SCIENCES   (Sweden)

^d MOTE MARINE LABORATORY   (United States)

^e BIGELOW LABORATORY FOR OCEAN SCIENCES   (United States)

Author keywords

DON; ESI MS; FT ICR MS; Karenia brevis; Red tide; Trichodesmium

Indexed keywords

ABUNDANCE; BIOAVAILABILITY; DISSOLVED ORGANIC NITROGEN; EXPERIMENTAL STUDY; GROWTH RATE; LIPID; MICROBIAL COMMUNITY; NITROGEN FIXATION; NUTRIENT AVAILABILITY; POLYMORPHISM; PROTEIN; RED TIDE; TOXIC SUBSTANCE;

ATLANTIC OCEAN; GULF OF MEXICO;

BACTERIA (MICROORGANISMS); DINOPHYCEAE; KARENIA BREVIS; OTUS; TRICHODESMIUM; TRICHODESMIUM SP.;

EID: 84878615369     PISSN: 01718630     EISSN: None     Source Type: Journal    
DOI: 10.3354/meps10258     Document Type: Article

References (75)

1. Aluwihare LI, Meador T (2008) Chemical composition of marine dissolved organic nitrogen. In: Capone DG, Bronk DA, Mulholland M, Carpenter EJ (eds) Nitrogen in the marine environment, 2nd edn. Elsevier, San Diego, CA
2. Anderson DM, Glibert PM, Burkholder JM (2002) Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries 25: 704-726
3. Babcock DA, Wawrik B, Paul JH, McGuinness L, Kerkhof LJ (2007) Rapid screening of a large insert BAC library for specific 16S rRNA genes using TRFLP. J Microbiol Methods 71: 156-161
4. Baden DG, Mende TJ (1979) Amino acid utilization by Gymnodinium brevis. Phytochemistry 18: 247-251
5. Hansell DA, Carlson CA (eds) Biogeochemistry of marine dissolved organic matter. Elsevier, San Diego, CA, p 51-90
6. Bhatia MP, Das SB, Longnecker K, Charette MA, Kujawinski EB (2010) Molecular characterization of dissolved organic matter associated with the Greenland ice sheet. Geochim Cosmochim Acta 74: 3768-3784
7. Bissett WP, Arnone R, Debra S, Dye D, Kirkpatrick G, Mobley C, Schofield O (2008) The integration of ocean color remote sensing with coastal nowcast/forecast simulations of harmful algal blooms (HABs). In: Babin M, Cullen JJ (eds) Real time coastal observing systems for ecosystems dynamics and harmful algal blooms. UNESCO, Paris, p 695-732
8. Brand LE, Campbell L, Bresnan E (2012) Karenia: the bio-logy and ecology of a toxic genus. Harmful Algae 14: 156-178
9. Bronk DA (2002) Dynamics of dissolved organic nitrogen. In: Hansell DA, Carlson CA (eds) Biogeochemistry of marine dissolved organic matter. Elsevier, San Diego, CA, p 153-247
10. Bronk DA, Sanderson MP, Mulholland MR, Heil CA, O'Neil JM (2004) Organic and inorganic nitrogen uptake kinetics in field populations dominated by Karenia brevis. In: Steidinger KA, Landsberg JH, Tomas CR, Vargo GA (eds) Harmful algae 2002. Proc 10th International Conference on Harmful Algae. Florida Fish and Wildlife Conservation Commission, Florida Institute of Oceanography and Intergovernmental Oceanographic Commission of UNESCO, Paris, p 80-82
11. Bronk DA, Killberg-Thoreson L, Mulholland MR, Sipler RE and others (in press) Nitrogen uptake and regeneration (ammonium regeneration, nitrification and photoproduction) in waters of the west Florida shelf prone to blooms of Karenia brevis. Harmful Algae
12. Capone DG, Ferrier MD, Carpenter EJ (1994) Amino acid cycling in colonies of the planktonic marine cyanobacterium Trichodesmium thiebautii. Appl Environ Microbiol 60: 3989-3995
13. Capone DG, Zehr JP, Pearl HW, Bergman B, Carpenter EJ (1997) Trichodesmium, a globally significant marine cyanobacterium. Science 276: 1221-1229
14. Caron DA (1994) Inorganic nutrients, bacteria and the microbial loop. Microb Ecol 28: 295-298
15. Carpenter EJ, Romans K (1991) Major role of the cyanobacterium Trichodesmium sp. in nutrient cycling in the North Atlantic Ocean. Science 254: 1356-1358
16. Chen YB, Zehr JP, Mellon M (1996) Growth and nitrogen fixation of the diazotrophic filamentous non-heterocystous cyanobacterium Trichodesmium sp. IMS101 in defined media: evidence for a circadian rhythm. J Phycol 32: 916-923
17. Dittmar T, Koch B, Hertkorn N, Kattner G (2008) A simpler and efficient method for the solid-phase extraction of dissolved organic matter (SPE-DOM) from seawater. Limnol Oceanogr Methods 6: 230-235
18. Dixon LK, Steidinger KA (2004) Correlation of Karenia brevis presence in the eastern Gulf of Mexico with rainfall and riverine flow. In: Steidinger KA, Landsberg JH, Tomas CR, Vargo GA (eds) Harmful Algae 2002. Proc 10th International Conference on Harmful Algae. Florida Fish and Wildlife Conservation Commission, Florida Institute of Oceanography and Intergovernmental Oceanographic Commission of UNESCO, Paris, p 29-31
19. Doucette GJ, McGovern ER, Babinchak IA (1999) Algicidal bacteria active against Gymnodinium breve (Dinophyceae). I. Bacterial isolation and characterization of killing activity. J Phycol 35: 1447-1457
20. Field MP, LaVigne M, Murphy KR, Ruiz GM, Sherrell RM (2007) Direct determination of P, V, Mn, As, Mo, Ba and U in seawater by SF-ICP-MS. J Anal At Spectrom 22: 1145-1151
21. Fleming LE, Kirkpatrick B, Backer LC, Walsh CJ and others (2011) Review of Florida red tide and human health effects. Harmful Algae 10: 224-233
22. Geesey M, Tester PA (1993) Gymnodinium breve: ubiquitous in Gulf of Mexico waters? In: Smayda TJ, Shimizu Y (eds) Toxic phytoplankton blooms in the sea. Elsevier, San Diego, CA, p 251-255
23. Glibert PM, Bronk DA (1994) Release of dissolved organic nitrogen by marine diazotrophic cyanobacteria, Trichodesmium sp. Appl Environ Microbiol 60: 3996-4000
24. Glibert PM, Heil CA, Hollander DJ, Revilla M, Hoare A, Alexander J, Murasko S (2004) Evidence for dissolved organic nitrogen and phosphorus uptake during a cyanobacterial bloom in Florida Bay. Mar Ecol Prog Ser 280: 73-83
25. Glibert PM, Harison J, Heil C, Seitzinger S (2006) Escalating worldwide use of urea-a global change contributing to coastal eutrophication. Biogeochemistry 77: 441-463
26. Glibert PM, Burkholder JM, Kana TM, Alexander J, Skelton H, Shilling C (2009) Grazing by Karenia brevis on Synechococcus enhances its growth rate and may help to sustain blooms. Aquat Microb Ecol 55: 17-30
27. Havens JJ, Heil CA, Hollander D, Vargo GA, Ault D, Murasko S, Walsh JJ (2004) Isotopic constraints on nutrient sources supporting the 2001 Karenia brevis bloom. In: Steidinger KA, Landsberg JH, Tomas CR, Vargo GA (eds) Harmful Algae 2002. Proc 10th International Conference on Harmful Algae. Florida Fish and Wildlife Conservation Commission, Florida Institute of Oceanography and Intergovernmental Oceanographic Commission of UNESCO, Paris, p 32-34
28. Heil CA, Revilla M, Glibert P, Murasko S (2007) Nutrient quality drives differential phytoplankton community composition on the southwest Florida shelf. Limnol Oceanogr 52: 1067-1078
29. Jeong HJ, Park JY, Nho JH, Park MO and others (2005) Feeding by red-tide dinoflagellates on the cyanobacterium Synechococcus. Aquat Microb Ecol 41: 131-143
30. Jones KL, Mikulski CM, Barnhorst A, Doucette G (2010) Comparative analysis of bacterioplankton assemblages from Karenia brevis bloom and nonbloom water on the west Florida shelf (Gulf of Mexico, USA) using 16S rRNA gene clone libraries. FEMS Microbiol Ecol 73: 468-485
31. Kebarle P, Ho Y (1997) On the mechanism of electrospray ionization, in electrospray ionization mass spectrometry. In: Cole R (ed) Electrospray ionization mass spectrometry. Wiley Inter Science, New York, NY, p 3-63
32. Kido Soule MC, Longnecker K, Giovannoni SJ, Kujawinski EB (2010) Impact of instrument and experiment parameters on reproducibility of ultrahigh resolution ESI FT-ICR mass spectra of natural organic matter. Org Geochem 41: 725-733
33. Killberg-Thoreson LM, Roberts QN, Sanderson MP, Mulholland MR, Heil CA, O'Neil JM, Bronk DA (in press) Nitrogen uptake kinetics in field populations of Karenia brevis. Harmful Algae
34. Kim S, Kramer RW, Hatcher PG (2003) Graphical method for analysis of ultrahigh-resolution broadband mass spectra of natural organic matter, the van Krevelen diagram. Anal Chem 75: 5336-5344
35. Kirkpatrick B, Fleming LE, Sqicciarini D, Backer LC and others (2004) Literature review of Florida red tide: implications for human health effects. Harmful Algae 3: 99-115
36. Koch BP, Witt M, Engbrodt R, Dittmar T, Kattner G (2005) Molecular formulae of marine and terrigenous dissolved organic matter detected by electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry. Geochim Cosmochim Acta 69: 3299-3308
37. Kodama M, Doucette GJ, Green DH (2006) Relationships between bacteria and harmful algae. In: Granéli, E, Turner, JT, (eds) Ecology of harmful algae. Springer, New York, NY, p 163-175
38. Kujawinski EB, Longnecker K, Blough NV, Del Vecchio R, Finlay L, Kitner JB, Giovannoni SJ (2009) Identification of possible source markers in marine dissolved organic matter using ultrahigh resolution mass spectrometry. Geochim Cosmochim Acta 73: 4384-4399
39. Landsberg JH, Flewelling LJ, Naar J (2009) Karenia brevis red tides, brevetoxins in the food web, and impacts on natural resources: decadal advancements. Harmful Algae 8: 598-607
40. Larkin SL, Adams CL (2007) Harmful algal blooms and coastal businesses: economic consequences in Florida. Soc Nat Resour 20: 849-859
41. Lenes JM, Darrow BP, Cattrall C, Heil CA, Callahan M, Vargo GA, Byrne RH (2001) Iron fertilization and the Trichodesmium sp. response on the West Florida shelf. Limnol Oceanogr 46: 1261-1277
42. Loret P, Tengs T, Villareal TA, Singler H and others (2002) No difference found in ribosomal DNA sequence from physiological diverse clones of Karenia brevis (Dinophyceae) from the Gulf of Mexico. J Plankton Res 24: 735-739
43. Magurran AE (2004) Measuring biological diversity. Blackwell publishing, Oxford
44. Mayali X, Doucette GJ (2002) Microbial interactions and population dynamics of an algicidal bacterium active against Karenia brevis (Dinophyceae). Harmful Algae 1: 277-293
45. McEwen CN, Larsen BS (1997) Electrospray ionization on quadrapole and magnetic-sector mass spectrometer. In: Cole R (ed) Electrospray ionization mass spectrometry. Wiley Inter Science, New York, NY, p 177-202
46. McGuinness LM, Salganik M, Vega L, Pickering KD, Kerkhof LJ (2006) Replicability of bacterial communities in denitrifying bioreactors as measured by PCR/T-RFLP analysis. Environ Sci Technol 40: 509-515
47. Mopper K, Stubbins A, Ritchie JD, Bialk HM, Hatcher PG (2007) Advanced instrumental approaches for characterization of marine dissolved organic matter: extraction techniques, mass spectrometry, and nuclear magnetic resonance spectroscopy. Chem Rev 107: 419-442
48. Mulholland MR, Capone DG (2001) The stoichiometry of N and C utilization in cultured populations of Trichodesmium IMS101. Limnol Oceanogr 46: 436-443
49. Mulholland MR, Heil CA, Bronk DA, O'Neil JM, Bernhardt P (2004) Does nitrogen regeneration from the N2 fixing cyanobacteria Trichodesmium sp. fuel Karenia brevis blooms in the Gulf of Mexico. In: Steidinger KA, Landsberg JH, Tomas CR, Vargo GA (eds) Harmful Algae 2002. Proc 10th International Conference on Harmful Algae. Florida Fish and Wildlife Conservation Commission, Florida Institute of Oceanography and Intergovernmental Oceanographic Commission of UNESCO, Paris, p 47-49
50. NOAA (2007) Gulf of Mexico harmful algal bloom bulletin, Region: Southwest Florida. http://tides and currents.noaa.gov/hab/bulletins.html
51. Ransom Hardison D, Sunda WG, Litaker RW, Shea D, Tester PA (2012) Nitrogen limitation increases brevetoxins in Karenia brevis (Dinophyceae) implications for bloom toxicity. J Phycol 48: 844-858
52. Sakano Y, Kerkhof L (1998) Assessment of changes in microbial community structure during operation of an ammonia biofilter with molecular tools. Appl Environ Microbiol 64: 4877-4882
53. Schofield O, Kerfoot J, Mahoney K, Moline M, Oliver M, Lohrenz S, Kirkpatrick G (2006) Vertical migration of the toxic dinoflagellate Karenia brevis and the impact on ocean optical properties. J Geophys Res 111: C06009, doi: 10.1029/2005JC003115
54. Schofield O, Bosch J, Glenn SM, Kirkpatrick G and others (2008) Bio-optics in integrated ocean observing networks: potential for studying harmful algal blooms. In: Babin M, Roelser C, Cullen JJ (eds) Real time coastal observing systems for ecosystems dynamics and harmful algal blooms. UNESCO, Paris, p 85-108
55. Seitzinger SP, Hartnett H, Lauck R, Mazurek M, Minegishi T, Spyres G, Styles R (2005) Molecular-level chemical characterization and bioavailability of dissolved organic matter in stream water using electrospray-ionization mass spectrometry. Limnol Oceanogr 50: 1-12
56. Sharp JH, Benner R, Bennett L, Carlson CA, Dow R, Fitzwater SE (1993) Re-evaluation of high temperature combustion and chemical oxidation measurements of dissolved organic carbon in seawater. Limnol Oceanogr 38: 1774-1782
57. Sharp JH, Beauregard AY, Burdige D, Cauwet G and others (2004) A direct instrument comparison for measurement of total dissolved nitrogen in seawater. Mar Chem 84: 181-193
58. Simjouw JP, Minor EC, Mopper K (2005) Isolation and characterization of estuarine dissolved organic matter: comparison of ultrafiltration and C18 solid-phase extraction techniques. Mar Chem 96: 219-235
59. Sipler RE (2009) The role of dissolved organic matter in structuring microbial community composition. PhD dissertation, Rutgers, The State University of New Jersey, New Brunswick, NJ
60. Sipler RE, Seitzinger SP (2008) Use of Electrospray Ionization (ESI) Mass Spectrometry to investigate complex Dissolved Organic Matter (DOM) and its potential applications in phytoplankton research. Harmful Algae 8: 182-187
61. Sipler RE, McGuinness LM, Kirkpatrick GJ, Kerkhof LJ, Schofield OM (in press) Bacteriocidal effects of brevetoxin on natural microbial communities. Harmful Algae
62. Sleighter RL, Hatcher PG (2007) The application of electrospray ionization coupled to ultrahigh resolution mass spectrometry for the molecular characterization of natural organic matter. J Mass Spectrom 42: 559-574
63. Sleighter RL, Hatcher PG (2008) Molecular characterization of dissolved organic matter (DOM) along a river to ocean transect of the lower Chesapeake Bay by ultrahigh resolution electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry. Mar Chem 110: 140-152
64. Steidinger KA (1975) Implications of dinoflagellate life cycles on initiation of Gymnodinium breve red tides. Environ Lett 9: 129-139
65. Steidinger KA, Haddad K (1981) Biological and hydrographic aspects of red tides. Bioscience 31: 814-819
66. Stolte W, Garcés E (2006) Ecological aspects of harmful algal in situ population growth rates. In: Granéli E, Turner JT (eds) Ecology of harmful algae. Springer, New York, NY, p 163-175
67. Tester PA, Steidinger KA (1997) Gymnodinium breve red tide blooms: initiation, transport and consequences of surface circulation. Limnol Oceanogr 42: 1039-1051
68. Van Berkel GJ (1997) The electrolytic nature of electrospray. In: Cole RB (ed) Electrospray ionization mass spectro-metry. Wiley Inter Science, New York, NY, p 65-105
69. Van Dolah FM, Leighfield TA, Kamykowski D, Kirkpatrick GJ (2008) Cell cycle behavior of laboratory and field populations of the Florida red tide dinoflagellate, Karenia brevis. Cont Shelf Res 28: 11-13
70. Vargo GA (2009) A brief summary of the physiology and ecology of Karenia brevis Davis (G. Hansen and Moestrup comb. nov.) red tides on the West Florida Shelf and of hypotheses posed for their initiation, growth, maintenance, and termination. Harmful Algae 8: 573-584
71. Vargo GA, Carder KA, Gregg W, Heil CA, Shanley E, Steidinger KA, Haddad KD (1987) The potential contribution of primary production by red tides to the West Florida Shelf ecosystem. Limnol Oceanogr 32: 762-767
72. Vargo GA, Heil CA, Alut DN, Neely MB and others (2004) Four Karenia brevis blooms: a comparative analysis. In: Steidinger KA, Landsberg JH, Tomas CR, Vargo GA (eds) Harmful Algae 2002. Proc 10th International Conference on Harmful Algae. Florida Fish and Wildlife Conservation Commission, Florida Institute of Oceanography and Intergovernmental Oceanographic Commission of UNESCO, Paris, p 14-16
73. Vargo GA, Heil CA, Fanning KA, Dixon LK and others (2008) Nutrient availability in support of Karenia brevis blooms on the central West Florida Shelf: What keeps Karenia blooming? Cont Shelf Res 28: 73-98
74. Walsh JJ, Steidinger KA (2001) Saharan dust and Florida red tides: the cyanophyte connection. J Geophys Res 106: 11597-11612
75. Walsh JJ, Jolliff JK, Darrow BP, Lenes JM and others (2006) Red tides in the Gulf of Mexico: where, when and why? J Geophys Res 111: C11003, doi: 10. 1029/2004 JC 002813