The processes by which microorganisms, particularly bacteria, produce inorganic mineral particles are reviewed

Frankel, Richard B.

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n  I N O R G A N I C  P A R T I C L E S  P R O D U C E D  B Y  M I C R O O R G A N I S M S  R I C H A R D  B .  F R A N K E L  D e p a r t m e n t  o f  P h y s i c s ,  C a l i f o r n i a  P o l y t e c h n i c  S t a t e  U n i v e r s i t y ,  S a n  L u i s  O b i s p o ,  C A  9 3 4 0 7  A B S T R A C T  T h e  p r o c e s s e s  b y  w h i c h  m i c r o o r g a n i s m s ,  p a r t i c u l a r l y  b a c t e r i a ,  p r o d u c e  i n o r g a n i c  m i n e r a l  p a r t i c l e s  a r e  r e v i e w e d .  I N T R O D U C T I O N  B i o m i n e r a l i z a t i o n  p r o c e s s e s  b y  w h i c h  o r g a n i s m s  f o r m  i n o r g a n i c  m i n e r a l s  a r e  b r o a d l y  d i s t r i b u t e d  a n d  o c c u r  i n  a l m o s t  e v e r y  p h y l u m  o f  t h e  b i o l o g i c a l  w o r l d  [ 1 - 5 ] .  T h e r e  i s  a  l a r g e  d i v e r s i t y  o f  m i n e r a l s  f o r m e d ,  w i t h  o v e r  6 0  c u r r e n t l y  k n o w n  [ 1 ] .  M i c r o o r g a n i s m s ,  i n c l u d i n g  e u k a r y o t e s  ( f u n g i ,  p r o t o z o a  a n d  a l g a e )  a n d  p r o k a r y o t e s  ( b a c t e r i a ) ,  a r e  d e e p l y  i n v o l v e d  i n  t h e  g e o c h e m i c a l  c y c l i n g  o f  i n o r g a n i c  e l e m e n t s  v i a  m i n e r a l  f o r m a t i o n  a n d  d i a g e n e s i s .  B i o m i n e r a l i z a t i o n  p r o d u c t s  i n c l u d e  c a l c i u m  c a r b o n a t e s ,  c a l c i u m  p h o s p h a t e s ,  s i l i c a ,  i r o n  o x i d e s "  m a n g a n e s e  o x i d e s ,  i r o n  p h o s p h a t e s ,  i r o n  s u l f i d e s ,  a n d  o t h e r  h e a v y  m e t a l  s u l f i d e s .  T h e  p o t e n c y  o f  b a c t e r i a  i n  b i o m i n e r a l i z a t i o n  i s  d u e  t o  t h e i r  h i g h  s u r f a c e  t o  v o l u m e  r a t i o  a n d  t o  t h e  n e g a t i v e l y  c h a r g e d  m o i e t i e s  t h a t  c o n s t i t u t e  t h e i r  c e l l  w a l l s  a n d  a r e  p o t e n t i a l  s i t e s  f o r  t h e  b i n d i n g  o f  c a t i o n s  [ 6 ] .  B I O M I N E R A L I Z A T I O N  L o w e n s t a m  [ 7 ]  h a s  d i s t i n g u i s h e d  t w o  g e n e r a l  m o d e s  o f  b i o m i n e r a l i z t i o n ,  n a m e l y ,  b i o l o g i c a l l y - i n d u c e d  m i n e r a l i z a t i o n  ( B I M )  a n d  b i o l o g i c a l l y  c o n t r o l l e d  m i n e r a l i z a t i o n  ( B C M )  ( a l s o  r e f e r r e d  t o  a s  b o u n d a r y - o r g a n i z e d  b i o m i n e r a l i z a t i o n  ( B O B )  [ 8 ] ) .  I n  a  B I M  p r o c e s s ,  c e l l u l a r  e x p o r t  o f  m e t a b o l i c  p r o d u c t s  r e s u l t s  i n  e x t r a c e l l u l a r  m i n e r a l  f o r m a t i o n  w i t h  i o n s  i n  t h e  e n v i r o n m e n t .  T h e  p a r t i c l e s  a r e  e s s e n t i a l l y  i n d i s t i n g u i h a b l e  f r o m  t h o s e  p r o d u c e d  b y  p u r e l y  i n o r g a n i c  p r o c e s s e s .  I n  a  B C M  p r o c e s s ,  t h e  m i n e r a l  p h a s e  i s  d e p o s i t e d  i n  o r  o n  p r e f o r m e d  o r g a n i c  v e s i c l e s  o r  m a t r i c e s  p r o d u c e d  b y  t h e  o r g a n i s m .  B I M  p r o c e s s e s  a r e  n o t  c o n t r o l l e d  b y  t h e  o r g a n i s m  a n d  t h e  m i n e r a l  p a r t i c l e s  t y p i c a l l y  h a v e  a  l a r g e  s i z e  d i s t r i b u t i o n  a n d  n o  u n i q u e  m o r p h o l o g y .  B C M  p r o c e s s e s  i n v o l v e  h i g h l y  c o n t r o l l e d  m i n e r a l i z a t i o n  a n d  t h e  p a r t i c l e s  o f t e n  h a v e  a  n a r r o w  s i z e  d i s t r i b u t i o n  a n d  s p e c i e s - s p e c i f i c  m o r p h o l o g y .  M u c h  o f  t h e  c u r r e n t  r e s e a r c h  o n  b i o m i n e r a l i z a t i o n  p h e n o m e n a  i s  d i r e c t e d  a t  e l u c i d a t i n g  t h e  s t r u c t u r e  o f  t h e  o r g a n i c  m a c r o m o l e c u l e s  i n v o l v e d  i n  t h e  B C M  p r o c e s s e s  a n d  t h e  n a t u r e  o f  t h e  o r g a n i c - i n o r g a n i c  i n t e r a c t i o n s .  I n  a  v e r y  g e n e r a l  w a y ,  a l l  i r o n  o x i d a t i o n  b y  m o l e c u l a r  o x y g e n  o n  t h e  s u r f a c e  o f  t h e  e a r t h  o c c u r s  b y  a  B l M  p r o c e s s  b e c a u s e  m o l e c u l a r  o x y g e n  i n  t h e  a t m o s p h e r e  i s  a  b y p r o d u c t  o f  p h o t o s y n t h e s i s .  H o w e v e r ,  t h e  d i s t i n c t i o n  b e t w e e n  B I M  a n d  B C M  p r o c e s s e s  i s  m o r e  u s e f u l  i n  c o n s i d e r i n g  m o r e  r e s t r i c t e d  s i t u a t i o n s ,  s u c h  a s  i n s t a n c e s  o f  i r o n  b i o m i n e r a l i z a t i o n  b y  b a c t e r i a .  M a t .  R e s .  S o c .  S y m p .  P r o c .  V o l .  2 1 8 .  @ 1 9 9 1  M a t e r i a l s  R e s e a r c h  S o c i e t y  Magnetite (Fe304) formation by bacteria occurs by both BIM and BCM processes, in dissimilatory iron-reducing bacteria and magnetotactic bacteria, respectively. The dissimilatory iron­reducing bacteria [9J respire Fe 3+ obtained from ferric oxy­hydroxide in the environment, that is, they use ferric ions as terminal electron acceptors in their metabolism. The resulting ferrous ions are exported into the environment where they interact with excess ferric oxy-hydroxide to produce magnetite by a BIM process. The ferrous ions can also interact with carbonate in the medium to form ferrous carbonate, siderite [10]. In contrast. magnetotactic bacteria form magnetite particles [11,12] by a BCM process in intracellular membrane vesicles [13] from a ferric oxy­hydroxide precursor and ferrous ions [14J A particle and its enveloping membrane is known as a magnetosome, and the process is presumably mediated by the magnetosome membrane. The particles constitute a permanent magnetic dipole in each cell that is the basis of the magnetotactic response. The structures and magnetic properties of the magnetite particles produced by the BIM and BCM processes noted above have characteristic differences [10,15]. In the case of the dissimilatory iron reducing bacteria, the particles have a broad size distribution and no apparently preferred morphology. The magnetite particles produced by magnetotactic bacteria on the other hand, have a narrow size distribution and species-specific morphologies. Under certain culture conditions, magnetotactic bacteria produce extracellular ferrous phosphate, vivianite [16], presumably by a BIM process. Iron sulfide formation by bacteria also occurs by both BIM and BCM processes, with sulfate-reducing bacteria in marine sediments [17,18] and magnetotactic bacteria from high sulfide environments [19,20], respectively. Extracellular iron sulfides are produced by BIM processes in marine sediments as a byproduct of bacterial sulfate reduction (respiration) and export of sulfide ions. This results in a mixture of iron sulfides, including material known as framboidal iron pyrites [17]. In contrast, intracellular crystalline particles of the iron sulfides greigite and pyrite [19J, and pyrrhotite [20], have been reported in magnetotactic bacteria from marine salt ponds with high sulfide concentrations. The particles are related to the magnetotactic response of these organisms, and possibly to other, metabolic, functions as well. Some types of the magnetotactic bacteria contain greigite particles (without pyrite) with species-specific morphologies (21], suggesting BCM processes. Ferric oxy-hydroxides are produced both extracellularly and intracellularly by bacteria. Extracellular production occurs in the case of the so-called iron bacteria [4J which utilize oxidation of ferrous ions by molecular oxygen as an energy source, resulting in the export and subsequent hydrolysis of ferric ions. Intracellular production occurs as mineral core particles in the iron storage proteins known as bacterioferritins [22). In the latter case the mineral particles are associated with phosphate. It is tempting to characterize the extra- and intracellular production as BIM and BCM processes, respectively. However. the formation of ferric oxy-hydroxides by the iron-bacteria has some characteristics of a BCM process. While the mineral particles themselves are indistinguishable from particles formed by purely inorganic hydrolysis the precipitate is molded into sheaths and 7 9  s t a l k s ,  p r e s u m a b l y  b y  o r g a n i c  m o l e c u l e s  o n  t h e  o u t e r  s u r f a c e s  o f  t h e  c e l l s .  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Inorganic Particles Produced by Microorganisms

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Inorganic Particles Produced by Microorganisms

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