Progress in Understanding Harmful Algal Blooms

36 Pages·2012·2.12 MB·English

MA04CH07-Anderson ARI 3November2011 14:18
Progress in Understanding
Harmful Algal Blooms:
Paradigm Shifts and New
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d fro4/23/ 1BiologyDepartment,WoodsHoleOceanographicInstitution,WoodsHole,Massachusetts
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2.4:ed Annu.Rev.Mar.Sci.2012.4:143–76 Keywords
Sci. 201ung Alfr FSeirpsttepmubbelirsh1e9d,2o0n1l1ineasaReviewinAdvanceon redtide,shellfishtoxicity,fishkills,ecogenomics,climatechange
Marine. 2 - Stift TmhareinAen.annunaluRalerveiveiwewofs.MoragrineScienceisonlineat AThbestpruabcltichealth,tourism,fisheries,andecosystemimpactsfromharmful
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Annby Copyright(cid:2)c 2012byAnnualReviews. of many new technologies and approaches for research and management.
Allrightsreserved
This,inturn,isleadingtosignificantparadigmshiftswithregardto,e.g.,
1941-1405/12/0115-143$20.00 ourinterpretationofthephytoplanktonspeciesconcept(strainvariation),the
dogmaoftheirapparentcosmopolitanism,theroleofbacteriaandzooplank-
tongrazinginHABs,andourapproachestoinvestigatingtheecologicaland
geneticbasisfortheproductionoftoxinsandallelochemicals.Increasingly,
eutrophicationandclimatechangeareviewedandmanagedasmultifactorial
environmentalstressorsthatwillfurtherchallengemanagersofcoastalre-
sourcesandthoseresponsibleforprotectinghumanhealth.Herewereview
HABsciencewithaneyetowardnewconceptsandapproaches,emphasizing,
wherepossible,theunexpectedyetpromisingnewdirectionsthatresearch
hastakeninthisdiversefield.
143
MA04CH07-Anderson ARI 3November2011 14:18
INTRODUCTION
Virtuallyeverycoastalregionoftheworldisaffectedbyharmfulalgalblooms(HABs)commonly
calledredtides(Figure1).Sincethelattertermerroneouslyincludesmanybloomsthatdiscolor
thewaterbutcausenoharm,andalsoexcludesbloomsofhighlytoxiccellsthatcauseproblems
atlow(andessentiallyinvisible)cellconcentrations,scientistspreferthetermHAB.
HABsaremostcommonincoastalmarineecosystems,buttheymayalsoaffecttheopenocean
as well as brackish or freshwater ecosystems. Most HAB phenomena are caused by blooms of
microscopicalgaeorphytoplankton,includingcertaincyanobacteria(blue-greenalgae),although
the term also applies to harmful blooms of macroalgae (seaweeds). HAB events are typically
associatedwithrapidproliferationand/orhighbiomassaccumulationoftoxicorotherwisenoxious
microalgaeattheseasurfaceorinthewatercolumn,butevenlowcellnumbersofhighlytoxic
planktonicspeciesoraccumulationsofcellsonbenthicsubstratesmaycauseproblems.
The HAB designation is a societal concept rather than a scientific definition—blooms are
ualreviews.orgonal use only. cocthaorurntososeuicdgioelhlmrnetepdhsoetsnofaeofinnotdtdtshdoweefaeHatbqhA.uoHBaftcuificrmisethaec,nroissoecynaosbtniefisrmtudhmsse.,yeSmrcosaamumosefmeHsieanaAljsfuB,oraoysndptdeoccoohietnuhstmeaarmraenmitnhoaaerxtaiiengldteehnbloiiyfcretas,honoecdfsitoepeerntocoovdxinuianoctsemombxicliaoniyontmtarealssrnoetshsfbteasert,
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m w12. andskinirritationwhenreleasedfromtoxiccells.
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Figure1
NoctilucascintillansredtideatapristinetourismresortofftheeastcoastofTasmania,southeastAustralia,
believedtorepresentarecentclimate-drivenrangeextensionfromSydneycoastalwaters.(Source:Erin
Watson,UniversityofTasmania.)
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144 Anderson Cembella Hallegraeff
MA04CH07-Anderson ARI 3November2011 14:18
injuriousandevenlethaltofinfish,especiallywhenheldcaptiveinaquacultureoperations.Non-
toxicHABscausedamagetoecosystems,fisheryresources,andrecreationalfacilities,oftendue
tothehighbiomassofaccumulatedalgae,whichcancreatenoxiousscumsandfoam,shadeother
phytoplanktonandseagrassbeds,andcausefaunalmortalitiesviadecayandoxygendepletion.
ThediversityofHABspeciesandtheirimpactspresentsasignificantchallengetothoserespon-
sibleformanagementofcoastalresourcesandtheprotectionofpublichealth.HABsarecomplex
oceanographicphenomenathatrequiremultidisciplinarystudyandmethodologiesrangingfrom
molecular and cell biology to large-scale field surveys, numerical modeling, and remote sens-
ing.Ourknowledgebaseandabilitytounderstandandmanagethesephenomenahaveexpanded
greatlyinthepastseveraldecades.Consequently,therearemanyexcellentbooksandpapersthat
reviewthisprogress(e.g.,Hallegraeff1993,Andersonetal.1998,Hallegraeffetal.2003,Grane´li
&Turner2006).Thepurposeofthiscontributionisnottoduplicatetheseefforts,butratherto
highlightnewdiscoveries,technologicaladvances,andparadigmshiftsinourviewofHABs.
ws.orgonly.
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alrenal For many years, HAB research was conducted in relative isolation. Individual researchers or
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Rev. B631 withoutsufficientlong-termdata.Withthebenefitofhindsightwecanhighlightregionalcases
u. WI whereexpansionhasoccurredandprobablemechanismscanbeidentified.OneexampleofaHAB
nny expansioncausedbystormsorothernaturaleventsisintheGulfofMaine,UnitedStates,where
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in1972amajortropicalstormstimulatedanddispersedalargeAlexandriumredtidethroughout
theregion.Thisledtothedepositionofdormantcystsinwatersthathadvirtuallynohistoryof
paralyticshellfishpoisoning(PSP),butthathavehadannualoutbreaksnearlyeveryyearthereafter
(Anderson1998).Anexampleofshipballastwater–mediatedrangeexpansionistheintroduction
of the toxic dinoflagellate Gymnodinium catenatum into Tasmania in the mid-1970s (see review
of molecular, plankton, and cyst evidence in Bolch & de Salas 2007), from where it has since
dispersedtomainlandAustralia.
Itisalsoclearthatsomeaspectsoftheapparentexpansionareduetoheightenedandmore
effectivescientificandregulatoryattentiontotheproblem.Ineffect,wearebetterdefiningthe
boundariesofaproblemwhosescalewehadnotfullyunderstoodorappreciated.Aprominent
exampleinthisregardisassociatedwiththeamnesicshellfishpoisoning(ASP)syndrome,which
causedmorethanahundredcasesofhumanillnessandseveraldeathsin1987afterconsumption
www.annualreviews.org • ProgressinHABScienceandManagement 145
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Figure2
Distributionofeventsupto(a)1970and(b)2009,respectively,whereparalyticshellfishpoisoningtoxins
weredetectedinshellfishorfish.(Source:U.S.NationalOfficeforHarmfulAlgalBlooms.)
ofmusselsfromAtlanticCanada(Batesetal.1989).ThecausativeagentofASPwaspromptly
identifiedastheneurotoxindomoicacid,producedbyseveralspeciesofmarinediatoms.Following
thisdiscovery,novelanalyticalmethodswerequicklyintroducedintotheregulatorystructureand
usedforscientificresearch.Afewyearslater,theunusualmortalityofseabirdsinCalifornialed
totheidentificationofdomoicacidasthecause,withthatdiscoveryattributeddirectlytoreports
fromthe1987Canadianevent(Worketal.1993).ThesubsequentdocumentationofASPtoxins
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146 Anderson Cembella Hallegraeff
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yearafteryearalongmuchoftheWestCoastoftheUnitedStates(Andersonetal.2008)leaves
no doubt that the toxin had been present in those waters for many years but had never been
properlyidentified.Twenty-fiveyearsaftertheAtlanticCanadianpoisoningevent,ASPisnowa
recognizedpublichealththreatinmanycountries.
A number of researchers have investigated potential linkages between HAB expansion and
eutrophication(e.g.,Smayda1989,Andersonetal.2002,Glibertetal.2008).Asdiscussedbelow,
in some instances, the linkage is clear and unequivocal, whereas in others, it is subtle or even
nonexistent(Andersonetal.2008).
KEYDEVELOPMENTSINHARMFULALGALBLOOM
SCIENCEANDTECHNOLOGY
The significant public health, tourism, fishery, and ecosystem impacts from HABs have led to
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aden 0 applied to the local situation. Resolution of the species concept for harmful algae has become
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Rev. B631 nal transcribed spacer (ITS), or cytochrome c oxidase subunit 1 (cox1) genes. Ribotyping and
u. WI application of conservative single-gene markers such as rDNA have been valuable in resolving
nny taxonomicandphylogeneticissuesamongHABspecies,butrevealingcrypticdiversityatthein-
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traspecificandpopulationlevelsrequiresfinerdiscrimination.Forexample,molecularsequencing
ofstrainsinculturerevealedthatthewidelyreportedcosmopolitancoastaldiatomSkeletonema
costatum includes five distinct morphotaxa, at least some of which have discrete regional distri-
butions and distinct ecophysiological characteristics (Kooistra et al. 2008). The dinoflagellate
generaGymnodiniumandGyrodiniumwereinitiallyseparatedmorphologicallyonthebasisofgir-
dledisplacement;withsupportfromanewmolecularphylogeny,thesegenerawereredefinedon
thebasisoftheshapeoftheapicalgroove,allowingforthecreationofthefamilyKareniaceae
forthefucoxanthin-containing,fish-killingdinoflagellategeneraKarenia(10+spp.nowknown),
Karlodinium (8 spp.), and Takayama (6 spp.) (Daugbjerg et al. 2000, de Salas et al. 2008). This
combinationofimprovementsinmorphotaxonomycoupledwiththedevelopmentofmolecular
probes (see below) also led to the new recognition that what were thought to be monospecific
KareniabrevisredtidesinFloridaareinfactoftenmultispeciesblooms(Steidingeretal.2008).
www.annualreviews.org • ProgressinHABScienceandManagement 147
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4e (cid:2) (cid:3) (cid:4) (cid:5) (cid:6)
1W RNAsequences.Blackarrows( , ,and )indicateputativenaturaldispersal,whereasgrayarrows( and )suggesthuman-
2.4:ed assisteddispersal.(ModeledafterScholinetal.1995,RuizSebastia´netal.2005.)
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nny Anderson 1994, Scholin et al. 1995; Figure 3). Morphologically indistinguishable populations
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thuscanhidecrypticgenotypes,someofwhichareconsistentlytoxicwhereasothers(European
andTasmanianribotypes,nowtermedGroupsIIIandV;Lillyetal.2007)aremostlynontoxic.
Insuchcasesitiscriticalthatmolecularprobesusedinshellfishandphytoplanktonmonitoring
programs discriminate between ribotypes rather than simply morphospecies. On the basis of
rRNA studies the appearance of the temperate Asian (Group IV) ribotype of A. tamarense in
1983intheMediterraneancouldonlybeexplainedbyhuman-assistedintroduction(Lillyetal.
2002). However, when Masseret et al. (2009) examined these same strains using hypervariable
microsatellitemarkersthisrevealedrelationshipsthatwerenotapparentfromrRNAsequences
studiesonthesamegroup.Mediterraneanpopulationswereshowntobeadistinctlineage,and
thereforeotheroriginsmustnowbeexplored.
Thesameprinciplesapplytotheciguatera-causingbenthicdinoflagellategenusGambierdiscus.
Until recently, only a single species of G. toxicus was recognized even though a >100-fold
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148 Anderson Cembella Hallegraeff
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variation in toxicity and variations in ciguatoxin profiles have long been known. Molecular
sequencing in combination with a reexamination of morphotaxonomy allowed discrimination
of12species,ofwhich5areendemictotheAtlantic(includingtheCaribbean/WestIndiesand
GulfofMexico),5areendemictothetropicalPacific,and2(G.carpenteriandG.caribaeus)are
circumtropicallydistributed.ThedifferencesinGambierdiscusspeciescompositionintheAtlantic
and Pacific correlate with structural differences in the ciguatoxins accumulated in Atlantic and
Pacificfish(Litakeretal.2009)andwithdifferencesinthesymptomsofpoisonedindividuals.
Becauseoftheapparentcontinuityoftheworld’soceans,similarhydrologicalenvironmentsin
differentoceanstendtohavemorphologicallysimilarphytoplanktonassemblages(referredtoas
latitudinalcosmopolitanism;Taylor&Pollingher1987),andmanyscientistshavelongclaimed
thatmarineprotistshavehadampleevolutionarytimetoreachandinhabitallsuitableenviron-
ments. Molecular taxonomy is, however, increasingly contradicting the dogma of widespread
cosmopolitanismofmicroalgae.Genetic,reproductive,andmorphologicalvariationin193global
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alrenal only Clade I was recovered in all global locations in temperate coastal waters (Casteleyn et al.
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Rev. B631 EcogenomicsandGeneExpressionandFunction
u. WI Therecentdevelopmentandapplicationofadvancedtechnologiesfromthegenericallydefined
nny “-omics”sciences(genomics,transcriptomics,proteomics,metabolomics)coupledwithbioinfor-
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maticsplatformshasalreadyprovideddeepandoftenrevolutionaryshiftsinunderstandingthe
ecology and evolution of HAB species and bloom dynamics. Although the field remains in its
infancy, noteworthy contributions to HAB research have already been made in addressing the
followingfourquestions:(a)WhatarethephylogeneticrelationshipsamongHABtaxathatac-
countfortheirpatternsofevolution?(b)Whatarethebiosyntheticgenesandmetabolicpathways
involvedinbiosynthesisoftoxinsandotherallelochemicals?(c)Whatarethepatternsofdiver-
sityatthepopulationandspecieslevelwithinandamongnaturalblooms?And(d)whatarethe
mechanismsofgeneexpressionandregulationwithincellsofHABtaxaandthatgoverninter-
and intraspecific responses to putative competitors and/or grazers? The ecogenomic approach
to HAB research provides the opportunity to quantify functions and interactions of organisms
(cellstopopulations)atanecosystemlevel—relevanttocausesandconsequencesofHABs—by
determiningtherelationshipstoecologicalandevolutionaryprocesses.
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Conventionalgenomicsisoftenbaseduponthesequencingandannotationofwholegenomes,
withsubsequentbioinformaticfocusonthestructureandfunctionofkeygroupsofgenes.This
approachhasbeensuccessfullyappliedtoelucidatethecomparativestructureandfunctionofgene
clustersforthetoxinanalogsofsaxitoxinsandmicrocystinsoftoxigenicHAB-formingcyanobacte-
ria,suchasRaphidiopsisbrookiiandCylindrospermopsisraciborskii(Stuckenetal.2010),withgenome
sizes of <4 Mb. The much larger size of the nuclear genomes of eukaryotic microalgae has
severely restricted the whole-genome sequencing approach—there is only one published fully
sequencedandannotatedclosedgenomeforaHABspecies,thatofthebrowntidespeciesAureo-
coccusanophagefferens(Gobleretal.2011).ThispaucityofwholegenomesforHABtaxaisbeing
addressed,albeitnotsystematically.Adraftgenome(300Mb)hasbeengeneratedforthetoxigenic
diatomPseudo-nitzschiamultiseries(Armbrust2009),whichproducestheneurotoxindomoicacid,
andtheexpectedpartialannotationisexpectedtoyieldinsightsintopathwaysoftoxigenesisand
ironacquisitionrelevanttobloomdynamics.Nevertheless,mosttoxigenicHABtaxabelongto
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Marine. 2 - Stift iwshreenstrtihcetecdobrryestphoenfadcintgthmatRoNnlAyaisferaxcptrieosnseodf,tthheistraapnpsrcoraibchedhgasenboemeneeisffesuctrivveeylyedu,saenddtothiednenotniflyy
Rev. B631 genetranscripts,discovernewgenes,anddeterminesequencehomologyforvariousHABtaxa.
u. WI ESTdatabasesarenowextensiveandrepresentativeofawidediversityoforganisms,including
nny the HAB species Alexandrium fundyense (Hackett et al. 2005), A. catenella (Uribe et al. 2008),
Ab
A. ostenfeldii (Jaeckisch et al. 2008), A. minutum (Yang et al. 2010), Karenia brevis (Lidie et al.
2005),Chrysochromulinapolylepis(Johnetal.2010),andPrymnesiumparvum(LaClaire2006),with
moreinthepipelineawaitingfurtherannotationandverification.
AnESTlibraryconstructedforthedinoflagellateA.minutum(Yangetal.2010)combinedwith
theapplicationofanoligonucleotidemicroarrayuncoveredthepresenceof192genesthatwere
differentiallyexpressedbetweentoxicandnontoxicstrainsofthisspecies(Figure4).Neverthe-
less,althoughpotentialcandidategenesweredetectedforpossibleinvolvementingrowthregu-
lationand/ortoxinbiosynthesis,noconfirmedhitsforthePSPtoxinbiosyntheticgenesfoundin
cyanobacteriaweredetected.AmajoradvanceinthisregardwasreportedbyHackettetal.(2011),
whoassembledcomprehensivetranscriptomedatasetsforseveralsaxitoxin-producingdinoflag-
ellatesandarelatednontoxicspecies.Theyidentified265putativehomologsof14cyanobacterial
saxitoxinsynthesisgenes,includingallofthegenesdirectlyinvolvedintoxinsynthesis,asdescribed
· ·
150 Anderson Cembella Hallegraeff
MA04CH07-Anderson ARI 3November2011 14:18
Microarray design
Designed using Agilent eArray platform
60mer oligonucleotides ensure high-binding, organism-specific stringency
Contig from overlapping ESTs

ESTs = raw sequences
>Alexandrium-C-a-01a02.m13f 1026 letters
ws.orgonly. T T T T TCTCTGTATATTTCTCTATATGTGTATATATATTTATGTACGAGACCTGGGCCAGACCAAAAAATAGATACACGCGCAGGCGTCCCAAAAGACCTAAGTGGGTGGCGCTACTCCAAGCCTGAACCGCTGAACGCCTCGGCCGTGCCGGCGGCTTCCTAGCAG
alrevienal use CCAGTAGCGTGCCCCGGGGACAGCGCGCGCCAGAACTGCCCGACGCCAACCCCCCAGAACAGACAATGAGCAGACGACGGGGGGAACGGAGGCTGTACTACCAAACGGGACCTGCCGGGGTCCTCCTTGCTCGGCCCAGAATGTGCCCGATCACGAGCATCACCATCAGGTCACCGCACGTTGGCAGAAGGGTCGCTCCCGGAGTTTAGATGCCGCGGCCACAGTCGCATAATAAGAAC
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ns TGGACGGAGCTCTTGGACTCGATGCGCGGGATGATCCTGCCCCAAACCTCGGGGTGGCTCAGGATGTCGGTGGACTTCGC
m www.an12. For per CGGAGGGGGGATCCGCAGCGCCCTGACCCCTGCTCCCCGGTGGGCGCACCCATGTCTCTGGCCTGGGCTGCTGAATAGGGACCAGCCCGCTGTACAGTGCTGCCAAACCAGACATCTGGCTTTCCGGGCGCGCCCTGTGTTTTGGGTTTGGTGGGGCACAAAAGCCCGGGCTATGGGTCTCCCCTCCCCCCGTCTTTTGTATTTTGGCGCCCCAAAGGGATTTTTTCACACCCCATACCCAGCGGGGTCCCGGGGACAGGGGGAGCCCTGCGCCCGGTGCCCCGCGTTTCGGGCCCCACACCATCCCGGAGTTCCGATACGTGTGAGCTACCGTGAGGGTGGTCGGCTGGAGTCTGGAGCTGTGCAATGAGCAGGGAGGCGGGTTGTCCACCCACAC
d fro4/23/ TTTTCCTCCGGCTTTCGCTCATGGAAGACCTATTGCATATCCCTAGGGCTCAGCGCCTCGCGATAATTCTTCGCCGACACTAATCGCGTTTTCCCCCGCGGGGGTCTCGCGCGTGTTCTCGGGGTCTCAAAACGCGGTGTGAGAGCCGTTTTACCACGCGGAGGAAGTGTGGAACACCCTATGCTTCCCCTGTTGGTGTGCGTTCGGCCAATGGCCCTGGT
aden 0 GCAGCAGGCAGTGCTTGTACGTGCCCTCATTCCCGGCCCCCCAATTGGAACCGGCCGGGGCCCCCCAAAACCGGAAGGGGGGGGGAAG
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Sci. 201ung Alfr FOilgiguorneu4cleotidemicroarrayforstudiesofgeneexpressioninthetoxigenicdinoflagellateAlexandriumminutum.Themicroarraywas
Marine. 2 - Stift dseeqruiveendcefrtoamgst(hEeStTrasn)s(cYriapntgometicala.n2a0l1y0si)s.oGfetnheeecxoprrreessspioonndpinatgtecronmspcalenmbeendtaertyerDmNinAed(cfrDoNmAa)uatonmdaseteqduescnacninnginogfo>f1t5h,e00co0loexrppraetstseerdn
Rev. B631 gMeanreirnaeteRdevsieaarhcyhb.r)idizationandfluorescencelabeling.(AdaptedafterimagesuppliedbyI.Yang,AlfredWegenerInstituteforPolarand
u. WI
nny
Ab
by Kellmann et al. (2008). Putative homologs of four proteins grouped closely in phylogenies
withcyanobacteriaandarelikelythefunctionalhomologsofsxtA,sxtG,andsxtBindinoflagel-
lates.However,thephylogeniesdonotsupportthetransferofthesegenesdirectlybetweentoxic
cyanobacteriaanddinoflagellates.Thesaxitoxinsynthesispathwaywaslikelyassembledindepen-
dently in the distantly related cyanobacteria and dinoflagellates. The independent evolution of
thesaxitoxinbiosyntheticgenesinthesetwoecologicallydistinctgroupsoforganismssuggests
thatthistoxinmayconferabenefittoproducersthatwedonotyetfullyunderstand.
In dinoflagellate species producing polyketide toxins, including spirolides (Jaeckisch et al.
2008)andbrevetoxins(Monroe&VanDolah2008),searchstrategiesbasedonESTorcDNA
librariesweresuccessfulinidentifyingarangeofPKSsfromhighsequenceconservationinseveral
PKSdomains.Yetitremainsunclearwhichofthesegenesareresponsibleforproductionofthe
correspondingtoxins.
www.annualreviews.org • ProgressinHABScienceandManagement 151
MA04CH07-Anderson ARI 3November2011 14:18
Sequence analysis based upon a normalized cDNA library of the fish-killing haptophyte
C.polylepis(Johnetal.2010)revealedseveralgenesputativelyrelatedtotoxinsynthesisand13
putative PKS-related gene sequences. Semiquantitative reverse-transcription polymerase chain
reaction(RT-PCR)followingexpressionofPKSgenesoverthephotocycleofsynchronizedcul-
turesyieldedthefirstexpressionofPKSgenesinatoxichaptophyte.
ThedevelopmentandapplicationofcDNAandoligonucleotidemicroarrays—well-established
technologiesinbiomedicalandenvironmentalstudies—provideaquantumleapforwardforHAB
research.Patternsofgeneexpressionandregulationcanbescreenedsimultaneouslyusingthou-
sandsofgeneprobesspottedonthe“labonachip.”Wecannowsurveygenesrelatedtogrowth
dynamics, toxigenesis, interspecific interactions, and ecophysiology, to name but a few of the
processesunderstudy.Inanovelstudyofpredator-preyinteractionsandpossibledefensemech-
anisms,anEST-basedoligonucleotidemicroarrayforthedinoflagellateA.minutumwasusedto
demonstrateashiftingeneexpressionof14genesinresponsetoacopepodgrazer,concomitant
ws.orgonly. withTraannisnccrripetaosemiincdainnaolyflsaigseilsl,atheocweellvteorx,insucbojencttentot(aYacnrigtiectalall.im20it1a0t)io.n, as this type of analysis
vieuse applies only to expression at the transcriptional level. Many key genes may be posttranslation-
alrenal allymodified,therebyaffectingthestructureandfunctionofproteins.Infact,ahighdegreeof
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d from www.ann4/23/12. For pers pfecaotoimlasuAtl.tprnre2laae0nolmy1sfs0lemia)nst.iitoc—ornfocaatalrhnmreaoaypddardinfioratceelasyostsimoitshnete—ooficcsobosunimoefispryormnifstihepnxeogptsirtcttehrsgaeseninossneltarptouirfocotntudoaruxleicnmtsa-osnmpddeiaficyficufibanctecigotaienocnnoebnsuottirfnihbAtauhslteeixnnaegonntfdtairorcifeuttomerpnr(inYobtaetenheinnge
aden 0 applied to HAB taxa. Earlier proteome analysis was dependent upon generation of a “protein
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Downlnstitut fitonbgeerapbrlientt”obryestowlvoe-dseimveernasligornoaulpgselofelpercotrteoipnhsoarsetsaisx.oBnyomthiicsmmaertkheords,,dCihscarnimetinaalt.i(n2g00to5x)icclvaeimrseuds
3-176. gener I nspornatyoixoicnisztartaiionns(oEfSAI.)manindumtuamtr.ixT-hasissiastpepdrolaascehrhdeassobrepetniocno/miopnliezmatieonnte(dMoArLsuDpIe)rosefdwehdobleyperleoctetrion-s
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Sci. 2012.4:1ung Alfred W osa2pn0red0pc9emt)pr,ootaimddneedeatdarcinytgia(oelesny.tgssoi.sf,foCotlhflhoetahwdneienedpotlbaflaysla.tgdi2dee0lp0lnar6oto)ev.toemPosremeotqateeubooeomnflicttihiecnesygheFosalsorsorpptireodopxavitrniidedodeendmtiavdaaheslsuudmfiainbnaolgneflelirainpvgfereoirlrnlcmatetinealltgKiloib.nnyberot(eanYvniotsdhudeenmegetefmefcettaceastdlss.
Marine. 2 - Stift alongeicleacltsruocncetsrsaninsfierronpruottieliizna(tpiolans(tNocoysaennikno)ienthael.ri2t0ed06f)r.oNmegvreerethnealelgsas,emthuacthmparyomcoisnetrriebmutaeintsoteocboe-
Rev. B631 fulfilledintheapplicationofproteomicstostudiesofHABecophysiologyandbloomdynamics.
u. WI Thestudyoftheprofileoflow-molecular-weightmetaboliteswithincellshasyettobeapplied
nny toHABresearchinaconcertedfashion.Therearenoapparentmajortechnologicalimpediments,
Ab
and the metabolomics approach has already been successfully applied to the dinoflagellate en-
dosymbiontSymbiodinium(reviewedinGordon&Leggatt2010).AmongHABspecies,metabolic
fingerprintingofK.brevisextractsbymassspectrometrywasnotsuccessfulinidentifyingspecific
compoundsresponsibleforallelopathy(Princeetal.2008).Thisfrontierfieldislikelytobemore
fruitfulwhenmorecomprehensivespectrallibrariesbecomeavailableandasstructural-functional
relationshipsofthemetabolitesarebetterdefined.
DiversityandInteractionofPhycotoxinsandAllelochemicals
MuchoftheattentiondirectedtowardsHABs—bysocietyingeneral,socioeconomicinterests,
regulatoryagencies,andthescientificcommunity—hasbeenfocusedonthefactthatmanyHAB
taxa produce potent toxins with ecosystem and human health consequences. Regulatory and
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152 Anderson Cembella Hallegraeff