Uptake Rates as Fundamentals
of Iron Availability to
Phytoplankton
Yeala Shaked
Interuniversity Inst. for Marine Sciences, Eilat
Hebrew University, Jerusalem, Israel
GEOTRACES Synthesis Workshop Aug 1-4th 2016
Whatdeterminesthebioavailability
ofirontophytoplankton?
FundamentalsofFeavailability
Chemicalreac(vityofFespecies&
compa(bilitywithuptakesystems
PathwaysandratesofFe
acquisi(onbyphytoplankton
Interac(onsandecosystemprocesses
!  Feinputs,recycling&residence
(mes
!  Phytoplanktonphysiology,
biochemistryandspeciescomposi(on
!  Chemical&photochemical
transforma(onsofFe
!  Foodwebinterac(ons
!  Bio-mediatedtransforma(onsofFespecia(on
!  Physicaleffects(e.g.light,temperature)onphytoplankton
physiology&ecologyandFespecia(on&fate
ShakedandLis,2012
FundamentalsofFeavailability
Emphasisonkine(cs-Usinguptakerateconstants(Kin)forcomparisons&
extrapolaBontotheenvironment
Chemicalspecia(onandkine(cs
Uptakepathways&rates
FeL
Par(cles Colloids Dissolved
Organic Inorganic
Fe(III)
Fe(II)
Fe(II)
Lis,Shaked,Kranzler,KerenandMorel.2015.ISME
Ironbioavailabilitytophytoplankton:anempiricalapproach
FeL, Fe’
T.weisfloggii
T.psuedonana
Syenchococcus
E.hux
Psuedo-nitzschia
Thalassiosira
P.micans
N.oculata
P.calceolata
Anabaena
Compiling5decadesofuptakestudies:
• Dophytoplanktondifferintheirabilityto
acquireFe?
• Aretherelower/upperlimitstouptakerates?
P.tricornutum
• WhichFecomplexesaremore/lessavailable?
Phaeocys:s
P.minimum
• CanlabstudieshelpdefineFeavailabilityin
naturalenvironments?
Chaetocerous
T.antarc:ca
Trichodesmium
Phaeocys:s
Thalassiosira
Psuedo-nitzschia
T.weisfloggii
T.psuedonana
Syenchococcus
E.hux
Phaeocys:s
Psuedo-nitzschia
Thalassiosira
P.micans
N.oculata
P.calceolata
Anabaena
Compiling5decadesofuptakestudies:
18studiesfrom13researchgroups
Shorttermandlongterm(growth)uptake
15phytoplanktonspeciesand28strains
~25%our
5majordivisions(Euks&Cyanos)
owndata
16Fe-substrates
P.tricornutum
Thalassiosira
StringentdataselecBoncriteria
(Felimitedcells,logphase,[Fe]belowthatofVmax,etc..)
P.minimum
Chaetocerous
T.antarc:ca
Trichodesmium
Phaeocys:s
Psuedo-nitzschia
Uptakeratebasics&selec(oncriteria
Steadystate
U
U
Felimited
U
U
Fe-replete
Time(hrs)
U
IntracellularFe
Uptakeratebasics&selec(oncriteria
Fe
Fe
Fe
Fe
Fe
Fe
Fe
[Fe]>Kρ
Fe
X2
IntracellularFe
Fe
Uptakerate
Vmax
Time(hrs)
Sub-saturaBon
FeconcentraBon
Fe
Fe
Uptakeratebasics&selec(oncriteria
Fe’
Fe’
Fe
Fe
Fe’
Fe’
StrongLigands–FeDFB
Fe'
Fe
InorganicFe–limitedbylowsolubility
Fe'
InorganicFe–bufferedbyEDTA
Fe
Fe'
Fe'
UptakeofinorganicIron(Fe')
U U
growth(days)
U
U U
U
U
Smallcells
U
Largecells
U U
shortterm(hrs)
UptakeofinorganicIron(Fe')in/S.A)is
Surfaceareanormalizeduptake(k
similaramongallstudiedeukaryotes
Regressionline:
DirectproporBonalitybetween
parametersandR2=0.94
UptakeofsiderophoreboundFe(FeDFB)
Regressionline:
DirectproporBonalitybetween
parametersandR2=0.9
UptakeofFe‘andsiderophoreboundFe(FeDFB)
Surfaceareanormalizeduptake(Kin/S.A)issimilaramongallEuks
forFe’andforFeDFB.ButFe’>>FeDFB(x1000)
Uptake rate / [Fe Sub]
Fe‘(inorgan
ic)
FeDFB
(Fe-siderophore)
Thebioavailabilityenvelope
Empiricalresultsoflabstudieswitheuks
surfacearea(μm2)
1
10
100
1000
10000
1.E-07
kin(Lcell-1hr-1)
Uptake rate / [Fe Sub]
1.E-06
1.E-08
Fe'
1.E-09
1.E-10
1.E-11
1.E-12
1.E-13
Comparewithotherorganisms,field
studies,differentFesubstrates…
kin/S.AissimilaramongallstudiedorganismsforFe’
Thebioavailabilityenvelope:cyanobacterialuptake
surfacearea(μm2)
FeDFBuptakeofcyanosisslowerthanineuks
0.1
1.E-05
1.E-06
kin(Lcell-1hr-1)
1.E-07
1.E-08
1.E-09
1.E-10
1.E-11
1.E-12
1.E-13
1.E-14
1.E-15
1
marinesyn
BrackishSyn
Synechosys)s
Proch
Tricho
Anbn
10
100
1000
10000
s
e
t
o
ry
a
k
u
F'ee
FeDF
es
t
o
y
ar
k
u
e
B
Thebioavailabilityenvelope:comparingFesubstrates
surfacearea(μm2)
1
10
1.E-06
1000
10000
Fe'
1.E-07
kin(Lcell-1hr-1)
100
1.E-08
B
F
FeD
1.E-09
1.E-10
1.E-11
1.E-12
1.E-13
e
r
o
M
le
b
a
l
i
va
b i oa Less
siderophore
freshferrihydrate
saccharide
naturalligands
porphyrin
Fe-dPS
organicamine
humicacid
Thebioavailabilityenvelope:
comparingFesubstrates
FeDFB
MorebioavailableFe
substrates
LessbioavailableFe
substrates
log(kin/S.A)
Fe’
ConclusionsandImplica(ons
"  Feuptakeratesofdefinedsubstratescanbepredicted
accordingtocellsize.
"  Wepresentaconvenientframeworkforaddressing
bioavailabilitybycomparingacrossFe-substratesand
organisms.
ConclusionsandImplica(ons
# Allphytoplanktonarelimitedbythesame
fundamentalphysical,chemicalorbiochemicalfactors.
Uptakesystemshaveevolvedtooperateattheir
maximalefficiency.
# Phytoplanktonmayemployasimilarironuptake
mechanism:reducBveFeuptake
Experimentaldatafor~10cyanosand~30euks!!
#  Ifphytoplanktoncannotfurtherincreaseuptakerates,
acompeBBveadvantageinFe-limitedwatersmustbe
gainedthroughalternaBvemeans.
Decreasecellsize,decreaseFedemands,usealternaBve
Fesources
AvailabilityofSolidPhaseFetoPhytoplankton:
Definingmajorfactorsatplay
Whichphysico-chemicalformcanthecellaccess?
Colloidal/Par(culate
(directlyingested)
Dissolved
ThewholepFepoolisavailable
(generatedfromtheparBcles)
Howsolubleisthemineral?(chemical
reacBvity,[ligand],lightetc…)
Cancellsenhancemineraldissolu(onrate?
Availabilityextractedfrom
solubility&dissolu(onrates
Addbio-mediateddissolu(on
" RemovingFe’(shikingequilibrium)
" AcBvedissoluBonbyphytoplankton
" Team-upwithbacteria(siderophores)
Mineralresidence(meinupperwater
Longer-availability
CanphytoplanktonkeepmineralFeattheoceansurface?
Dust-Fecapturingandmodifica(onbynaturalTrichodesmium
Rubinetal.2011
Ydistance(mm)
CenteringofFe-richdust
00.20.40.60.81.01.21.4
Dust-Fecapturingandmodifica(onsbynaturalTrichodesmium
InsituassociaBon
withFe-rich
parBcles
00.20.40.60.81.01.21.4
Xdistance(mm)
Rapid&significant
FereducBon
Fe(II)
SynchrotronstudywithSaBshMyneni
SensingofFeinpar(clesbyTrichodesmium
t0
1hour
1.5hour
24hour
Aveof9Exps
Naturaldust
30coloniesineach
Acidcleaneddust
Fecoateddust
Index
3.0
2.8
2.6
2.4
2.2
2.0
1.8
1.6
1.4
1.2
1.0
InteracBon Movement RetenBon
SensingofFe
SensingofFeinpar(clesbyTrichodesmium
t0
1hour
BiogenicSilica
Quartz
3.0
2.8
Shortterminteraction
1.5hour
24hour
Fecoatedbiogenicsilica
Fecoatedquartz
2.6
2.4
2.2
2.0
1.8
1.6
1.4
1.2
1.0
1
1.2
1.4
1.6
1.8
2
2.2
2.4
Overnightretention
2.6
2.8
3
Dust-Fecapturingandmodifica(onsbynaturalTrichodesmium
Lowlevelassayfor55Fe-oxdissoluBonwithSid
6.0E-09
5.0E-09
Fewithincells
DissFewithcells
DissSid-Fe(abio(c)
4.0E-09
Feconc
(M) 3.0E-09
2.0E-09
1.0E-09
0.0E+00
18-Nov
9-Dec 16-Mar 17-Mar 19-Mar 28-Mar 4-Apr
10-Apr 14-Apr
Dust-Fecapturingandmodifica(onsbynaturalTrichodesmium
Bio-mediated55Fe-oxdissoluBon
6.0E-09
5.0E-09
Fewithincells
DissFewithcells
DissSid-Fe(abio(c)
4.0E-09
Feconc
(M) 3.0E-09
2.0E-09
1.0E-09
0.0E+00
18-Nov
9-Dec 16-Mar 17-Mar 19-Mar 28-Mar 4-Apr
10-Apr 14-Apr
Dust-FeuptakebynaturalTrichodesmium
AssistedbyBacteria
Uptake&Dissolutionrates
(M/d)
1.E-09
Trichoupt
Bactupt
dissolution
MineralFe
8.E-10
L Fe
L
?
4.E-10
BACTERIA
0.E+00
-Sid
+Sid
55Fe-Ox,Naturalcolonies,RedSea,Mar2016
TRICHODESMIUM
PhytoplanktonmayacBvely
mineFefrommineralsand
effecttheirfateintheocean
Thankyou