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New oxylipins produced at the end of a diatom bloom and their effects on copepod reproductive success and gene expression levels

Chiara Lauritano

a,

*, Giovanna Romano

a

, Vittoria Roncalli

b

, Angela Amoresano

c

, Carolina Fontanarosa

c

, Mauro Bastianini

d

, Federica Braga

d

, Ylenia Carotenuto

a

, Adrianna Ianora

a

aStazioneZoologicaAntonDohrn,VillaComunale,80121Napoli,Italy

bBe´ke´syLaboratoryofNeurobiology,PacificBiosciencesResearchCenter,UniversityofHawaiiatManoa,1993East-WestRoad,Honolulu,HI96822,USA

cDipartimentodiScienzeChimiche,Universita` degliStudidiNapoli,MonteSant’Angelo,80126Napoli,Italy

dIstitutodiScienzeMarineCNR,Castello2737/f,I30122Venice,Italy

1. Introduction

Diatomsareakeycomponentofaquaticfoodwebsandhave traditionally been considered an optimal food source for the reproduction and development of planktonic grazers, mainly crustaceancopepods,and essential in thetransferof energy to highertrophiclevels(asreviewedbyIanoraandMiralto,2010).

Intense blooms that negatively impact the hatching successof calanoidcopepodshavebeendescribedworldwide,includingthe North Adriatic Sea (Miralto et al., 1999, 2003), Gulf of Bothnia (BalticSea;Asketal., 2006)andDabobBay(Washington,USA;

Halsband-Lenketal.,2005).TheNorthAdriaticbloomcanlastfor severalmonths(FebruarytoApril)andismostlydominatedbythe diatomSkeletonemamarinoiwiththephytoplanktonassemblage becoming more heterogeneous toward the end of the bloom (Ribaletetal.,2014).Duringthebloom,S.marinoico-occurswith thecopepodCalanushelgolandicus,acalanoidcopepoddominantin the North East Atlantic and Adriatic Sea (Mauchline, 1998;

Papadopoulosetal.,2005).

Numerousstudieshaveshownthatseveralspeciesofdiatoms producepolyunsaturatedaldehydes(PUAs)andaplethoraofother metabolites,collectivelytermedoxylipins(Cutignanoetal.,2006;

d’Ippolitoetal.,2004,2009;Fontanaetal.,2007a;Wichardetal., 2005),thatareoxygenatedfattyaciddegradationproductswith toxic effects on reproductive processes in crustacean copepods (Fontana et al., 2007b; Ianora et al., 2004) and cladocerans HarmfulAlgae55(2016)221–229

ARTICLE INFO

Articlehistory:

Received18January2016

Receivedinrevisedform11March2016 Accepted11March2016

Availableonline

Keywords:

Oxylipins

Secondarymetabolites Diatoms

Bloom Copepods Geneexpression

ABSTRACT

Diatomsaredominantphotosyntheticorganismsintheworld’soceansandareconsideredessentialin thetransferofenergytohighertrophiclevels.However,theseunicellularorganismsproducesecondary metabolitesderivingfromtheoxidationoffattyacids,collectivelytermedoxylipins,withnegative effectsonpredators,suchascopepods,thatfeedonthem(e.g.reductioninsurvival,eggproductionand hatchingsuccess)and,indirectly,onhighertrophiclevels.Here,amultidisciplinarystudy(oxylipin measurements, copepodfitness, gene expressionanalyses, chlorophyll distribution, phytoplankton composition,physico-chemicalcharacteristics)wascarriedoutattheendofthespringdiatombloomin April2011intheNorthernAdriaticSea(MediterraneanSea)inordertodeeplyinvestigatecopepod–

diatom interactions, chemical communication and response pathways. The results showthat the transectwiththelowestphytoplanktonabundancehadthelowestcopepodeggproductionandhatching success,butthehighestoxylipinconcentrations.Inaddition,copepodsinboththeanalyzedtransects showed increasedexpressionlevelsof key stress-related genes(e.g.heat-shockproteins, catalase, glutathioneS-transferase,aldehydedehydrogenase)comparedtocontrollaboratoryconditionswhere copepodswerefedwiththedinoflagellateProrocentrumminimumwhichdoesnotproduceanyoxylipins.

Newoxylipinsthathaveneverbeenreportedbeforeformicroalgaearedescribedforthefirsttime,giving newinsightsintothecomplexnatureofplant–animalsignalingandcommunicationpathwaysatsea.

Thisisalsothefirststudyprovidinginsightsonthecopepodresponseduringadiatombloomatthe molecularlevel.

ß2016ElsevierB.V.Allrightsreserved.

* Correspondingauthor.Tel.:+390815833221;fax:+390817641355.

E-mailaddress:chiara.lauritano@szn.it(C.Lauritano).

ContentslistsavailableatScienceDirect

Harmful Algae

j our na l ho me p a ge : w ww . e l se v i e r . com / l oc a te / h a l

http://dx.doi.org/10.1016/j.hal.2016.03.015 1568-9883/ß2016ElsevierB.V.Allrightsreserved.

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