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~ i J o u rn a l f

m a g n e t i cm a t e r i a l s

EL SE V IER Journal of Magnet i sm and Magnet ic Mater ia ls 149 (1995) 279-286

R e man e n c e me as u r e me n t s on i n d i v i d u a l magn e t o t ac t i c b ac t e r i a

u s i n g a p u l s e d m agn e t i c f ie l d

I e t j e P e n n i n g a a , H e n d r i k d e W a a r d a , B r u c e M . M o s k o w i t z b ,

D e n n i s A . B a z y l i n s k i c , R i c h a r d B . F r a n k e l d ,,

a

Department o f Physics, Un iversity of Groningen, Nyenborgh 4, 9747 AG Groningen, The NetherlandsInstitute for R ock M agnetism and Department o f Geology and G eophysics, University of Minnesota, Minneapolis, MN 55455, USA

c Marine Science C enter, Northeastern U niversity, East Point , Nahant, MA 01908, USA

d Department o f Physics, Cali fornia Polytechnic State Universi ty, San Lu is Obispo, CA 93407, USA

Received 4 Novem ber 1994; in revised form 10 January 1995

Abstract

W e d e s c r i b e p u l s e d - m a g n e t i c - f i e l d r e m a n e n c e m e a s u r e m e n t s o f i n d i v i d u a l , k i l l e d , u n d i s r u p t e d c e l l s o f t h r e e d i f f e r e n t

t y p e s o f m a g n e t o t a c t i c b a c t e r i a . T h e m e a s u r e m e n t t e c h n i q u e i n v o l v e d t h e o b s e r v a t i o n o f a l i g n e d , i n d i v i d u a l m a g n e t o t a c t i c

b a c t e r i a w i t h a l i g h t m i c r o s c o p e a s t h e y w e r e s u b j e c t e d t o m a g n e t i c p u l s e s o f i n c r e a s i n g a m p l i t u d e . W e s h o w t h a t f o r M M

cel l s , t he hys t e r es i s l oop i s squa re , w i t h t he coe rc i ve f i e l d va r i ab l e f rom ce l l t o ce l l . T h i s i s cons i s t en t w i t h j us t t wom a g n e t i z a t io n s t a t e s f o r t h e s i n g le c h a i n o f m a g n e t i te p a r t ic l e s. F o r M R a n d M M P c e l ls , t h e h y s t e r e s i s lo o p s a r e n o t s q u a r e ,

i nd i ca t i ng t ha t t he r e a r e s eve ra l d i f f e r en t magne t i za t i on s t a t e s , and t ha t i nd i v i dua l ce l l s can be demagne t i zed . T he coe rc i ve

f i e ld s i n t h e M R a n d M M P c e l ls a r e l e s s v a r ia b l e t h a n f o r t h e M M c e ll s.

I . I n t r o d u c t i o n

M a g n e t o t a c t i c b a c t e r i a , a d i v e r s e g r o u p o f

p r o k a r y o t e s , c o n t a i n m a g n e t o s o m e s [ 1 , 2 ] , w h i c h a r e

m a g n e t i c m i n e r a l p a r t i c l e s e n c l o s e d i n m e m b r a n e s .

I n m o s t c a s es , t he m a g n e t o s o m e s a r e a r ra n g e d i n as i n g l e o r m u l t i p l e c h a i n s , a n d a r e a p p a r e n t l y f i x e d

w i t h i n t h e c e ll . I n m a n y m a g n e t o t a c t i c b a c t e r i a l ty p e s ,

t h e m a g n e t o s o m e m i n e r a l p a r ti c l e s c o n s is t o f f e r ri -

m a g n e t i c m a g n e t i t e , F e 3 0 4 [ 3] , a r e c h a r a c t e r i z e d b y

n a r r o w p a r t i c l e s i z e d i s t r i b u t i o n s , a n d h a v e u n i f o r m ,

s p e c i e s - s p e c i f i c , c r y s t a l l i n e h a b i t s [ 2 ] . T h e p a r t i c l e

s i z e s r a n g e b e t w e e n 4 0 t o 1 0 0 n m , a n d a r e w i t h i n t h e

* Corresponding author .

p e r m a n e n t s i n g l e - m a g n e t i c - d o m a i n s i z e r a n g e f o r

m a g n e t i t e [ 4 ] .

I n m a n y m a g n e t o t a c ti c b a c t e ri a f r o m m a r i n e , s u l-

f i d i c e n v i r o n m e n t s , t h e m a g n e t o s o m e p a r t i c l e s c o n -

s i s t o f t h e i ro n - s u l f i d e m i n e r a l g r e i g i t e , F e 3 S 4 [ 5 ] ,

w h i c h i s i s o s tr u c t u r a l w i t h m a g n e t i t e a n d i s a ls o

f e r r i m a g n e t i c a l l y o r d e r e d a t a m b i e n t t e m p e r a t u r e .

T h e g r e i g i t e p a r t i c l e s a r e a l s o c h a r a c t e r i z e d b y n a r -

r o w p a r t ic l e s i z e d i s tr i b u t io n s a n d s p e c i e s - s p e c i f i c

c r y s t a l h a b i t s [ 6 ] . H o w e v e r , w h e r e a s t h e m a g n e t i t e

p a r t i c l e s i n a m a g n e t o s o m e c h a i n a r e u s u a l l y o r i -

e n t e d s o t h a t a [ 1 1 1] c r y s t a l l o g r a p h i c a x i s o f e a c h

p a r t i c l e l i e s a l o n g t h e c h a i n d i r e c t i o n , t h e g r e i g i t e

p a r t i c l e s i n a m a g n e t o s o m e c h a i n a r e u s u a l l y o r i -

e n t e d s o t h a t a [ 1 0 0] c r y s t a l l o g r a p h i c a x i s o f e a c h

p a r t ic l e i s o r i e n t e d a l o n g t h e c h a i n d i r e ct i o n . I n o n e

0304-8853/95/$09.50 © 1995 Elsevier Science B.V. Al l r ights reservedS S D I 0 3 0 4 - 8 8 5 3 ( 9 5 ) 0 0 0 7 8 - X

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2 8 0 L P e n n i n g a e t al . / J o u r n a l o f M a g n e t i s m a n d M a g n e t i c M a t e r i a l s 1 4 9 ( 1 9 95 ) 2 7 9 - 2 8 6

organ i sm , an unusua l , m any-ce l l ed , m agne to tac t i c

p rokaryo te (MM P) [7 ] , pa r t ic les o f non-m agne t ic

pyr i te , FeS 2 , occu r in addi t ion to Fe3S 4 [5] . In

another organism, both magnet i te and greigi te par t i -

c les occur in the s am e cha in o f m a gne tosom es [8 ].W hether the m inera l pa r t i c les a r e m agne t i t e o r

g re ig it e , the cha in o f m agne tosom e par t ic les cons t i-

tu tes a pe rm anen t m agne t ic d ipo le f ixed w i th in the

bac te r ium [9 ] . The r em anen t m om e nt i s genera l ly

close to i ts saturat ion value. Normally i t i s suff i -

c ien t ly la rge r than the background the rm al energy so

that i t , and consequent ly the bacter ium, is or iented

a long geom agne t ic f i e ld l ines as i t sw im s , caus ing

the bacter ium to migrate a long the f ie ld l ines .

K a l m i j n a n d B l a k e m o r e [ 1 0 ] a n d M i z o t a a n d

Maeda [11 ] have r epor ted on the e f f ec t o f pu l s edm agne t ic f i e lds on the m ig ra t ion o f uncharac te r i zed

m agne to tac t i c bac te r i a co l l ec ted f rom na tu ra l env i -

ronm en ts . An in tense m agn e t ic pu l se o f s evera l hun-

dred gauss , or iented oppos i te to a s teady, several

gaus s m agne t ic f i e ld in wh ich the bac te r i a were

migrat ing, caused a f ract ion of the bacter ia , which

increased over a ce r ta in r ange w i th the s t r eng th o f

the pulses , to reverse their d irect ion of migrat ion.

S im i la r ly , exposure o f m agne to tac t i c bac te r i a to an

in tense 60 Hz m agne t ic f i e ld caused abou t 50 pe r -

cen t o f m agne to tac t i c bac te r ia in a s am ple to m ig ra teoppos i te to the or ig inal migrat ion direct ion, subse-

quent to removal of the 60 Hz f ie ld [12] .

These obse rva t ions were cons i s ten t w i th on ly two ,

oppos i te , d irect ions of magnet izat ion rela t ive to the

chain direct ion and a square hys teres is loop for each

cel l , but with coercive f ie lds that var ied f rom cel l to

cel l , or var ied accord ing to the ins tantaneou s or ienta-

t ion of the cel l with respect to the d irect ion of the

m agne t ic pu l s e.In th is paper , we descr ibe pulsed-magnet ic- f ie ld

rem anence m easurem en ts o f ind iv idua l , k i l l ed ,

und is rup ted ce l ls o f th ree d i f f e ren t types o f m agne to -

tac t ic bac te ri a . The m easurem en t t echn ique was based

on a m ethod desc r ibed by Kn owles [13 ] fo r sm al l

synthe t ic ma gnet ic par t ic les. I t involved the observa-

t ion o f a l igned , ind iv idua l m agne to tac t i c bac te r i a

wi th a l igh t m ic roscope as they were sub jec ted to

m agne t ic pu l s es o f inc reas ing am pl i tude . The m i -

c roorgan i sm s s tud ied were the cu l tu rab le m agne to -

tact ic bacter ium Magnetospirillum magnetotacticum(MM) ( fo rm er ly Aquaspirillum magnetotacticumATCC 31632) , wh ich con ta ins a s ing le cha in o f

cubo-oc tahedra l m agne t i t e - con ta in ing m agne tosom es

[3 ] , and two uncu l tu red m agne to tac t i c bac te r i a ; an

uncharac te r i zed m agne to tac t i c cu rved rod tha t con-

ta ins two o r m ore ad jacen t cha ins o f g re ig i te - con ta in -

ing m agne tosom es (MR) , and the MMP desc r ibed

a b o ve . T h e M R a n d M M P w e r e c o l le c t ed f ro m w a t e r

and s ed im en t ob ta ined f rom a b rack i sh s a l t m ar sh

poo l a t M or ro Bay , C a l i fo rn ia . ,

As we show be low , the MM hys te res i s loop i ssquare, with the coercive f ie ld var iable f rom cel l to

ce l l . Th i s i s cons i s ten t w i th ju s t two m agne t iza t ion

s tates for the s ingle chain of magnet i te par t ic les . For

the MR and MMP, the hys te res i s loops a re no t

t:~lsed ie ld Mag netization Alignmentfield

(Bp)" (M) (B.) bA ,F .~ ~ . ~ ~ . )

B < - - I -- ,~ >

C < - - - t • )

D < ; < _- )

E ( = ( ~. )

M

, A , F

~ D ) -Bp

" , , ~ E

=0 ~±7 00G b7G

F i g . 1 . S c h e m a t i c d i a g r a m o f t h e p u l s e d m a g n e t i c f i e ld r e m a n e n c e m e a s u r e m e n t s . A c e l l a l i g n e d i n t h e fi e l d B , i s s u b j e c t e d t o h i g h f ie l d

p u l s e s B p , m o s t l y o r ie n t e d o p p o s i t e t o B , . F o l l o w i n g e a c h p u l s e , t h e r e l a ti v e r e m a n e n t m o m e n t o f t h e c e l l M r i s d e t e r m i n e d a s d e s c r i b e d in

t h e t e xt . A - F c o r r e s po n d t o a s e q u e n c e o f p u l s e s a n d r e m a n e n t m o m e n t m e a s u r e m e n t s th a t r e s u lt s in t h e r e m a n e n c e p l o t s h o w n t o t h e r i g ht .

A , B p = 0 G ; B - E ; - 7 0 0 G < B p < 0 G ; F , Bp = + 7 0 0 G ( B p p a r a ll e l t o B a ).

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L Penninga et al./Journal of Magnetism and Magnetic Materials 149 (1995) 279-286 281

square , indica t ing tha t the re a re severa l d i f fe rent

magne t iza t ion s ta tes , and tha t individua l ce l l s can be

de ma gne t i z e d . The c oe rc i ve f i e l d s i n t he MR a nd

MMP c e l l s a re l e s s va r i a b l e t ha n fo r t he MM c e l l s .

2 . M e t h o d

C e l l s o f MM we re c u l t u re d a s p re v i ous l y de -

sc r i be d [14 ] a nd f i xe d i n 1% g l u t a ra lde hyde . S o me o f

t he f i xe d c e l l s we re de p os i t e d on c a rbon -c oa t e d e l ec -

t ron mi c rosc ope g r i d s fo r t r a nsmi s s i on e l e c t ron mi -

c r o s c o p y .

C e l ls o f M R a n d M M P w e r e c o l le c t e d f r o m

bra c k i sh s a l t ma rsh s e d i me n t s u s i ng a mod i f i e d

ra c e - t r a c k t e c hn i que [15 ]. T he c e l ls we re f i xe d i n 3%f o r m a l d e h y d e . S o m e o f t he M R c e ll s w e r e d e p o s i te d

on c a rbon-c oa t e d e l e c t ron mi c rosc ope g r i d s fo r

t r a nsmi s s i on e l e c t ron mi c rosc opy .

Ma gne t i c me a su re me n t s a re shown sc he ma t i c a l l y

i n F i g . 1 . T h e y w e r e m a d e w i t h a n O l y m p u s B H - 2

mi c rosc ope f i t t e d wi t h a v i de o c a me ra , VC R a nd

mo n i t o r , a nd a c o i l sy s t e m. The × 40 ob j e c t i ve wa s

mod i f i e d by re mov i ng a ma gne t i c sp r i ng t ha t p re s se d

on t he l e ns a nd c a use d a d i s t o r t ion o f t he f i e l d a t the

ob j e c t s it e . The m e t a l mi c rosc op e s ta ge wa s r e p l a c e d

by a luc i te s tage tha t was f i t t ed wi th a coi l sys temc ons i s t i ng o f i n su l a t e d c oppe r wi re wound on l uc i t e

f o r m s .

The c o i l sy s t e m c ons i s t e d o f t wo o r t hogona l ,

5 0 0 - t u r n c o i l p a i r s ( n o m i n a l l y o r i e n t e d N - S a n d

E -W ) t ha t ge ne ra t e d a va r ia b l e (up t o 15 G) , DC

a l i gnme n t f i e l d B a i n t he op t i c a l p l a ne o f t he mi c ro -

sc ope . Th e o r i e n t a t i on o f B a i n t he p l a ne c ou l d be

c on t ro l l e d by a d j us t i ng t he c u r re n t s t h rough t he t wo

c o i l pa ir s . A f i e l d B a wi t h c o ns t a n t ma gn i t ude c ou l d

a lso be used, ro ta t ing in the p lane a t a va r iable ra te

by a pp l y i ng s i nuso i da l c u r re n t s , 90 de g re e s ou t o fpha se , t o t he t wo c o i l pa i r s . Ano t he r 600 - t u rn c o i l

pa i r, o r i e n t e d pa ra l le l t o the E - W a l i gnme n t pa i r,

wa s u se d t o ge ne ra t e a 1 t o 5 ms ma gne t i c pu l s e

f i e l d B p wi t h va r i a b l e a mpl i t ude up t o 700 G. The

t wo pu l se c o i l s , c a l i b ra t e d fo r f i e l d a s a func t i on o f

c u r re n t , we re c o nne c t e d t h rough swi t c h i ng t r a ns is t o r s

t o a 5 0 - 1 5 0 V p o w e r s u p p l y. T h e m a g n i t u d e o f t h e

pu l se f i e l d wa s ob t a i ne d f rom t he r e a d i ng o f a pe a k

vo l t me t e r t ha t me a su re d t he sum o f t he vo l t a ge s

ac ross s tandard res i s tors in se r ies wi th the coi l s .

F i xe d c e l l s i n a que ous suspe ns i on we re d ra wn up

into a g lass capi l la ry tube wi th a rec tangula r c ross-

s e c t i on a nd a n op t i c a l pa t h l e ng t h o f 0 .1 m m ( InVi t ro

Dyna mi c s ) . The c a p i l l a ry t ube wa s p l a c e d on t he

s t a ge a nd v i e we d t h rough t he mi c rosc ope . The sus -pe nde d c e l ls we re obse rve d t o o r i e n t a l ong B a , a nd

t o ro t a t e by 180 de g re e s i f t he d i r e c t ion o f B a wa s

re ve r se d by re ve r s i ng t he d i r e c t i on o f c u r re n t i n t he

coils .

M o s t o f t h e m e a s u r e m e n t s w e r e m a d e w i t h o n l y

t he E- W a l i gnme n t c o i ls a c ti va t e d , wi t h B a a pp rox i -

ma t e l y 7 G . P u l s e d ma gne t i c f i e l d s o f i nc re a s i ng

a mpl i t ude wi t h B p o r i e n t e d oppos i t e t o B a we re

a pp l i e d t o t he s a mpl e . W he n B p e xc e e de d t he c oe r -

c i ve fo rc e H c o f t he c ha i n o f pa r t i c le s i n a pa r t i c u l a r

c e l l , t he c e l l c ou l d be s e e n t o ro t a t e by 180 de g re e sfo l l owi n g t he pu l s e.

T h e r e m a n e n t m a g n e t i c d i p o le m o m e n t o f t h e c e l l

Mr , fo l l owi ng a pu l s e o f a mpl i t ude B p , r e l a ti ve t o it s

or ig ina l va lue , i . e . , be fore be ing subjec ted to any

pu l se s , wa s de t e rmi ne d by me a su r i ng t he t i me T

re qu i re d fo r t he c e l l t o ro t a t e be t we e n t w o a ng l e s , th l

and qb2 , wi t h r e spe c t t o B ~ , fo l l owi ng a r e ve r sa l o f

B a. The re l a t ionsh i p be t w e e n t he t o rque e xe r t e d by

B a on M r a nd t he v i s c ou s d ra g on t he c e l l a s i t

ro ta tes i s g iven by [16] :

MrB a s in 0 = V d O / d t , ( 1 )

whe re 0 i s the i n s t a n t a ne ous a ng l e be t we e n M r a nd

B a , and Vd i s t he ro t a t i ona l -v i s c ous -d ra g c oe f f i c i e n t ,

wh i c h fo r a sphe re i s e qua l t o 8 7 r 1 / R 3 ( 1 / is the

v i s c os i t y c oe f f i c i e n t o f wa t e r a nd R i s the r a d i us o f

t he sphe re ) [17 ] . R e a r ra nge me n t a nd i n t e g ra t i on o f

Eq. (1) y ie lds

T = (Vd/MrBa) [ In t a n ( t h J 2 ) - In t an ( t h 2 / 2 ) ] .

(2 )

For cons tant Vd, Ba , t h l and thE, T i s inver se lyp ropor t i ona l t o M r B e c a use o f t he l oga r i t hmi c d i -

ve rge n c e o f T a t th = 0 a nd 180 ° , T wa s me a su re d

be tw een th l = 10° and t h E = 170° " Th i s m e t hod c ou l d

no t be u se d t o de t e rmi ne t he a bso l u t e ma gn i t ude o f

t he c e l l u l a r r e ma ne n t mome n t be c a use t he a c t ua l

v i s c ous d ra g c oe f f i c i e n t s fo r t he c e l l s in t he w a t e r

m e d i u m w e r e n o t k n o w n .

A va r i a t ion on t h i s me t hod u t i l i z e d B ~ ro t a t i ng i n

t he foc a l p l a ne a t a f i xe d f r e q ue nc y ( = 0 .5 H z ) [18] ,

i n i t i a l l y wi t h a f i e l d ma gn i t ude o f a pp rox i ma t e l y 7

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2 8 2 I. Penninga et al. /Jo urn al of Magnetism and Magnetic Materials 149 (1995) 279-2 86

F i g . 2 . T r a n s m i s s i o n e l e c t r o n m i c r o g r a p h o f a Magnetospirillum

magnetotacticum ( M M ) c e l l . B a r = 1 ~ m .

m i n e d b y a p p l y i n g p r o g r e s s i v e l y l ar g e r d c f i e ld s t o

a n i n i t i a l l y d e m a g n e t i z e d s a m p l e a n d m e a s u r i n g t h e

r e m a n e n c e a f t e r r e m o v a l o f th e f i el d . T h e d c d e m a g -

n e t i z a t i o n ( D C M ) c u r v e w a s d e t e r m i n e d b y s a t u r a t -

i ng the s a m p le i n a l a r ge pos i t i ve f i e ld a nd m e a su r -i n g t h e r e m a n e n c e a f t er a p p l y i n g p r o g r e s s i v e l y la r g er ,

n e g a t iv e , d c f i el d s. T h e b u l k s a m p l e w a s p r e p a r e d b y

d r y ing a sm a l l d r op o f t he c e l l su spe ns ion on to a

g l a s s c ove r s l i p .

3 . Re su l t s

G . A t f i r s t t he c e l l r o t a t e d a t c ons t a n t a ngu la r ve loc -

i t y w i th t he f i e ld . The n , w i th t he r o t a t i on f r e que nc y

u n c h a n g e d , t h e f i e ld m a g n i t u d e B a w a s s l o w l y r e -

duc e d un t i l a t a va lue ( n a ) m i n , t h e c e ll w a s o b s e r v e d

to s top r o t a t i ng w i th t he f i e ld . A c c o r d ing to Eq . ( 1 ) ,

r o t a t i on o f a c e l l a t c ons t a n t a ngu la r ve loc i ty w i l l

oc c u r a s l ong a s t he t o r que on the c e l l due to t he

r o t a t i ng f i e ld i s ba l a nc e d by the v i s c ou s d r a g . A s B a

i s de c r e a se d , O inc r e a se s . A t B a = ( B a ) m i n , 0 = 9 0 ° ,

f o r B a < ( B a ) m i n , t he c e l l s t ops r o t a t i ng w i th t he

f i e ld . F r o m Eq . 1 , M r i s p r opo r t i ona l t o ( B a ) m i n . A S

n o t e d a b o v e , s i n c e V w a s n o t k n o w n , o n l y th e

r e l at i v e m a g n i t u d e o f t h e r e m a n e n t m o m e n t M r o f

the c e l l c ou ld be de t e r m ine d in t h i s w a y .

B e s i d e s t h e p u l s e m e a s u r e m e n t s d e s c r i b e d a b o v e ,

t h e a v e r a g e c o e r c i v e f o r c e a n d r e m a n e n c e c u r v e s o f

a b u l k s a m p l e o f t h e c u l t u r e d M M c e l l s w e r e m e a -

s u r e d w i t h a n a l t e r n a ti n g g r a d i e n t f o r c e m a g n e t o m e -

t e r i n s t a t i c f i e ld s up to 1 . 0 kG . The i so the r m a l

r e m a n e n t m a g n e t i z a t i o n ( I R M ) c u r v e w a s d e t e r -

E= .

Eo

U

¢ -

o~

30 L ~ - ~ - - - ~

20

lo i ~ i ~''''

- 1 0 I ' ~' /

-20 ~ ./"i ~ ,

i

-30 ~ . - - - ~ - J ' ~ :

-3ooo -2o oo 1o oo o tooo 200o 30o0Magnetic Field (G)

F i g . 3 . H y s t e r e s i s l o o p f o r a b u l k M M s a m p l e a t 2 9 5 K . T h e

c o e r c i v e f o r c e i s 3 0 3 G .

3 . 1 . M a g n e t o s p i r ill u m a g n e t o ta c t ic u m

A n e l e c tr o n m i c r o g r a p h o f o n e o f t he M M s p i ri l law i th i t s s i ng l e c ha in o f c ubo - oc t a he d r a l m a gne t i t e

pa r t i c l e s is show n in F ig . 2 . Exa m ina t ion o f t h i rt y

m i c r o g r a p h s s h o w e d t h a t t h e c e l l s c o n t a i n e d f r o m 8

t o 5 2 m a g n e t o s o m e s ( a v e. 2 4 ) w i t h a n a v e r a g e p a r ti -

c l e vo lu m e o f 9 . 6 x 10 - 17 c m 3. U s in g the va lue o f

4 8 0 e m u / c m 3 f o r F e 3 0 4 a t 2 95 K , t h i s y i el d s a n

e s t i m a t e d m a g n e t i c m o m e n t p e r c e l l r a n g i n g f r o m

M = 0 . 32 to 2 . 4 X 10 - 12 e m u , w i th a n a v e r a ge va lue

o f 1 .1 × 10 - 12 e m u ( 1 e m u = 1 e r g / g a u s s ) . T h e

bu lk c oe r c ive f o r c e a t 295 K w a s 303 G ( F ig . 3 ) ,

w h i c h i s c o n s i s t e n t w i t h p r e v i o u s m e a s u r e m e n t s o nM M c e l l s [ 19 ] . The r e m a ne nc e r a t i o ( M r /M ) w a s

0 . 48 , i n e xc e l l e n t a g r e e m e n t w i th t he t he o r e t i c a l

v a l u e o f 0 . 5 f o r a r a n d o m d i s p e r s i o n o f s i n g l e - m a g -

ne t i c - dom a in pa r t i c l e s .

1 5 i

1(I _ _ ~

~ ° o o c

0. 5

~ o.o

~ - (L5

- 1 , 0

- 1 . 5 I

2 0 0 2 5 0

I3 0 0 3 5 0 4 0 0

Pulsed Field (G)

F i g . 4 . P u l s e d m a g n e t i c f i e l d r e m a n e n c e p l o t f o r a n i n d i v i d u a l

M M c e l l .

Edited by Foxit ReaderCopyright(C) by Foxit Corporation,2005-2009For Evaluation Only.

8/2/2019 REMANE~1


1 . P e n n i n g a e t a l. / J o u r n a l o f M a g n e t i s m a n d M a g n e t i c M a t e r i a l s 1 4 9 ( 1 99 5 ) 2 7 9 - 2 8 6 2 8 3

In t he pu l s e d re ma ne nc e c u rve o f F i g . 4 , t he

re l a t ive ma gn i t ude o f t he r e ma ne n t d i po l e mom e n t o f

a ce l l M r i s p lo t ted aga ins t the am pl i tude Bp o f the

pu l se d ma gn e t i c f i el d . S i nc e B a wa s t a ke n a s de f i n -

ing the pos i t ive d i rec t ion , and Bp i s ant ipa ra l le l toB a , -B p i s p l o t t e d a long t he absc i ss a i n F i g . 4. F o r

ne ga t i ve va l ue s o f M r t he ma gn e t i z a t ion o f t he c ha i n

ha s r e ve r se d d i re c t i on wi t h i n t he c e l l. Th e hy s t e re s is

loop in th i s sp i r i l lum is ve ry square . In such cases ,

the co erc iv e f ie ld , H c , i s de f ine d as the f ie ld a t

wh i c h t he ma gn e t i z a t ion re ve r sa l t a kes p l a c e ; fo r t he

p re se n t s a mpl e , H c = 3 10(3 ) G . A squa re hys t e re s i s

loop i s charac te r i s t ic of a l l MM ce l l s , sugges t ing tha t

t he ma gne t i z a t i on o f a c e l l c a n be r e ve r se d , bu t t ha t

t he c e l l c a nno t be de ma gne t i z e d . In a f e w c e l l s ,

howe ve r , t he ma gne t i z a t i on re ve r sa l oc c u r re d i n t wos t a ge s , wi t h a sudde n sma l l de c re a se i n mome n t

fo l l owe d by c ompl e t e ma gne t i z a t i on re ve r sa l a t a

s l ight ly h igher pulse f ie ld .

The ma g n i t ude o f M r fo r a c e l l wa s t he s a me

be fo re a nd a f t e r a s a t u ra t ion pu l s e (B p = 700 G) ,

wi th Bp para l le l t o n a , indica t ing tha t the mic ro-

ma gne t i c sp i n s t ruc t u re o f t he c ha i n wa s t he s a me i n

bo t h s t a te s , a nd t ha t the na t u ra l r e ma ne n t mo me n t o f

t he c e l l s equa l s t he s a t u ra t ion re m a ne n t mo me n t .

T h e I R M a n d D C M c u r v e s f o r t h e b u l k s a m p l e

a re shown i n F i g . 5 . As a me a su re o f i n t e r - s t r a nd o rin t ra -s t rand dipola r in te rac t ions , the two se t s of re -

m a n e n c e m e a s u r e m e n t s a r e c o m b i n e d t o f o r m a

mM

0 .5

0 . 0

, ~o iol

- 0 . 5 "?

DC MI

-1 .0 . . . . 2 . . . . . . . . . . . . . ~ J 2 ~ : : ~ . . . . .0 1 0 0 2 0 0 3 0 0 4 0 0 5 0 0 6 0 0 7 0 0 8 0 0

Magnet ic F ie ld (G)

F i g . 5. N o r m a l i z e d c u r v e s o f i s o t h e r m a l r e m a n e n t m a g n e t i z a t i o n

( I R M ) a n d d c d e m a g n e t i z a t i o n ( D C M ) f o r b u l k s a m p l e . C u r v e s

h a v e b e e n n o r m a l i z e d t o th e s a t u r a ti o n r e m a n e n c e p r o d u c e d i n 1

k G . A H e n k e l p l o t f o r th i s s a m p l e i s s h o w n i n th e i n s e rt .

6 .0 [ . . . . . . ~ . . . . . . . . . . . . . . . 10

i o i . i. 0 : : • c o . s ' : : ' i, 8

/, ! ' 6m / i o

3.0 F :'- - - 4 _ ~

_ /

. . . . . . . . . .

0 .00 100 200 300 400 500 600

Coercivity (G)

F i g . 6 . H i s t o g r a m o f s w i t c h i n g f i e l d s f o r M M c e l l s w i t h s w i t c h i n g

f i e ld d i s t r ib u t i o n s o b t a i n e d b y d i f f e r e n t i a t i n g th e D C M a n d I R M

d a t a in F i g . 5. T h e r e m a n e n t S F D s h a v e b e e n n o r m a l i z e d b y t h e

t o t a l a r e a u n d e r e a c h c u r v e .

Henke l p lo t (e .g . , Ref . [20]) and shown in the inse t

o f F i g . 5 . F o r non - i n t e ra c t i ng s i ng l e doma i n pa r t i -

c l e s , t he He nke l p l o t i s l i ne a r wi t h a s l ope o f -2 .

The s l i gh t c onc a ve upwa rd de pa r t u re f rom i de a l

be ha v i o r sugge s t s a mi n i ma l de g re e o f ne ga t i ve (de -

ma gne t i z i ng ) i n t e ra c t i ons be t we e n ma gne t osome

c ha i ns [19 -22 ] .

The pu l s e f i e l d s a t wh i c h ma gne t i z a t i on re ve r sa l

oc c u r re d we re me a su re d fo r 50 sp i ri l la a nd a re d i s -p l a ye d i n t he h i st og ra m sho wn i n F i g. 6 . The a v e ra ge

ma gne t i z a t i on re ve r sa l f i e l d fo r t he se c e l l s wa s 292

G, i n good a g re e me n t wi t h t he bu l k c oe rc i v i t y o f 303

G fo r t he s a mpl e bu t l e s s t ha n t he r e ma ne n t c oe rc i v -

i ty ( H r ) o f 339 G . The so l i d a nd da she d l i ne s i n F i g.

6 we re ob t a i ne d by d i f f e re n t i a t i ng t he DC M a nd

IR M re ma n e nc e p l o t s o f the bu l k da t a wi t h r e spe c t to

ma gne t i c f i e l d a nd p rov i de e s t i ma t e s o f t he swi t c h -

i ng f i e l d d i s t r i bu t i ons (S F D) du r i ng ma gne t i z a t i on

a nd re ma gne t i z a t i on . B o t h r e ma ne n t S F Ds a re a p -

p rox i ma t e l y t he s a me sugge s t i ng mi n i ma l i n t e ra c t i one f fe c t s a nd i s a no t he r e xp re s s i on o f t he ne a r l i ne a r

He nk e l p l o t. A l t houg h t he a ve ra ge c o e rc i v i t y i s a p -

p rox i m a t e l y t he s a me fo r bo t h t he bu l k a nd s i ng le

ce l l exper ime nts , the re i s a sha rp cuto ff in the s ingle

c e l l S F D c ompa re d t o t he h i gh - f i e l d t a i l fo r t he

ra ndom d i spe r s i on o f d r i e d c e l ls .

The de pe n de nc e o f H c on t he o r i e n t a t ion o f B p

wi t h r e spe c t t o t he o r i e n t a t ion o f M r w a s i nve s t i-

g a t ed b y c o m p a r i n g H c fo r Bp or iented ant ipa ra l le l

to B a , to H c fo r B p or iented a t 45 degree s to B a .

8/2/2019 REMANE~1


2 8 4 L P enninga e t a l. / Jo urn a l o j :Magne ti sm and Magne t ic Mater ia l s 149 (1995) 279- 286

i

F i g . 7 . T r a n s m i s s i o n e l e c t r o n m i c r o g r a p h o f a n u n c u l t u r e d m a g n e -

t o t a c t i c r o d ( M R ) . B a r = 1 i x m .

T he va lue s o f H e w e r e 300 G a nd 320 G , r e spe c -

t ive ly .

F e 3 S 4 m a g n e t o s o m e s . A n e l e c t r o n m i c r o g r a p h o f a

M M P i s show n in F ig . 8 . T he o r ga n i sm c ons i s t s o f

mul t i p l e c e l l s , e a c h o f w hic h c on t a ins s i ng l e o r

d o u b l e m a g n e t o s o m e c h a in s . T h e m a g n e t o s o m e m i n -

erals a r e F e 3 S 4 a nd Fe S2 , bu t t he a r r a nge m e nt o f t heminera ls in the cha ins i s not known. F ig . 8 shows the

M M P w i th t he i nd iv idua l c e l l s d i sa gge ga t e d on t he

gr id . T he r e i s e v ide nc e f r om e l e c t r on mic r osc opy

( B .R . H e yw ood , S . M a nn , a nd R .B . F r a nke l , unpub-

l i she d) t ha t t he ma gne tosome c ha ins i n c e l l s o f t he

in t a c t o r ga n i sm ha ve a c ommon o r i e n t a t i on .

Pu l se d f i e l d r e ma ne nc e p lo t s f o r s i x M R c e l l s a nd

f ive MMP ce l l s a re shown in Figs . 9 and 10, r espec-

t i ve ly . T he a ve r a ge va lue s o f H c w e r e 32 0 + 20 G

a nd 200 + 3 G , r e spe c t i ve ly . U n l ike t he M M c e l ls ,

t he M R a nd M M P hys t e r e s i s l oops w e r e no t squa r e ,i nd i c a t i ng t ha t i nd iv idua l M R a nd M M P c e l l s c a n be

de ma gne t i z e d .

3 .2 . M R a n d M M P 4 . D i s cu s s i on

A n e l e c t r on mic r ogr a ph o f a M R c e l l i s show n in

Fig. 7 . The ce l l conta ins two adjacent cha ins of

T he h igh squa r e ne ss o f the pu l se d r e ma n e nc e da t a

ob t a ine d f o r M M i s c ons i s t e n t w i th t he s i ng l e c ha in

F i g . 8 . T r a n s m i s s i o n e l e c t r o n m i c r o g r a p h o f a n u n c u l t u re d , m a n y - c e l l e d , m a g n e t o t a c t i c p r o k a r y o t e ( M M P ) . B a r = 1 I~ m .

8/2/2019 REMANE~1


L Penninga et al./Journal of Magnetism and Magnetic Materials 149 (1995) 279-286 28 5

15

1 o [

.~ 0,5

0. 0

1.0

-1.5

100 200

m o

z~ o

z~13A

z~

I30 0

I

4 0 0 5 0 0 6 0 o

Pulsed Field (G)

Fig. 9. Pulsed magnetic field remanence plots for a six magneto-tactic rods (MR).

of s i ng l e -doma i n ma gne t i t e pa r t i c l e s i n t h i s o rga n -

i sm. Th i s s t ruc t u re i s r e mi n i s c e n t o f t he ' c ha i n o f

sphe re s ' mode l fo r e l onga t e d s i ng l e doma i n pa r t i c l e s

[23 ]. M a gne t i c i n t e ra c t i ons be t we e n t he pa r t i c le s a nd

t he pe r fe c t c rys t a l l og ra ph i c a l i gnme n t o f t he c rys -

t a ll i ne e a sy a x i s a l ong t he c ha i n d i re c t i on c om bi ne t o

ma ke t he c ha i n a x i s t he e a sy a x i s o f ma gne t i z a t i on ,

a nd ma gne t i z a t i on re ve r sa l oc c u rs by a f a nn i ng o r

v o r t e x p r o p a g a t i o n m e c h a n i s m [ 2 3 - 2 5 ] . B e c a u s e o f

ga ps be t we e n t he pa r t i c l e s i n t he c ha i n , t he c oe rc i ve

fo rc e i s l e s s t ha n t he c oe rc i ve fo rc e e xpe c t e d fo r a

~ 0.0

a~ 05

-1.0

- I .5

I ~

0.5

]

DA

I I _ I

100 200 300 400 5~ 6~

Pulsed Field (G)

Fig. 10. Pulsed magnetic field remanence plots for five many-cel-

led, magnetotactic prokaryotes (MMP).

so l i d rod o r c y l i nde r [19 ]. F o r e xa m pl e , t he c l a s s i c al

n o n s y m m e t r i c f a n n i n g m o d e o f J a c o b s a n d B e a n [ 23 ]

p re d i c t s H c = 439 G fo r a c ha i n o f 12 m a gne t i t e

pa r t i cl e s o r g re a te r , whe re a s t he obse rv e d Hc fo r t he

M M s a m p l e i s a p p r o x i m a t e l y 3 0 0 G . T h e f a n n i n g -t ype re ve r sa l mode s a re a l so c ons i s t e n t wi t h t he

obse rve d d i s t r i bu t i on i n t he c oe rc i ve fo rc e i n t he

popula t ion , e i the r through a d i s t r ibut ion in gap s izes ,

c ha i n l e ng t hs , o r bo t h . The ore t i c a l mode l s fo r f a n -

n i ng - l ike m a gne t i z a t i on re ve r sa ls i n a l i ne a r c ha in o f

pa r t i c l e s p re d i c t t ha t c ha i n c oe rc i v i t y a pp roa c he s a

sa tura t ion va lue for n > 12 [23,25,26] . We in te rp re t

t he sha rp c u t o f f i n t he c oe rc i v i t y d i s tr i bu t ion ob -

se rve d fo r t he c e l l s i n t e rms o f t h i s s a t u ra ti on e f fe c t .

Howe ve r , s i nc e i t wa s no t pos s i b l e t o obse rve t he

c ha i n l e ng t h i n a c e l l w i t h l i gh t mi c rosc opy , i t wa sno t pos s i b l e t o c o r re l a t e the c o e rc i ve fo rc e o f a g i ve n

ce l l wi th cha in length .

The re l a t i ve l y sma l l i nc re a se , f rom 300 t o 320 G,

i n t he c oe rc i ve fo rc e wi t h c ha nge o f a ng l e f rom 0 t o

45 ° be t we e n t he ba c t e r i a l d i po l e a nd t he pu l s e f i e l d

i s a l so c ons i s t e n t wi t h a n on -c oh e re n t r e ve r sa l mo de ,

suc h a s t he f a nn i ng mode i n t he c ha i n o f sphe re s

mode l [23] .

T h e s u d d e n s m a l l d e c r e a s e i n m o m e n t f o l l o w e d

by c ompl e t e r e ma gne t i z a t i on a t s l i gh t l y h i ghe r pu l s e

f i e l d s , obse rve d i n some MM c e l l s , sugge s t s t ha t a ni n t e rme d i a t e r e ma ne n t s t a t e c a n oc c a s i ona l l y be ob -

ta ined. The reason for th i s i s unc lea r , but i s probably

re la ted to depar tures f rom an idea l , l inea r cha in

s t ruc t u re . One t ype o f de pa r t u re i s t he p re se nc e o f a

f e w i m m a t u r e m a g n e t o s o m e s a t t h e e n d s o f c h a i n s

[27 ] . Imma t u re ma gne t osome s a re sma l l e r - s i z e d pa r -

t i c l e s , a pp roa c h i ng t he supe rpa ra ma gne t i c - s i ng l e do -

ma i n t r a ns i t i on vo l ume , fo rme d du r i ng i n i t i a l c rys t a l

g rowt h . The mome n t s o f t he se pa r t i c l e s ma y swi t c h

a t a lower c r i t i ca l f ie ld than the res t of the cha in due

t o t he i r sma l l e r vo l ume s a nd t e rmi na l pos i t i ons . Theva r i a b l e oc c u r re nc e o f t he se sma l l e r ma gne t osome s

i n MM c e l l s wou l d e xp l a i n bo t h t he sma l l ma gn i t ude

o f t h e m o m e n t d e c r e a s e a n d w h y t h e i n t e r m e d i a t e

mi c roma gne t i c s t a t e i s obse rve d i n on l y some c e l l s .

T h e p u l s e d h y s t e r e s i s m e a s u r e m e n t s o n M R a n d

MMP c e l l s sugge s t t ha t o rga n i sms wi t h t wo o r more

a d j a c e n t c ha i ns c a n be e f fe c t i ve l y de ma gne t i z e d . F o r

t h i s t ype o f ge ome t r i c a l a r ra nge me n t o f ma gne t o -

some s , e i t he r t he mome n t s o f t he t wo s t r a nds a re

a n t i pa ra l l e l ( ' i n t e r -c ha i n ' ) , o r i nd i v i dua l ma gne t o -

8/2/2019 REMANE~1


286 L P e n n i n g a e t a l. / J o u r n a l o f M a g n e t is m a n d M a g n e t ic M a t e r i a ls 1 4 9 ( 1 9 95 ) 2 7 9 - 2 8 6

som es a long the s am e cha in can be an t ipa ra l l e l ( ' i n -

t ra-chain ' ) . I t i s noteworthy that the chains with

g re ig it e on ly (MR ) ha ve h igher coerc iv i ty than cha ins

wi th g re ig i t e and py r i t e (MMP) , even though the

greigi te magnetosomes have s imilar s ize d is t r ibu-t ions in both organisms. This observat ion can be

rat ional ized i f we hypothes ize that pyr i te par t ic les

a re co -o rgan ized in the cha ins o f the MMP. T hen i t

is l ikely that MR cel ls reverse their magnet iza t ion by

in te r- cha in r em agne t iza t ion on ly , whereas the MM P

cel ls reverse their magnet izat ion by in tra-chain re-

m agne t iza t ion . P resum ab ly , the non-m agn e t ic py r it e

par t ic les in the MMP chains reduce the s t rong pos i-

t ive in teract ions between the greigi te par t ic les , mak-

ing an in t r a -cha in r ever s ing m ode m ore p robab le

with a concomitant decrease in the energy barr ier forremagnet izat ion. These observat ions are in agree-

m en t w i th r ecen t m ic rom agne t ic m ode l ing o f sw i tch -

ing f i e ld behav io r in in te rac t ing cha ins o f cub ic and

spherical particles [24,25].

Acknowledgements

We thank J . Hils inger for help in the cons truct ion

of the pulsed magnet ic f ie ld apparatus . IP was sup-

por ted by a g ran t f rom the U n iver s ity o f Gron ingen .DA B and R BF were suppor ted by the U .S . Of f ice o f

Nava l Research . BMM and DAB were suppor ted by

the Nat ional Science Foundat ion. Suppor t for the

Ins ti tu te fo r Rock M agne t i sm was p rov ided by g ran t s

f rom the Keck Founda t ion and the Na t iona l Sc ience

Foundat ion. This is contr ibut ion 9409 of the Ins t i tu te

fo r Rock Magne t i sm .

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eds. (Will iam s and Wilkins, Balt imore, MD, 1989) p. 1882.

[2] D.A. Bazylinski, A .J. Garratt-Reed and R.B. Frankel, Mi-

crosc. Res. Tech. 27 (1994) 389.

[3] R.B. Frankel , R.P. B lakem ore and R.S. Wolfe, Scienc e 203

(1979) 1355.

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