title: Increased toxicity of Karenia brevis during phosphate limited growth: ecological and evolutionary implications.
abstract: Karenia brevis is the dominant toxic red tide algal species in the Gulf of Mexico. It produces potent neurotoxins (brevetoxins [PbTxs]), which negatively impact human and animal health, local economies, and ecosystem function. Field measurements have shown that cellular brevetoxin contents vary from 1-68 pg/cell but the source of this variability is uncertain. Increases in cellular toxicity caused by nutrient-limitation and inter-strain differences have been observed in many algal species. This study examined the effect of P-limitation of growth rate on cellular toxin concentrations in five Karenia brevis strains from different geographic locations. Phosphorous was selected because of evidence for regional P-limitation of algal growth in the Gulf of Mexico. Depending on the isolate, P-limited cells had 2.3- to 7.3-fold higher PbTx per cell than P-replete cells. The percent of cellular carbon associated with brevetoxins (%C-PbTx) was ~ 0.7 to 2.1% in P-replete cells, but increased to 1.6-5% under P-limitation. Because PbTxs are potent anti-grazing compounds, this increased investment in PbTxs should enhance cellular survival during periods of nutrient-limited growth. The %C-PbTx was inversely related to the specific growth rate in both the nutrient-replete and P-limited cultures of all strains. This inverse relationship is consistent with an evolutionary tradeoff between carbon investment in PbTxs and other grazing defenses, and C investment in growth and reproduction. In aquatic environments where nutrient supply and grazing pressure often vary on different temporal and spatial scales, this tradeoff would be selectively advantageous as it would result in increased net population growth rates. The variation in PbTx/cell values observed in this study can account for the range of values observed in the field, including the highest values, which are not observed under N-limitation. These results suggest P-limitation is an important factor regulating cellular toxicity and adverse impacts during at least some K. brevis blooms.
authors.affiliation: National Oceanic and Atmospheric Administration, National Ocean Service, Center for Coastal Fisheries and Habitat Research, Beaufort, North Carolina, USA. rance.hardison@noaa.gov
authors.forename: Donnie Ransom
authors.initials: DR
authors.lastname: Hardison
authors.forename: William G
authors.initials: WG
authors.lastname: Sunda
authors.forename: Damian
authors.initials: D
authors.lastname: Shea
authors.forename: Richard Wayne
authors.initials: RW
authors.lastname: Litaker
mesh_terms: D004141:Dinoflagellida / Q000254:growth & development*; D017753:Ecosystem; D060851:Gulf of America; D057097:Harmful Algal Bloom; D006801:Humans; D008387:Marine Toxins / Q000378:metabolism; D010710:Phosphates / Q000378:metabolism*
chemical_list: C017885:Gymnodinium breve toxin; D008387:Marine Toxins; D010710:Phosphates
references.citation: Sci Prog. 1960;11:150-70
references.pmid: 24545739
references.citation: J Phycol. 2009 Feb;45(1):154-63
references.pmid: 27033654
references.citation: Toxicon. 2010 Aug 15;56(2):137-49
references.pmid: 19925816
references.citation: Environ Health Perspect. 2009 Aug;117(8):1239-43
references.pmid: 19672403
references.citation: Harmful Algae. 2010 Feb 1;9(2):186-189
references.pmid: 20161504
references.citation: J Environ Qual. 2008 Feb 11;37(2):318-24
references.pmid: 18268293
references.citation: Science. 2008 May 16;320(5878):893-7
references.pmid: 18487184
references.citation: Harmful Algae. 2012 Jan 1;13:89-94
references.pmid: 23762030
references.citation: J Phycol. 2009 Feb;45(1):176-92
references.pmid: 27033656
references.citation: Ecotoxicology. 2008 Oct;17(7):623-31
references.pmid: 18758951
references.citation: Biol Lett. 2006 Jun 22;2(2):194-7
references.pmid: 17148360
references.citation: Nature. 2005 Jun 9;435(7043):755-6
references.pmid: 15944690
references.citation: Neurotoxicology. 1999 Dec;20(6):909-20
references.pmid: 10693972
references.citation: Environ Health Perspect. 2005 May;113(5):644-9
references.pmid: 15866778
references.citation: J Phycol. 2012 Aug;48(4):844-58
references.pmid: 27008996
references.citation: Nat Rev Microbiol. 2011 Jun 16;9(7):499-508
references.pmid: 21677685
references.citation: Nature. 2006 Jan 5;439(7072):68-71
references.pmid: 16397497
references.citation: Harmful Algae. 2006 Oct 1;5(5):526-533
references.pmid: 20357898
references.citation: Nat Toxins. 1998;6(3-4):127-35
references.pmid: 10223628
references.citation: Ann Rev Mar Sci. 2009;1:245-78
references.pmid: 21141037
references.citation: Mar Drugs. 2011;9(9):1625-1648
references.pmid: 22131962
references.citation: Mol Pharmacol. 1986 Aug;30(2):129-35
references.pmid: 2426567
references.citation: Aquat Toxicol. 2012 Jan 15;106-107:85-94
references.pmid: 22115907
references.citation: PLoS One. 2012;7(5):e36845
references.pmid: 22629336
references.citation: Chemosphere. 2008 Nov;73(8):1373-7
references.pmid: 18845312
references.citation: Mar Drugs. 2008;6(3):431-55
references.pmid: 19005578
references.citation: Toxicon. 1988;26(10):961-3
references.pmid: 3201483
references.citation: Environ Health Perspect. 2005 May;113(5):638-43
references.pmid: 15866777
references.citation: Science. 2000 Aug 4;289(5480):759-62
references.pmid: 10926534
references.citation: J Allergy Clin Immunol. 1984 Jun;73(6):824-8
references.pmid: 6327792
references.citation: Environ Sci Technol. 2006 Dec 15;40(24):7548-53
references.pmid: 17256493
references.citation: Harmful Algae. 2004 Apr 1;3(2):99-115
references.pmid: 20411030
references.citation: Annu Rev Plant Physiol Plant Mol Biol. 1999 Jun;50:333-359
references.pmid: 15012213