Phytoplankton Cell Lysis Associated with Polyunsaturated Aldehyde Release in the Northern Adriatic Sea

Diatoms are able to react to biotic and abiotic stress, such as competition, predation and unfavorable growth conditions, by producing bioactive compounds including polyunsaturated aldehydes (PUAs). PUAs have been shown to act against grazers and either enhance or inhibit the growth of different phytoplankton and bacteria both in culture and in the field. Presence of nanomolar concentrations of dissolved PUAs in seawater has been reported in the North Adriatic Sea (Mediterranean), suggesting that these compounds are released in seawater following diatom cell lysis. However, the origin of the PUAs and their effects on natural phytoplankton assemblages remain unclear. Here we present data from four oceanographic cruises that took place during diatom blooms in the northern Adriatic Sea where concentrations of particulate and dissolved PUAs were monitored along with phytoplankton cell lysis. Cell lysis was positively correlated with both concentrations of particulate and dissolved PUAs (R = 0.69 and R = 0.77, respectively), supporting the hypothesis that these compounds are released by cell lysis. However, the highest concentration of dissolved PUAs (2.53 nM) was measured when cell lysis was high (0.24 d−1) but no known PUA-producing diatoms were detected, suggesting either that other organisms can produce PUAs or that PUA-producing enzymes retain activity extracellularly after diatom cells have lysed. Although in situ concentrations of dissolved PUAs were one to three orders of magnitude lower than those typically used in laboratory culture experiments, we argue that concentrations produced in the field could induce similar effects to those observed in culture and therefore may help shape plankton community composition and function in the oceans.

[1]  J. Gasol,et al.  Group-specific effects on coastal bacterioplankton of polyunsaturated aldehydes produced by diatoms , 2011 .

[2]  M. Bastianini,et al.  Quantification of Dissolved and Particulate Polyunsaturated Aldehydes in the Adriatic Sea , 2011, Marine drugs.

[3]  G. Pohnert,et al.  Dynamics of Dissolved and Particulate Polyunsaturated Aldehydes in Mesocosms Inoculated with Different Densities of the Diatom Skeletonema marinoi , 2011, Marine drugs.

[4]  S. Dittami,et al.  Culture conditions affect fatty acid content along with wound-activated production of polyunsaturated aldehydes in Thalassiosira rotula (Coscinodiscophyceae) , 2010 .

[5]  G. Pohnert,et al.  High plasticity in the production of diatom-derived polyunsaturated aldehydes under nutrient limitation: physiological and ecological implications. , 2009, Protist.

[6]  Scott D. Soelberg,et al.  Surface plasmon resonance detection using antibody-linked magnetic nanoparticles for analyte capture, purification, concentration, and signal amplification. , 2009, Analytical chemistry.

[7]  G. Pohnert,et al.  Growth phase-specific release of polyunsaturated aldehydes by the diatom Skeletonema marinoi , 2008 .

[8]  R. Casotti,et al.  Differential effect of three polyunsaturated aldehydes on marine bacterial isolates. , 2008, Aquatic toxicology.

[9]  R. Casotti,et al.  Growth inhibition of cultured marine phytoplankton by toxic algal-derived polyunsaturated aldehydes. , 2007, Aquatic toxicology.

[10]  K. Bidle,et al.  Iron Starvation and Culture Age Activate Metacaspases and Programmed Cell Death in the Marine Diatom Thalassiosira pseudonana , 2007, Eukaryotic Cell.

[11]  A. Fontana,et al.  LOX‐Induced Lipid Peroxidation Mechanism Responsible for the Detrimental Effect of Marine Diatoms on Zooplankton Grazers , 2007, Chembiochem : a European journal of chemical biology.

[12]  Thomas Wichard,et al.  Age and nutrient limitation enhance polyunsaturated aldehyde production in marine diatoms. , 2007, Phytochemistry.

[13]  Thomas Wichard,et al.  Lipid and Fatty Acid Composition of Diatoms Revisited: Rapid Wound‐Activated Change of Food Quality Parameters Influences Herbivorous Copepod Reproductive Success , 2007, Chembiochem : a European journal of chemical biology.

[14]  R. Tollrian,et al.  Chemical cues, defence metabolites and the shaping of pelagic interspecific interactions. , 2007, Trends in ecology & evolution.

[15]  G. Pohnert,et al.  Biosynthesis of polyunsaturated short chain aldehydes in the diatom Thalassiosira rotula. , 2007, Organic letters.

[16]  A. Fontana,et al.  Chemistry of oxylipin pathways in marine diatoms , 2007 .

[17]  K. Matsui Green leaf volatiles: hydroperoxide lyase pathway of oxylipin metabolism. , 2006, Current opinion in plant biology.

[18]  Georg Pohnert,et al.  Formation of halogenated medium chain hydrocarbons by a lipoxygenase/hydroperoxide halolyase-mediated transformation in planktonic microalgae. , 2006, Journal of the American Chemical Society.

[19]  Chris Bowler,et al.  A Stress Surveillance System Based on Calcium and Nitric Oxide in Marine Diatoms , 2006, PLoS biology.

[20]  K. Nagasaki,et al.  Previously Unknown Virus Infects Marine Diatom , 2005, Applied and Environmental Microbiology.

[21]  Dongyan Liu,et al.  Survey of the Chemical Defence Potential of Diatoms: Screening of Fifty Species for α,β,γ,δ-unsaturated aldehydes , 2005, Journal of Chemical Ecology.

[22]  Thomas Wichard,et al.  Determination and quantification of alpha,beta,gamma,delta-unsaturated aldehydes as pentafluorobenzyl-oxime derivates in diatom cultures and natural phytoplankton populations: application in marine field studies. , 2005, Journal of chromatography. B, Analytical technologies in the biomedical and life sciences.

[23]  M. Bastianini,et al.  Phytoplankton photosynthetic activity and growth rates in the NW Adriatic Sea , 2004 .

[24]  A. Fontana,et al.  The role of complex lipids in the synthesis of bioactive aldehydes of the marine diatom Skeletonema costatum. , 2004, Biochimica et biophysica acta.

[25]  M. Blondel,et al.  Cytotoxicity of diatom-derived oxylipins in organisms belonging to different phyla , 2004, Journal of Experimental Biology.

[26]  V. Smetácek,et al.  Aldehyde suppression of copepod recruitment in blooms of a ubiquitous planktonic diatom , 2004, Nature.

[27]  K. Nagasaki,et al.  Isolation and Characterization of a Novel Single-Stranded RNA Virus Infecting the Bloom-Forming Diatom Rhizosolenia setigera , 2004, Applied and Environmental Microbiology.

[28]  Ivo Feussner,et al.  The lipoxygenase pathway. , 2003, Annual review of plant biology.

[29]  G. Spiteller The relationship between changes in the cell wall, lipid peroxidation, proliferation, senescence and cell death , 2003 .

[30]  C. Legrand,et al.  Allelopathy in phytoplankton - biochemical, ecological and evolutionary aspects , 2003 .

[31]  C. Winter,et al.  Lysis of plankton in the non-stratified southern North Sea during summer and autumn 2000 , 2003 .

[32]  J. Rijstenbil Assessment of oxidative stress in the planktonic diatom Thalassiosira pseudonana in response to UVA and UVB radiation , 2002 .

[33]  A. Fontana,et al.  Detection of short-chain aldehydes in marine organisms: the diatom Thalassiosira rotula , 2002 .

[34]  A. Fontana,et al.  New birth-control aldehydes from the marine diatom Skeletonema costatum: characterization and biogenesis , 2002 .

[35]  G. Pohnert Phospholipase A2 Activity Triggers the Wound-Activated Chemical Defense in the Diatom Thalassiosira rotula , 2002, Plant Physiology.

[36]  J. Landsberg,et al.  The Effects of Harmful Algal Blooms on Aquatic Organisms , 2002 .

[37]  A. Pugnetti,et al.  Observations on phytoplankton productivity in relation to hydrography in the Northern Adriatic , 2002 .

[38]  G. Pohnert Wound-Activated Chemical Defense in Unicellular Planktonic Algae. , 2000, Angewandte Chemie.

[39]  M. Cabrini,et al.  The insidious effect of diatoms on copepod reproduction , 1999, Nature.

[40]  Manfred Ehrhardt,et al.  Methods of seawater analysis , 1999 .

[41]  S. Agustí,et al.  Dissolved esterase activity as a tracer of phytoplankton lysis: Evidence of high phytoplankton lysis rates in the northwestern Mediterranean , 1998 .

[42]  C. Brussaard,et al.  INFLUENCE OF BACTERIA ON PHYTOPLANKTON CELL MORTALITY WITH PHOSPHORUS OR NITROGEN AS THE ALGAL-GROWTH-LIMITING NUTRIENT , 1998 .

[43]  P. Falkowski,et al.  Physiological stress and cell death in marine phytoplankton: Induction of proteases in response to nitrogen or light limitation , 1998 .

[44]  C. Brussaard,et al.  AUTOLYSIS KINETICS OF THE MARINE DIATOM DITYLUM BRIGHTWELLII (BACILLARIOPHYCEAE) UNDER NITROGEN AND PHOSPHORUS LIMITATION AND STARVATION 1 , 1997 .

[45]  D. M. Nelson,et al.  Production and dissolution of biogenic silica in the ocean: Revised global estimates, comparison with regional data and relationship to biogenic sedimentation , 1995 .

[46]  R. Bak,et al.  Effects of grazing, sedimentation and phytoplankton cell lysis on the structure of a coastal pelagic food web , 1995 .

[47]  Y. Ishida,et al.  Killing of marine phytoplankton by a gliding bacterium Cytophaga sp., isolated from the coastal sea of Japan , 1993 .

[48]  R. Bak,et al.  Lysis-induced decline of a phaeocystis spring bloom and coupling with the microbial foodweb , 1992 .

[49]  E. Laws,et al.  Appropriate use of regression analysis in marine biology , 1981 .

[50]  Dongyan Liu,et al.  SURVEY OF THE CHEMICAL DEFENCE POTENTIAL OF DIATOMS: SCREENING OF FIFTY ONE SPECIES FOR a,b,g,dYUNSATURATED ALDEHYDES , 2005 .

[51]  D. Conley,et al.  Annual cycle of dissolved silicate in Chesapeake bay: implications for the production and fate of phytoplankton biomass , 1992 .

[52]  Y. Ishida,et al.  Lysis of Skeletonema costatum by Cytophaga sp. Isolated from the Coastal Water of the Ariake Sea. , 1992 .

[53]  H. Utermöhl Zur Vervollkommnung der quantitativen Phytoplankton-Methodik , 1958 .