10
Bacterial magnetosomes: microbiology, biomineralization and biotechnological applications D. Schiiler . R. B. Frankel Max-Planck-Institut fUr Marine Mikrobiologie, 28 359 Bremen, Germany Department of Physics, California Polytechnic State University, San Luis Obispo, CA 93407, USA Abstract Magnetotactic bacteria orient and migrate along geomagnetic field lines. This ability is based on intracellular magnetic structures, the magnetosomes, which comprise nanometer-sized, membrane-bound crystals of the magnetic iron minerals magnetite (Fe304) or greigite (Fe3S4)' Magnetosome formation is achieved by a mineralization process with biological control over the accumulation of iron and the deposition of the mineral particle with specific size and orientation within a membrane vesicle at specific locations in the cell. This review focuses on the current knowledge about magne- totactic bacteria and will outline aspects of the physi- ology and molecular biology of the biomineralization process. Potential biotechnological applications of magnetotactic bacteria and their magnetosomes as well as perspectives for further research are discussed. Introduction The formation of biological hard materials, i.e., bone, shell and spicule, involves the deposition of specific in- organic minerals on or in an organic matrix in a highly controlled manner (Lowenstam 1981). Much current research is directed towards understanding these bio- mineralization processes, which are collectively known as biologically controlled mineralization, because of their relevance to the synthesis of advanced materials with tailored properties (Mann 1993; Moskowitz 1995). One of the most intriguing examples of biologically controlled mineralization is the formation of magnetic nano-crystals in magnetosomes within magnetotactic bacteria. The formation of magnetosomes in these or- ganisms is a well-documented example of the appar- ently widespread occurrence of magnetic minerals in the living world. Biomineralization of ferromagnetic materials, mainly magnetite, has been reported for an extremely diverse range of organisms including algae (Torres de Araujo et al. 1986), insects (Maher 1998), molluscs (Lowenstam 1981), fish (Mann et al. 1988), birds (Wiltschko and Wiltschko 1995) and even hu- mans (Kirschvink et al. 1992). The discovery of mag- netotactic bacteria by R. Blakemore (1975) stimulated interdisciplinary research interest among scientists, in- cluding microbiologists, physicists, geologists, chemists, and engineers. Commercial uses of bacterial magneto- some particles have been suggested, including the manufacture of magnetic tapes and printing inks, magnetic targeting of pharmaceuticals, cell separation and their application as contrast-enhancement agents in magnetic resonance imaging (Blakemore 1983; Mann et al. 1990; Matsunaga 1991; Schwartz and Blakemore 1984). Ecology and phylogeny of magnetotactic bacteria Magnetotactic bacteria represent a heterogeneous group of procaryotes with a variety of morphological types including cocci, rods, vibrios, spirilla and apparently multicellular forms (Bazylinski et al. 1994; Spring and Schleifer 1995). They are constituents of natural micro- bial communities in sediments and chemically stratified water columns and a broad diversity of morphological forms has been found in many marine and freshwater habitats. The highest numbers of magnetotactic bacteria are generally found at the oxic/anoxic transition zone or redoxocline, which is located in many freshwater habi- tats at the sediment/water interface or just below (Bazylinski 1995; Stolz 1993). Accordingly, nearly all of

Bacterial Magnetosomes: Microbiology, Biomineralization ...materials, mainly magnetite, has been reported for an extremely diverse range of organisms including algae (Torres de Araujo

  • Upload
    others

  • View
    5

  • Download
    0

Embed Size (px)

Citation preview

Page 1: Bacterial Magnetosomes: Microbiology, Biomineralization ...materials, mainly magnetite, has been reported for an extremely diverse range of organisms including algae (Torres de Araujo

Bacterial magnetosomes: microbiology, biomineralization and biotechnological applications D. Schiiler . R. B. Frankel

Max-Planck-Institut fUr Marine Mikrobiologie, 28 359 Bremen, Germany

Department of Physics, California Polytechnic State University, San Luis Obispo, CA 93407, USA

Abstract Magnetotactic bacteria orient and migrate along geomagnetic field lines. This ability is based on intracellular magnetic structures, the magnetosomes, which comprise nanometer-sized, membrane-bound crystals of the magnetic iron minerals magnetite (Fe304) or greigite (Fe3S4)' Magnetosome formation is achieved by a mineralization process with biological control over the accumulation of iron and the deposition of the mineral particle with specific size and orientation within a membrane vesicle at specific locations in the cell. This review focuses on the current knowledge about magne­totactic bacteria and will outline aspects of the physi­ology and molecular biology of the biomineralization process. Potential biotechnological applications of magnetotactic bacteria and their magnetosomes as well as perspectives for further research are discussed.

Introduction

The formation of biological hard materials, i.e., bone, shell and spicule, involves the deposition of specific in­organic minerals on or in an organic matrix in a highly controlled manner (Lowenstam 1981). Much current research is directed towards understanding these bio­mineralization processes, which are collectively known as biologically controlled mineralization, because of their relevance to the synthesis of advanced materials with tailored properties (Mann 1993; Moskowitz 1995).

One of the most intriguing examples of biologically controlled mineralization is the formation of magnetic nano-crystals in magnetosomes within magnetotactic bacteria. The formation of magnetosomes in these or­ganisms is a well-documented example of the appar­ently widespread occurrence of magnetic minerals in

the living world. Biomineralization of ferromagnetic materials, mainly magnetite, has been reported for an extremely diverse range of organisms including algae (Torres de Araujo et al. 1986), insects (Maher 1998), molluscs (Lowenstam 1981), fish (Mann et al. 1988), birds (Wiltschko and Wiltschko 1995) and even hu­mans (Kirschvink et al. 1992). The discovery of mag­netotactic bacteria by R. Blakemore (1975) stimulated interdisciplinary research interest among scientists, in­cluding microbiologists, physicists, geologists, chemists, and engineers. Commercial uses of bacterial magneto­some particles have been suggested, including the manufacture of magnetic tapes and printing inks, magnetic targeting of pharmaceuticals, cell separation and their application as contrast-enhancement agents in magnetic resonance imaging (Blakemore 1983; Mann et al. 1990; Matsunaga 1991; Schwartz and Blakemore 1984).

Ecology and phylogeny of magnetotactic bacteria

Magnetotactic bacteria represent a heterogeneous group of procaryotes with a variety of morphological types including cocci, rods, vibrios, spirilla and apparently multicellular forms (Bazylinski et al. 1994; Spring and Schleifer 1995). They are constituents of natural micro­bial communities in sediments and chemically stratified water columns and a broad diversity of morphological forms has been found in many marine and freshwater habitats. The highest numbers of magneto tactic bacteria are generally found at the oxic/anoxic transition zone or redoxocline, which is located in many freshwater habi­tats at the sediment/water interface or just below (Bazylinski 1995; Stolz 1993). Accordingly, nearly all of

Page 2: Bacterial Magnetosomes: Microbiology, Biomineralization ...materials, mainly magnetite, has been reported for an extremely diverse range of organisms including algae (Torres de Araujo

G�8 �W�GK�4G8� D4�G8TK4 8Z�KDKG 4 UGTBA: CT898T8A�8 9BT �B� BZ�:8A �BA�8AGT4GKBAU 4A� D8�4�8 4U G�CK�4� @K�Y TB48TBC�K�8U� +A UB@8 8A�KTBA@8AGUI @4:A8GBG4�GK� D4�G8TK4 �4�8 D88A U�B�A GB D8 G�8 �B@KA4AG UC8�K8U B9 G�8 D4�G8TK4� CBCW�4GKBA E5CTKA: 8G 4�� NVV2FI K@C��KA: 4 UK:AK��4AG 8�B�B:K�4� TB�8 9BT G�8U8 BT:4AKU@U�

�Z4@KA4GKBAU B9 A4GWT4� �B@@WAKGK8U D� @B�8�W�4T C���B:8A8GK� G8��AKSW8U �4�8 T8�84�8� 4 �BAUK�8T4D�8 C���B:8A8GK� �K�8TUKG� B9 A4GWT4� CBCW�4GKBAU B9 @4:Y A8GBG4�GK� D4�G8TK4� 6�8 �4UG @4�BTKG� B9 @4:A8GBG4�GK� D4�G8TK4I KA��W�KA: �B��K 4A� TB�UI 4U �8�� 4U 4�� �W�GK�Y 4D�8 �KDTKBU 4A� UCKTK��4I 4T8 @8@D8TU B9 G�8 �Y�TBG8BY D4�G8TK4� O @BTC�B�B:K�4��� �KUGKA�GI �4T:8 @4:A8GK� TB� �4U 4UUK:A8� GB G�8 �����-���B C���W@I ��8T84U 4 ��@W�GK�8��W�4T @4:A8GK� CTB�4T�BG8�� 4A� 4 @4:A8GK� UW�94G8YT8�W�KA: D4�G8TKW@ �8T8 9BWA� GB D8�BA: GB G�8 � UWD��4UU B9 �TBG8BD4�G8TK4 Ea8�BA: 8G 4�� NVV2� 5CTKA: 4A� 5���8K98T NVVRF�

����B�,�� B�c B���,� ����,:B�,��

6�8KT �KT8�G8� @K:T4GKBA KA @4:A8GK� �8��U �4A 84UK�� D8 WU8� GB 8ATK�� @4:A8GBG4�GK� D4�G8TK4 4A� �B��8�G G�8@ 9TB@ A4GWT4� U4@C�8U KA UK:AK��4AG AW@D8TU� �B�8�8TI �8UCKG8 G�8KT WDKSWKGBWU B��WTT8A�8 4A� �K:� 4DWA�4A�8I �W�GK�4GKBA B9 @4:A8GBG4�GK� D4�G8TK4 KA G�8 �4DBT4GBT� �4U CTB�8A �K'�W�G GB 4��K8�8 4A� BA�� 4 U@4�� @KABTKG� B9 G�8 DTB4� UC8�GTW@ B9 A4GWT4��� B��WTTKA: @4:A8GBY G4�GK� D4�G8TK4 �4�8 D88A KUB�4G8� KA CWT8 �W�GWT8� aK'Y �W�GK8U KA KUB�4GKA: 4A� �W�GK�4GKA: B9 @4:A8GBG4�GK� D4�G8TK4 4TKU8 9TB@ G�8KT �K98UG��8I ��K�� KU 4�4CG8� GB U8�K@8AGU 4A� ��8@K�4��� UGT4GK�8� 4SW4GK� �4DKG4GU� OU G�CK�4� :T4�K8AG BT:4AKU@UI @4:A8GBG4�GK� D4�G8TK4 4CY C84T GB �8C8A� BA 4 �B@C�8Z C4GG8TA B9 �8TGK�4� ��8@K�4� 4A� T8�BZ :T4�K8AGUI ��K�� 4T8 �K'�W�G GB @K@K� WA�8T �4DBT4GBT� �BA�KGKBAU� �Z4@C�8U B9 KUB�4G8U G�4G �4A D8

���A D ��8�GTBA @K�TB:T4C� B9 4 .B�����-����DDME ������-OBD, c��-� �8�� 8Z�KDKGKA: G�8 ��4TY 4�G8TKUGK� @BTC�B�B:� B9 @4:A8GK� UCKTK��4� 6�8 �8�K�4� �8��U 4T8 DKCB�4T�� ;4:8��4G8� 4A� �BAG4KA WC GB b� KAGT4�8�Y �W�4T @4:A8GKG8 C4TGK��8U KA @4:A8GBUB@8UI ��K�� 4T8 4TY T4A:8� KA 4 ��4KA� E�B� 8SWK�Y 4�8AG GB ��R �@F

:TB�A WA�8T �4DBT4GBT� �BA�KGKBAU KA��W�8 U8�8T4� UGT4KAU B9 .B�����-����DDME E(K:� N� 3�4/8@BT8 8G 4�� NVcV� 3WT:8UU 8G 4�� NVV2� 5���8K98T 8G 4�� NVVN� 5��WJ �8T 4A� �BJ ��8T NVV�F� 6�B UGT4KAU B9 4 @4TKA8 @4:A8GK� �KDTKB �8T8 KUB�4G8� G�4G �4A D8 :TB�A 8KG�8T 4A48TBY DK�4��� BT @K�TB48TBDK�4��� E34M��KAU/K 8G 4�� NV))� �8��TW@ 8G 4�� NVV24F� 6�8 BA�� �W�GK�4D�8 @4:A8GK� �B��WU �4U :TB�A @K�TB48TBDK�4��� KA :T4�K8AG �W�GWT8U E�8��TW@ 8G 4�� NVV2DF� 54/4:W��K 8G 4�� ENVV2F �8T8 G�8 �TUG GB KUB�4G8 4A BD�K:4G8 4A48TBDK�I UW�94G8YT8�W�KA: @4:A8GBG4�GK� D4�G8TKW@�

�B������B�,�

O �K�8�� 4��8CG8� ��CBG�8UKU 4DBWG G�8 9WA�GKBA B9 @4:A8GBG4ZKU KU G�4GI D8�4WU8 4�� /AB�A @4:A8GBG4�GK� D4�G8TK4 4T8 8KG�8T @K�TB48TBC�K�K� BT 4A48TBDK�I G�8� U88/ GB 4�BK� �K:� BZ�:8A �8�8�U 4A� G�8KT A4�K:4GKBA 4�BA: G�8 :8B@4:A8GK� �8�� �KA8U 94�K�KG4G8U @K:T4GKBA GB G�8KT 94�BT8� CBUKGKBA KA G�8 BZ�:8A :T4�K8AG E(T4A/8� 4A� 34M��KAU/K NVV`F� 6�8 CT898TT8� @BGK�KG� �KT8�GKBA 9BWA� KA A4GWT4� CBCW�4GKBAU B9 @4:A8GBG4�GK� D4�G8TK4 KU ABTG��4T� KA G�8 :8B@4:A8GK� �8�� KA G�8 ABTG�8TA �8@KUC�8T8I ��8T84U KG KU UBWG��4T� KA G�8 UBWG�8TA �8@KUC�8T8� 38�4WU8 B9 G�8 KA��KA4GKBA B9 G�8 :8B@4:Y A8GK� �8��I @K:T4GKBA KA G�8U8 CT898TT8� �KT8�GKBAU �BW�� �4WU8 �8��U KA DBG� �8@KUC�8T8U GB U�K@ �B�A�4T�� �8�8AG �A�KA:U KA�K�4G8 G�4G G�KU CTB�8UU KU �B@C�8Z 4A� KA�B��8U KAG8T4�GKBAU �KG� 4A 48TBG4�GK� U8AUBT� @8��4Y AKU@ E(T4A/8� 8G 4�� NVVcI NVV)F� 38UK�8U @4:A8GBG4ZKUI BG�8T CBUUKD�8 9WA�GKBAU B9 KAGT4�8��W�4T KTBA �8CBUKGKBA �4�8 D88A �KU�WUU8�I KA��W�KA: KTBA �B@8BUG4UKUI 8A8T:� �BAU8T�4GKBAI BT T8�BZ ����KA: E�4AA 8G 4�� NVV�� �W8TKA 4A� 3�4/8@BT8 NVV�� 5CTKA: 8G 4�� NVV2F� 6�KU @K:�G 8ZC�4KA G�8 �4T:8 AW@D8TU B9 @4:A8GK� �T�UG4�U KA UB@8 D4�G8TK4�

Page 3: Bacterial Magnetosomes: Microbiology, Biomineralization ...materials, mainly magnetite, has been reported for an extremely diverse range of organisms including algae (Torres de Araujo

�B����������

6�8 KABT:4AK� C�4U8� @4:A8GK� @KA8T4�U

�4:A8GBUB@8U 4T8 9BWA� KA 4�� @4:A8GBG4�GK� D4�G8TK4 4A� �BAUKUG B9 @4:A8GK� KTBA @KA8T4� C4TGK��8U 8A��BU8� �KG�KA @8@DT4A8 �8UK��8U� +A @BUG �4U8U G�8 @4:A8GBY UB@8U 4T8 BT:4AKM8� KA 4 ��4KA BT ��4KAUI ��K�� 4T8 4CC4T8AG�� �Z8� �KG�KA G�8 �8��� +A @4A� @4:A8GBG4�GK� D4�G8TK4� UGT4KAU G�8 KTBA @KA8T4� C4TGK��8U �BAUKUG B9

@4:A8GKG8I (821`I 4A� 4T8 ��4T4�G8TKM8� D� A4TTB� UKM8 �KUGTKDWGKBAU 4A� WAK9BT@I UC8�K8UYUC8�K�� �T�UG4� �4DKGU E(K:� �F� 6�8 �T�UG4� �4DKGU 4�� �BAUKUG B9 �4TKBWU �B@Y DKA4GKBAU B9 G�8 KUB@8GTK� 9BT@U �NNNPI �NN�P 4A� �N��P�

���A c.�� ��8�GTBA @K�TB:T4C�U B9 �T�UG4� @BTC�B�B:K8U 4A� KAGT4Y �8��W�4T BT:4AKM4GKBA B9 @4:A8GBUB@8U 9BWA� KA �4TKBWU @4:A8GBG4�Y GK� D4�G8TK4� 5�4C8U B9 @4:A8GK� �T�UG4�U KA��W�8 �WDBYB�G4�8�T4� E.FI 8�BA:4G8� �8Z4:BA4� CTKU@4GK� E�5 25 �5 �F 4A� DW��8GYU�4C8� @BTC�BY �B:K8U EbF� 6�8 C4TGK��8U 4T8 4TT4A:8� KA BA8 E.5 �5 bFI G�B E�F BT @W�GKC�8 ��4KAU E2F BT KTT8:W�4T�� E�F� E�B� 8SWK�4�8AG GB N�� A@F

Page 4: Bacterial Magnetosomes: Microbiology, Biomineralization ...materials, mainly magnetite, has been reported for an extremely diverse range of organisms including algae (Torres de Araujo

6�8 C4TGK��8U 4T8 BTK8AG8� �KG� 4 .N N N0 �T�UG4� 4ZKU 4�BA: G�8 ��4KA �KT8�GKBA� 6�8 C4TGK��8 UKM8U 4T8 G�CK�4��� 2R-N�� A@I ��K�� KU �KG�KA G�8 C8T@4A8AGI UKA:�8Y@4:A8GK�Y �B@4KAYUKM8 T4A:8 9BT @4:A8GKG8 E�BU/B�KGM NVVRF�

+A U8�8T4� @4:A8GBG4�GK� D4�G8TK4 9TB@ @4TKA8I UW��Y �K� 8A�KTBA@8AGUI G�8 @4:A8GBUB@8 C4TGK��8U �BAUKUG B9 G�8 KTBAYUW���8 @KA8T4� :T8K:KG8I (825`I ��K�� KU KUBY UGTW�GWT4� �KG� @4:A8GKG8 4A� KU 4�UB 98TTK@4:A8GK�4��� BT�8T8�� �T8K:KG8 @4:A8GBUB@8U 4T8 4�UB ��4T4�G8TKM8� D� A4TTB� UKM8 �KUGTKDWGKBAU 4A� UC8�K8UYUC8�K�� �T�UG4� �4DKGUI DWG 4T8 BTK8AG8� �KG� 4 .N � �0 �T�UG4� 4ZKU 4�BA: G�8 ��4KA �KT8�GKBA� �BAY@4:A8GK� @4�/KA4�KG8I (85I �4U D88A 9BWA� KA �8��U �KG� :T8K:KG8 @4:A8GBUB@8U 4A� KU G�BW:�G GB D8 4 CT8�WTUBT GB :T8K:KG8 @KA8T4�KM4GKBA E�BU94K 8G 4�� NVV)F�

+G U�BW�� D8 ABG8� G�4G @8G4DB�K� 4�GK�KGK8U B9 �KUUKY @K�4GBT� KTBAYT8�W�KA: D4�G8TK4 E�B��8� 8G 4�� NV)cF 4A� UW�94G8YT8�W�KA: D4�G8TK4 �4A T8UW�G KA G�8 9BT@4GKBA B9 8ZGT4�8��W�4T @4:A8GKG8 4A� :T8K:KG8 T8UC8�GK�8��I D� CTB�8UU8U /AB�A 4U DKB�B:K�4��� KA�W�8� @KA8T4�KM4GKBA� �B�8�8TI WA�K/8 G�8 @KA8T4� C4TGK��8U KA G�8 @4:A8GBY G4�GK� D4�G8TK4I DKB�B:K�4��� KA�W�8� @KA8T4�KM4GKBA KU ABG �BAGTB��8� D� G�8 BT:4AKU@ 4A� KU ��4T4�G8TKM8� D� �B:� ABT@4� UKM8 �KUGTKDWGKBAU 4A� ABAYWAKSW8 �T�UG4� �4DKGU E5C4T/U 8G 4�� NVV�F�

��8A @4:A8GBUB@8U 4T8 4TT4A:8� KA 4 UKA:�8 ��4KAI 4U KA .B�����-����DDME UC8�K8UI @4:A8GBUG4GK� KAG8T4�Y GKBAU D8G�88A G�8 UKA:�8Y@4:A8GK� �B@4KA C4TGK��8U �4WU8 G�8 C4TGK��8 @4:A8GK� @B@8AGU GB BTK8AG UCBAG4A8BWU�� C4T4��8� GB 84�� BG�8T 4�BA: G�8 ��4KA �KT8�GKBA E(T4A/8� 4A� 3�4/8@BT8 NV)�F� 6�KU T8UW�GU KA 4 C8T@4A8AG @4:A8GK� �KCB�8 4UUB�K4G8� �KG� G�8 ��4KA �KG� 4 A4GWT4� T8@4A8AG @4:A8GKM4GKBA 4CCTB4��KA: G�8 U4GWT4GKBA @4:A8GKM4GKBA EaWAKAY3BT/B�U/K 8G 4�� NVV)F 4A� UW'Y �K8AG�� �4T:8 GB D8 BTK8AG8� 4�BA: G�8 :8B@4:A8GK� �8�� 4G 4@DK8AG G8@C8T4GWT8� 5KA�8 G�8 ��4KA B9 C4TGK��8U KU �Z8� �KG�KA G�8 �8��I G�8 8AGKT8 �8�� �K�� D8 BTK8AG8� KA G�8 �8��� 6�KU C4UUK�8 BTK8AG4GKBA T8UW�GU KA G�8 @K:T4GKBA B9 G�8 �8�� 4�BA: G�8 @4:A8GK� �8�� �KA8U 4U KG U�K@U� 6�WU

���A � �4:A8GBUB@8 C4TGK��8U KUB�4G8� 9TB@ .A ������-OBD, c��-�� 6�8 @4:A8GKG8 �T�UG4�U 4T8 G�CK�4��� `� A@ KA �K4@8G8T 4A� 4T8 UWTTBWA�8� D� G�8 @4:A8GBUB@8 @8@DT4A8 EB���OF� E�B� 8SWK�4�8AG GB �R A@F

G�8 D4�G8TK4 �4�8 8�8:4AG�� UB��8� G�8 CTBD�8@ B9 �B� GB �BAUGTW�G 4 @4:A8GK� �KCB�8 G�4G �K�� D8 BTK8AG8� KA G�8 :8B@4:A8GK� �8�� �8G �G KAUK�8 4 @K�TB@8G8TYUKM8� �8��� 6�8 UB�WGKBA KU D4U8� BA G�8 4DK�KG� B9 G�8 D4�G8TK4 GB �BAGTB� G�8 @KA8T4� G�C8 B9 G�8 KTBAI G�8 UKM8 4A� BTK8AY G4GKBA B9 G�8 C4TGK��8UI 4A� G�8KT C�4�8@8AG KA G�8 �8���

6�8 BT:4AK� C�4U8� G�8 @4:A8GBUB@8 @8@DT4A8

+A 4�� @4:A8GKG8YCTB�W�KA: @4:A8GBG4�GK� D4�G8TK4 8ZY 4@KA8� GB �4G8I G�8 @4:A8GBUB@8 @KA8T4� C�4U8 4CC84TU GB D8 8A�8�BC8� D� 4 @8@DT4A8 E(K:� 2� �BTD� 8G 4�� NV))� �4GUWA:4 NVVN� 5��WJ �8T 4A� 348W8T�8KA NVVcDF� O�G�BW:� G�8 @4:A8GBUB@8 @8@DT4A8 �B8U ABG 4CC84T GB D8 �BAGK:WBWU �KG� G�8 �8�� @8@DT4A8 KA 8�8�GTBAY @K�TBU�BCK� K@4:8UI KG �4A D8 UC8�W�4G8� G�4G UB@8 UBTG B9 �BAA8�GKBA BT 4UUB�K4GKBA �KG� G�8 ��GBC�4U@K� @8@DT4A8 8ZKUGU� 6�KU �BW�� �8�C 8ZC�4KA G�8 DKBU�AY G�8GK� BTK:KA B9 G�8 @4:A8GBUB@8 �B@C4TG@8AG� O @8@DT4ABWU ��UWC8TUGTW�GWT8�� @4� 4�UB 4��BWAG 9BT G�8 KAG8:TKG� B9 �B@C�8Z KAGT4�8��W�4T 4TT4A:8@8AGU B9 @4:A8GBUB@8 C4TGK��8U 9BWA� KA UB@8 @4:A8GBG4�GK� D4�G8TK4� �@CG� 4A� C4TGK4��� ���8� �8UK��8U �4�8 D88A BDU8T�8� KA KTBAYUG4T�8� �8��U B9 .A EB������B����ME 4A� .A ������-OBDc��-� E�BTD� 8G 4�� NV))� 5��WJ �8T 4A� 348W8T�8KA NVVcDFI UB KG U88@U �K/8�� G�4G G�8 @4:A8GBY UB@8 @8@DT4A8 CT8Y8ZKUGU 4U 4A ��8@CG��� �8UK��8 CTKBT GB G�8 DKB@KA8T4�KM4GKBA B9 G�8 @KA8T4� C�4U8�

+A UGT4KAU B9 .B�����-����DDMEI G�8 @4:A8GBUB@8 @8@DT4A8 �4U 9BWA� GB �BAUKUG B9 4 DK�4�8T �BAG4KAKA: C�BUC�B�KCK�U 4A� CTBG8KAUI 4G �84UG U8�8T4� B9 ��K�� 4CC84T WAKSW8 GB G�KU @8@DT4A8 E�BTD� 8G 4�� NV))� 5��WJ �8T 4A� 348W8T�8KA NVVcDF� O�G�BW:� G�8 CTBG8KA C4GG8TAU B9 G�8 @4:A8GBUB@8 @8@DT4A8 4T8 �KUGKAY :WKU�4D�8 D8G�88A �K�8T8AG UGT4KAU B9 .B�����-����DDMEI 4G �84UG BA8 @4�BT CTBG8KA �KG� 4 @B�8�W�4T �8K:�G B9 4DBWG ��-�` /a4 4CC84TU GB D8 �B@@BA GB 4�� UGT4KAU G8UG8� UB 94TI 4U T8�84�8� D� U8SW8A�8 4A4��UKU 4A�

Page 5: Bacterial Magnetosomes: Microbiology, Biomineralization ...materials, mainly magnetite, has been reported for an extremely diverse range of organisms including algae (Torres de Araujo

4AGKDB�� �TBUUYT84�GK�KG� E1/W�4 8G 4�� NVVb� 5��WJ �8T 8G 4�� NVVcF�

%B@C4TG@8AG4�KM4GKBA G�TBW:� G�8 9BT@4GKBA B9 G�8 @4:A8GBUB@8 �8UK��8 8A4D�8U G�8 CTB�8UU8U B9 @KA8T4� 9BT@4GKBA GB D8 T8:W�4G8� D� DKB��8@K�4� C4G��4�U� 6�8 @8@DT4A8 @4� 4�G 4U 4 CBG8AGK4� :4G8 9BT �B@CBUKGKBA4�I C� 4A� T8�BZ �K�8T8AGK4GKBA D8G�88A G�8 �8UK��8 4A� G�8 �8��W�4T 8A�KTBA@8AG� O�G�BW:� G�8 8Z4�G TB�8 B9 G�8 @4:A8GBUB@8YUC8�K�� CTBG8KAU �4U ABG D88A 8�W�K�4G8�I KG �4U D88A UC8�W�4G8� G�4G G�8U8 �4�8 UC8�K�� 9WA�GKBAU KA G�8 4��W@W�4GKBA B9 KTBAI AW��84GKBA B9 @KA8T4�U 4A� T8�BZ 4A� C� �BAGTB� E�BTD� 8G 4�� NV))� �4AA 8G 4�� NVV�F�

EI��,����� B�c a,��I��,���� �� aB����,B� �B����,�� a,��,���B�,RB�,��

6�8 �TUG UG8C KA @4:A8GKG8 U�AG�8UKU KA @4:A8GBG4�GK� D4�G8TK4 KU G�8 WCG4/8 B9 KTBA� 38�4WU8 B9 G�8 �4T:8 4@BWAGU B9 KTBA T8SWKT8� 9BT @4:A8GKG8 U�AG�8UKUI @4:Y A8GBG4�GK� D4�G8TK4 �4A D8 8ZC8�G8� GB WU8 �8T� 8'�K8AG WCG4/8 U�UG8@U� 6�8 4UUK@K�4GKBA B9 KTBA @WUG D8 UGTK�G�� �BAGTB��8� D8�4WU8 B9 G�8 CBG8AGK4��� �4T@9W� 8�8�GU B9 8Z�8UU KAGT4�8��W�4T KTBA E�W8TKABG NVV`F� 58�8T4� UGW�K8UI 4�� KA�B��KA: @4:A8GK� UCKTK��4I �4�8 9B�WU8� BA KTBA WCG4/8� �4B�8GGK 4A� 3�4/8@BT8 ENV)bF T8CBTG8� G�8 CTB�W�GKBA B9 4 ���TBZ4@4G8YG�C8 UK�8TBC�BT8 K9 �8��U B9 .A EB������B����ME �8T8 :TB�A WA�8T �BA�KGKBAU B9 �K:� KTBA� �B�8�8TI G�8U8 T8UW�GU �4�8 ABG D88A T8C�KY �4G8� KA BG�8T UGW�K8U 4A� AB �BA��WUK�8 8�K�8A�8 9BT G�8 KA�B��8@8AG B9 UK�8TBC�BT8U KA G�8 9BT@4GKBA B9 @4:Y A8GKG8 �4U D88A 9BWA� UB 94T� �4/4@WT4 8G 4�� ENVV2DF ��CBG�8UKM8� G�4G 98TTK� KTBA �4U G4/8A WC KA .B���, ��-����DDME O�3YN D� 4 C8TKC�4U@K� DKA�KA:YCTBG8KAY �8C8A�8AG KTBAYGT4AUCBTG U�UG8@� +A .A ������-OBDc��-�I KG �4U 9BWA� G�4G G�8 @4�BT CBTGKBA B9 G�8 KTBA KU G4/8A WC 4U (8E+++F KA 4A 8A8T:�Y�8C8A�8AG CTB�8UU E5��WJ �8T 4A� 348W8T�8KA NVVbF� 6�8 BDU8T�8� �K:� T4G8U B9 98TTK� KTBA WCG4/8 @4� T8;8�G G�8 8ZGT4BT�KA4T� T8SWKT8@8AG 9BT KTBA KA G�8U8 BT:4AKU@U� 3BG� G�8 4@BWAG B9 @4:Y A8GKG8 9BT@8� 4A� G�8 T4G8 B9 98TTK� KTBA WCG4/8 �8T8 ��BU8 GB U4GWT4GKBA 4G 8ZGT4�8��W�4T KTBA �BA�8AGT4GKBAU B9 NR-�� �� (8I KA�K�4GKA: G�4G G�KU D4�G8TKW@ KU 4D�8 GB 4��W@W�4G8 �BCKBWU 4@BWAGU B9 KTBA 9TB@ T8�4GK�8�� �B� 8A�KTBA@8AG4� �BA�8AGT4GKBAU�

6�8 DKB@KA8T4�KM4GKBA B9 @4:A8GK� �T�UG4�U �B8U ABG B��WT �BAUGKGWGK�8��I DWG �4T:8�� �8C8A�U BA G�8 :TB�G� �BA�KGKBAU� 38UK�8U G�8 4�4K�4DK�KG� B9 @K�TB@B�4T 4@BWAGU B9 KTBAI @K�TB48TBDK� �BA�KGKBAU 4T8 T8SWKT8� 9BT @4:A8GKG8 9BT@4GKBA KA .B�����-����DDME UC8�K8U E3�4/8@BT8 8G 4�� NV)R� 5��WJ �8T 4A� 348W8T�8KA NVV)F� %8��U B9 .A ������-OBDc��-� 4T8 ABAY@4:A8GK� �WTKA: 48TBDK� :TB�G�I DWG UG4TG GB CTB�W�8 (821` K@@8�K4G8�� 49G8T G�8 8UG4D�KU�@8AG B9 @K�TB48TBDK� �BA�KGKBAU �BTY T8UCBA�KA: GB 4A BZ�:8A �BA�8AGT4GKBA B9 4DBWG N�-2� U4GWT4GKBA E(K:� `F� 6�8 4��W@W�4GKBA B9 KTBA �WTKA: :TB�G� KU 4CC4T8AG�� GK:�G�� �BWC�8� GB G�8 KA�W�GKBA B9 @4:A8GKG8 DKB@KA8T4�KM4GKBA� ��K�8 G�8 KAGT4�8��W�4T KTBA

���A 3 �TB�G� E�FI @4:A8GKU@ E.FI 4A� �KUUB��8� BZ�:8A �BA�8AY GT4GKBA Eb�F KA 4 �W�GWT8 B9 .A ������-OBDc��-� 4G �BAUG4AG 48T4GKBA� %�4A:8U KA @4:A8GKU@ B9 G�8 �8�� UWUC8AUKBA �8T8 @BAKGBT8� D� @84UWT8@8AG B9 �K�8T8AGK4� �K:�G U�4GG8TKA: E5��WJ �8T 8G 4�� NVVRF� :TB�G� �4U @84UWT8� D� 4DUBTD4A�8� 6�8 �8��U �8T8 ABAY@4:A8GK� �WTKA: 48TBDK� :TB�G�� O9G8T �� � G�8 CTB�W�GKBA B9 (821` �4U KA�W�8� D� G�8 8UG4D�KU�@8AG B9 @K�TB48TBDK� �BA�KGKBAUI �BTT8UCBA�Y KA: GB 4A BZ�:8A �BA�8AGT4GKBA B9 4DBWG N�-2� U4GWT4GKBA

�BAG8AG KA ABAY@4:A8GK� �8��U KU T8�4GK�8�� �B�I @4:A8GK� �8��U �4A �BAG4KA @BT8 G�8A �� KTBA BA 4 �T�Y�8K:�G D4U8 E5��WJ �8T 4A� 348W8T�8KA NVV)F�

+A 4A 8�BTG GB 8�W�K�4G8 G�8 T8�4GKBAU�KC D8G�88A T8UCKT4GBT� 8�8�GTBA GT4AUCBTG KA AKGT4G8 4A� BZ�:8A WGK�KM4GKBA 4A� @4:A8GKG8 U�AG�8UKUI ��GB��TB@8U KA .A EB������B����ME �4�8 D88A 8Z4@KA8�� 64@8:4K 8G 4�� ENVV2F T8CBTG8� 4 AB�8� ����GB��TB@8Y4NY�K/8�� �8@BY CTBG8KA G�4G �4U KA :T84G8T 4@BWAGU KA @4:A8GK� �8��U G�4A KA ABA@4:A8GK� �8��U� O A8� ���YG�C8 ��GB��TB@8 � BZK�4U8 E64@8:4K 4A� (W/W@BTK NVV`F 4A� 4 ��GBY ��TB@8 �cNYG�C8 AKGTKG8 T8�W�G4U8 E�4@4M4/K 8G 4�� NVVRF �8T8 KUB�4G8� 4A� CWTK�8� 9TB@ .A EB������B����ME� 6�8 �4GG8T CTBG8KA KU B9 C4TGK�W�4T KAG8T8UG UKA�8 KG U�B�8� (8E++F�AKGTKG8 BZK�BT8�W�G4U8 4�GK�KG�� +G �4U 4�UB D88A BDU8T�8� G�4G G�8 9BT@4GKBA B9 @4:A8GKG8 �4U 8A�4A�8� K9 �8��U B9 .A EB������B����ME �8T8 :TB�KA: D� �KUUKY @K�4GBT� AKGT4G8 T8�W�GKBA E3�4/8@BT8 8G 4�� NV)RF� 1A G�8 D4UKU B9 G�8U8 BDU8T�4GKBAUI KG �4U CTBCBU8� D� (W/W@BTK 8G 4�� ENVVcF G�4G G�8 �KUUK@K�4GBT� AKGTKG8 T8�W�G4U8 B9 .A EB������B����ME �BW�� 9WA�GKBA 4U 4A (8E++F BZK�KMKA: 8AM�@8 9BT @4:A8GKG8 U�AG�8UKU WA�8T 4A48TBDK� �BA�KGKBAU�

(T4A/8� 8G 4�� ENV)2F 8Z4@KA8� G�8 A4GWT8 4A� �KUY GTKDWGKBA B9 @4�BT KTBA �B@CBWA�U KA .A EB�����, �B����ME D� WUKA: (8YRc �BJ ,D4W8T UC8�GTBU�BC�� 6�8� CTBCBU8� 4 @B�8� KA ��K�� (8E+++F KU G4/8A WC D� G�8 �8�� 4A� T8�W�8� GB (8E++F 4U KG 8AG8TU G�8 �8��� +G KU G�8A G�BW:�G GB D8 T8BZK�KM8� GB 9BT@ 4 �B�Y�8AUKG� ���TBWU (8E+++F BZK�8I ��K�� KU G�8A �8���T4G8� GB 9BT@ 4 �K:�Y �8AUKG� (8E+++F BZK�8 E98TTK���TKG8FI ��K�� �4A D8 �KT8�G�� BDU8T�8� KA �8��U� +A G�8 �4UG UG8CI BA8YG�KT� B9 G�8 (8E+++F KBAU KA 98TTK���TKG8 4T8 T8�W�8� 4A�I �KG� 9WTG�8T �8��Y �T4GKBAI @4:A8GKG8 KU CTB�W�8�� +G KU G�BW:�G G�4G G�8

Page 6: Bacterial Magnetosomes: Microbiology, Biomineralization ...materials, mainly magnetite, has been reported for an extremely diverse range of organisms including algae (Torres de Araujo

�A4� G�B UG8CU B��WT �KG�KA G�8 @4:A8GBUB@8 �8UK��8I ��K�� 4�GU 4U 4 9WTG�8T �BAUGT4KAG BA �T�UG4� :TB�G��

�������B� a,����� �� �B������B��,� aB����,B

OGG8@CGU GB 4��T8UU G�8 @B�8�W�4T DKB�B:� B9 @4:A8Y GBUB@8 9BT@4GKBA �4�8 D88A �4@C8T8� D� U8�8T4� CTBD�8@U KA��W�KA: G�8 �4�/ B9 4 UK:AK��4AG AW@D8T B9 @4:A8GBG4�GK� D4�G8TK4� UGT4KAUS G�8 94UGK�KBWUA8UU B9 G�8 BT:4AKU@U KA �W�GWT8I G�8 8�4DBT4G8 G8��AKSW8U T8SWKT8� 9BT G�8 :TB�G� B9 G�8U8 BT:4AKU@U 4A� G�8 KA4DK�KG� B9 4�@BUG 4�� G�8U8 UGT4KAU GB :TB� BA G�8 UWT94�8 B9 4:4T C�4G8U WU8� GB U�T88A 9BT @WG4AGU� 6�8T89BT8I BWT /AB��8�:8 B9 G�8 :8A8GK� �8G8T@KA4GKBA B9 @4:A8GBUB@8 9BT@4GKBA KU UGK�� 9T4:@8AG4T��

+AKGK4� UGW�K8U 4��T8UUKA: @B�8�W�4T :8A8GK�U KA @4:Y A8GBG4�GK� D4�G8TK4 �8T8 @4�8 �KG� .A EB������B����ME UGT4KA �5YN� +G �4U U�B�A G�4G 4G �84UG UB@8 B9 G�8 :8A8U B9 G�KU BT:4AKU@ �4A D8 9WA�GKBA4��� 8ZCT8UU8� KA N-�, �������B ��D� 4A� G�4G G�8 GT4AU�TKCGKBA4� 4A� GT4AU�4Y GKBA4� 8�8@8AGU B9 G�8 G�B @K�TBBT:4AKU@U 4T8 �B@C4GKD�8� 38TUBA 8G 4�� ENV)VF �8T8 4D�8 GB ��BA8 4A� 9WA�GKBA4��� 8ZCT8UU G�8 ���� :8A8 9TB@ .A EB�����, �B����ME KA NA ��D�A 6�8� G�8A ��BA8� 4 �Y/D a�O 9T4:@8AG 9TB@ .A EB������B����ME G�4G �B@C�8@8AG8� KTBAYWCG4/8 �8��K8A�K8U KA NA ��D� 4A� �BDE���DDB ����, �EM��ME @WG4AGU �4�/KA: 4 9WA�GKBA4� B��a :8A8 EDKBY U�AG�8GK� �8���TBSWKA4U8F� 6�KU UW::8UGU G�4G G�8 �Y/D a�O 9T4:@8AG @4� �4�8 4 9WA�GKBA KA KTBA WCG4/8 KA .A EB������B����ME E38TUBA 8G 4�� NVVNF�

�4GUWA4:4 8G 4�� ENVV�F 4GG8@CG8� GB 8UG4D�KU� 4 :8Y A8GK� U�UG8@ KA .B�����-����DDME UGT4KA O�3YNA %8��U B9 G�KU UC8�K8U �8T8 T8CBTG8� GB 9BT@ @4:A8GK� �B�BAK8U BA G�8 UWT94�8 B9 4:4T C�4G8U ��8A :TB�A WA�8T 4A KA�WY D4GKBA 4G@BUC�8T8 �BAG4KAKA: �� BZ�:8AA 6�KU 984GWT8 94�K�KG4G8� G�8 U8�8�GKBA B9 ABAY@4:A8GK� @WG4AGU B9 .B�����-����DDME UGT4KA O�3YN D� 6AR @WG4:8A8UKU D� �BA�W:4� GT4AU98T� +G �4U �BA��W�8� G�4G 4G �84UG G�T88 T8:KBAU B9 G�8 ��TB@BUB@8 4T8 T8SWKT8� 9BT G�8 U�AG�8UKU B9 @4:A8GBUB@8U� 1A8 B9 G�8U8 T8:KBAU �4U 9BWA� GB �BAG4KA 4 :8A8S �8UK:A4G8� EB��I G�4G 8A�B�8U 4 CTBG8KA G�4G KU �B@B�B:BWU GB �4GKBA 8�WZ CTBG8KAUS KA C4TGK�Y W�4T G�8 NA ��D� CBG4UUKW@YKBAYGT4AU�B�4GKA: CTBG8KA �89% E�4/4@WT4 8G 4�� NVVR4FA �8@DT4A8 �8UK��8U CT8C4T8� 9TB@ NA ��D� �8��U 8ZCT8UUKA: EB�� GBB/ WC KTBA ��8A O6� �4U UWCC�K8�I KA�K�4GKA: G�4G 8A8T:� �4U T8Y SWKT8� 9BT G�8 WCG4/8 B9 KTBA� 6�8 8ZCT8UUKBA B9 EB�� �4U 8A�4A�8� ��8A �K��YG�C8 .B�����-����DDME O�3YN �8��U �8T8 :TB�A WA�8T KTBAY�K@KG8� �BA�KGKBAU T4G�8T G�4A KTBAYUW'�K8AG �BA�KGKBAU KA ��K�� G�8� �BW�� CTB�W�8 @BT8 @4:A8GBUB@8U E�4/4@WT4 8G 4�� NVVRDF� 6�WUI G�8 TB�8 B9 G�8 EB�� :8A8 KA @4:A8GBUB@8 U�AY G�8UKU KU WA��84T�

1/W�4 8G 4�� ENVVbF GBB/ 4 ��T8�8TU8 :8A8GK�U�� 4CY CTB4�� GB G�8 @4:A8GBUB@8 CTBD�8@� 6�8� WU8� G�8 �YG8T@KA4� 4@KAB 4�K� U8SW8A�8 9TB@ 4 ��Y/a4 CTBG8KA UC8�K��4��� 4UUB�K4G8� �KG� G�8 @4:A8GBUB@8 @8@DT4A8 GB ��BA8 4A� U8SW8A�8 KGU :8A8� 1A G�8 D4UKU B9 G�8 4@KAB

4�K� U8SW8A�8I G�8 CTBG8KA 8Z�KDKGU UK:AK��4AG �B@B�B:� �KG� 4 AW@D8T B9 9WA�GKBA4��� �K�8TU8 CTBG8KAU D8�BA:KA: GB G�8 G8GT4GTK�BC8CGK�8 T8C84G 94@K��� �B�8�8TI G�8 TB�8 B9 G�8 CTBG8KA KA @4:A8GBUB@8 U�AG�8UKU �4U ABG �8G D88A 8�W�K�4G8��

�B�� ����,:B�,�� B�c ,���B�,�� �� �B����������

1A�� 4 �K@KG8� AW@D8T B9 @4:A8GBG4�GK� D4�G8TK4 �4�8 D88A KUB�4G8� KA CWT8 �W�GWT8 UB 94T� �BUG B9 G�8 KUB�4G8U 4T8 CBBT�� ��4T4�G8TKM8� KA G8T@U B9 :TB�G� �BA�KGKBAU 4A� C��UKB�B:�� 6�8T89BT8I U8�8T4� .B�����-����DDME UGT4KAU �4�8 D88A WU8� 9BT G�8 KUB�4GKBA B9 @4:A8GBUB@8U G�4G �4A D8 :TB�A @K�TB48TBDK�4��� BA UK@C�8 @8�K4 �BAG4KAKA: U�BTG BT:4AK� 4�K�U 4U 4 �4TDBA UBWT�8 4A� 98TTK� ��8�4G8U 4U 4 UBWT�8 B9 KTBA E3�4/8@BT8 8G 4�� NVcV� 5��WJ �8T 4A� 348W8T�8KA NVVb� �4GUWA4:4 8G 4�� NVV�F� 6�8 �8��U �4�8 4 UGTK�G�� BZ�:8AY�8C8A�8AG T8UCKT4GBT� G�C8 B9 @8G4DB�KU@I DWG �B ABG GB�8T4G8 �K:�8T BZ�:8A �BA�8AGT4GKBAU� OU :TB�G� 4A� @4:A8GBUB@8 9BT@4GKBA �8C8A� BA @K�TB48TBDK� �BA�KGKBAUI G�8 �BAGTB� B9 4 �B� BZ�:8A �BA�8AGT4GKBA KA G�8 :TB�G� @8�KW@ EN�-2�F 1� KU B9 �TKGK�4� K@CBTG4A�8 E3�4/8@BT8 8G 4�� NV)R� 5��WJ �8T 4A� 348W8T�8KA NVV)F�

.A EB������B����ME �4U G�8 �TUG @4:A8GBG4�GK� D4�G8TKW@ 4�4K�4D�8 KA CWT8 �W�GWT8 4A� �4U WU8� KA G�8 KAKGK4� UGW�K8U� 1A8 B9 G�8 T84UBAU 9BT BZ�:8A U8AUKGK�KG� KA G�KU BT:4AKU@ @4� D8 G�8 �4�/ B9 G�8 BZ�:8AYCTBG8�Y GK�8 8AM�@8 �4G4�4U8� O��KGKBA B9 �4G4�4U8 GB G�8 :TB�G� @8�KW@ T8UW�G8� KA KA�T84U8� BZ�:8A GB�8T4A�8 E3�4/8Y @BT8 8G 4�� NVcVF� .A ������-OBDc��-� 4A� .B�����-, ����DDME O�3YN 4T8 @BT8 BZ�:8AYGB�8T4AG 4A� 84UK8T GB :TB� BA 4 �4T:8 U�4�8� +9 :TB�A 9TB@ �4T:8 KAB�W�4I �W�GWT8U 4T8 GB�8T4AG GB 4G@BUC�8TK� 4KTI ��K�� BD�K4G8U G�8 A88� 9BT 8�4DBT4G8 @K�TB48TBDK� G8��AKSW8U� 6�8 @4ZK@W@ �8�� �K8��U T8CBTG8� UB 94T 4T8 ��22 :�� E�T� �8K:�GF 9BT .A ������-OBDc��-� :TB�A KA 4 N��Y� 98TY @8AG8T E5��WJ �8T 4A� 348W8T�8KA NVVc4F 4A� ��2` :�� 9BT .B�����-����DDME O�3YN :TB�A 4G 4 `Y� U�4�8 E�4GUWY A4:4 8G 4�� NVVcF�

68��AKSW8U 9BT G�8 KUB�4GKBA 4A� CWTK��4GKBA B9 @4:A8GBUB@8 C4TGK��8U 9TB@ .B�����-����DDME UC8�K8U 4T8 D4U8� BA @4:A8GK� U8C4T4GKBA E�BTD� 8G 4�� NV))� 1/W�4 8G 4�� NVVbF BT 4 �B@DKA4GKBA B9 4 UW�TBU8Y:T4Y �K8AG �8AGTK9W:4GKBA 4A� 4 @4:A8GK� U8C4T4GKBA G8��Y AKSW8 E5��WJ �8T 4A� 348W8T�8KA NVVcDF� 6�8U8 CTB�8�WT8U �84�8 G�8 UWTTBWA�KA: @8@DT4A8 KAG4�G 4A� @4:A8GBY UB@8 CT8C4T4GKBAU 4T8 4CC4T8AG�� 9T88 B9 �BAG4@KA4GKA: @4G8TK4�� 1�KA: GB G�8 CT8U8A�8 B9 G�8 8A�8�BCKA: @8@DT4A8I KUB�4G8� @4:A8GBUB@8 C4TGK��8U 9BT@ UG4D�8I �8��Y�KUC8TU8� UWUC8AUKBAU E(K:� RF� O9G8T UB�WDK�KM4GKBA B9 G�8 @8@DT4A8 D� 4 �8G8T:8AGI G�8 T8@4KAKA: KABT:4AK� �T�UG4�U G8A� GB 4::�B@8T4G8 4U 4 T8UW�G B9 @4:A8GK� 4GY GT4�GK�8 9BT�8U� 6�CK�4���I ��b @: D4�G8TK4� @4:A8GKG8 �4A D8 �8TK�8� 9TB@ 4 N���Y@� �W�GWT8 B9 .B�����-����DDME O�3YN E�4GUWA4:4 8G 4�� NVVcFI ��K�8 4 UK@K�4T �K8�� �4U T8CBTG8� 9BT .A ������-OBDc��-� E5��WJ �8T 4A� 348W8T�8KA NVVc4F�

Page 7: Bacterial Magnetosomes: Microbiology, Biomineralization ...materials, mainly magnetite, has been reported for an extremely diverse range of organisms including algae (Torres de Araujo

���A 4 �WTK�8� @4:A8GBUB@8U 9TB@ .A ������-OBDc��-�� 1�Y KA: GB G�8 CT8U8A�8 B9 G�8 8A�8�BCKA: @8@DT4A8I KUB�4G8� @4:A8GBUB@8 C4TGK��8U 9BT@ UG4D�8I �8��Y�KUC8TU8� UWUC8AY UKBAU E�B� 8SWK�4�8AG GB N�� A@F

�,����I�����,�B� B���,�B�,���

6�8 9BT@4GKBA B9 @4:A8GK� C4TGK��8U �KG�KA DKB�B:K�4� @8@DT4A8U KU B9 :T84G KAG8T8UG KA G8T@U B9 9BT@KA: U@4�� U�AG�8GK� C4TGK��8U WA�8T ��BU8�� �BAGTB��8� U�AG�8UKU �BA�KGKBAU� 5@4�� @4:A8GK� C4TGK��8U �4A D8 9BT@8� U�AY G�8GK�4��� D� 9B��B�KA: �4TKBWU TBWG8U� �B�8�8TI C4TGK��8U 9BT@8� G�KU �4� 4T8 ABAYWAK9BT@I B9G8A ABG 9W��� �T�UY G4��KA8I �B@CBUKGKBA4��� ABA�B@B:8A8BWUI 4A� KA 4A 4::�B@8T4G8� UG4G8I ��K�� K@CBU8U CTBD�8@U KA CTBY �8UUKA: E54TK/4�4 NVV`F� 6�8T89BT8I G�8KT U�AG�8UKU D� 4 DKB�B:K�4� CTB�8UU CTB@KU8U 4��4AG4:8U KA G8T@U B9 �BAY GTB��KA: :TB�G� 4A� @BTC�B�B:K�4� CTBC8TGK8U� �BT8Y B�8TI DKB@KA8T4�KM4GKBA CTB�K�8U 4 �4� GB CTB�W�8 �K:��� WAK9BT@ @4:A8GKG8 �T�UG4�U �KG�BWG G�8 �T4UGK� T8:K@8U B9 G8@C8T4GWT8I C� 4A� CT8UUWT8 G�4G 4T8 B9G8A A88�8� 9BT G�8KT KA�WUGTK4� CTB�W�GKBA E�4AA 8G 4�� NVV�F� 5BBA 49Y G8T G�8 �KU�B�8T� B9 @4:A8GBG4�GK� D4�G8TK4I G�8KT DKBY G8��AB�B:K�4� CBG8AGK4� �4U T84�KM8� 4A� AW@8TBWU �B@@8T�K4� WU8U B9 G�8 U@4�� @4:A8GK� �T�UG4�U �4�8 D88A �BAG8@C�4G8�� �Z4@C�8U 9BT G�8 WU8 B9 @4:A8GK� @K�TBY BT:4AKU@U :8A8T4��� 94�� KAGB G�B �4G8:BTK8UI ��K�� KAY �B��8 8KG�8T ��B�8I �K�KA: �8��U 4A� G�8KT @4:A8GBG4�GK� D8�4�KBT BT WGK�KM8 KUB�4G8� @4:A8GBUB@8 C4TGK��8U�

OCC�K�4GKBAU B9 @4:A8GK� �8��U

OCC�K�4GKBAU D4U8� BA G�8 �TUG �4G8:BT� KA��W�8 G�8 WU8 B9 @4:A8GBG4�GK� D4�G8TK4 9BT G�8 ABA�8UGTW�GK�8 �B@4KA 4A4��UKU B9 UB9G @4:A8GK� @4G8TK4�U� ��8A @BGK�8 @4:Y A8GBG4�GK� �B��K �8T8 4CC�K8� GB G�8 U4@C�8 UWT94�8I G�8 D4�G8TK4 BTK8AG8�I @K:T4G8� 4A� 4��W@W�4G8� KA G�8 UGT4� �8��U BTK:KA4GKA: 9TB@ G�8 @4:A8GK� �B@4KAUI 4��B�KA: �KUW4�KM4GKBA B9 G�8 �B@4KA UGTW�GWT8 E�4T4U/B 8G 4�� NVV2I NVVRF� 7UKA: 4 UK@K�4T G8��AKSW8I (WA4/K 8G 4�� ENVV�F 8@C�B�8� @4:A8GBG4�GK� D4�G8TK4 GB �B�4G8 @4:Y

A8GK� CB�8U BA @8G8BTKGK� @4:A8GK� :T4KAU� 34�4� 8G 4�� ENVV`I NVV)F �BAUK�8T8� G�8 WU8 B9 @4:A8GBG4�GK� D4�G8Y TK4 9BT G�8 T8@B�4� B9 �84�� @8G4�U 4A� T4�KBAW��K�8U 9TB@ �4UG8�4G8T� �K:�Y:T4�K8AG @4:A8GK� U8C4T4GKBA 4U �8�� 4U 4 �B�Y@4:A8GK� �8�� U�UG8@ D4U8� BA G�8KT �KY T8�G8� @BGK�KG� �4�8 D88A WU8� GB T8@B�8 @8G4�Y�B4�8� D4�G8TK4 9TB@ �4G8T� O ��@K�TBDK4� @4:A8GB@8G8T�� �4U �8�KU8� 9BT G�8 CT8�K�GKBA B9 BZ�:8A �8C�8GKBA KA DBGGB@ U8�K@8AGU 4A� B�8T��KA: �4G8TI ��K�� KU D4U8� BA G�8 @4:A8GBG4�GK� 4A� @K�TB48TBC�K�K� D8�4�KBT B9 A4GWT4� CBCW�4GKBAU B9 @4:A8GBG4�GK� D4�G8TK4I GT4�/KA: G�8KT CBUKGKBA 4A� @4:A8GK� UGT8A:G� D� 4 @4:A8GK� U8AUBT E��B4�U NVVRF� O�� G�8 8Z4@C�8U �8U�TKD8� 4DB�8 T8�� BA �K�KA:I 4�GK�8�� U�K@@KA: 4A� C4TGK4��� ABAY�W�GK�4D�8 @4:A8GBG4�GK� D4�G8TK4� 38�4WU8 B9 G�8 94UGK�KBWUA8UU 4A� �K@KG8� 4�4K�4DK�KG� B9 G�8U8 D4�G8TK4I CT4�GK�4� 4CC�K�4GKBAU T8@4KA KA SW8UGKBA�

OCC�K�4GKBAU B9 KUB�4G8� @4:A8GBUB@8 C4TGK��8U

6�8 U@4�� UKM8 B9 KUB�4G8� @4:A8GBUB@8 C4TGK��8U CTB�K�8U 4 �4T:8 UWT94�8YGBY�B�W@8 T4GKBI ��K�� @4/8U G�8@ WU89W� 4U �4TTK8TU 9BT G�8 K@@BDK�KM4GKBA B9 T8�4GK�8�� �4T:8 SW4AGKGK8U B9 DKB4�GK�8 UWDUG4A�8UI ��K�� �4A G�8A U8C4Y T4G8� D� @4:A8GK� �8��U� +A KAKGK4� UGW�K8UI D4�G8TK4� @4:A8GBUB@8U 9TB@ ABAY�W�GK�4D�8 @4:A8GBG4�GK� D4�Y G8TK4 �8T8 WU8� 9BT K@@BDK�KMKA: G�8 8AM�@8U :�W�BU8 BZK�4U8 4A� WTK�4U8 4U �B@CBA8AGU B9 @8�K�4��� K@CBTY G4AG DKBU8AUBTU� 6�8 :�W�BU8 BZK�4U8 DBWA� GB DKB:8AK� @4:A8GKG8 C4TGK��8U �4� `�Y9B�� �K:�8T 4�GK�KG� G�4A G�8 U4@8 8AM�@8 DBWA� GB 4TGK��K4� @4:A8GKG8 4A� �KA� 98TY TKG8 C4TGK��8U KA G�KU UGW�� E�4GUWA4:4 4A� �4@�K4 NV)cF�

�4:A8GBUB@8U �4�8 D88A 4�UB WU8� 9BT G�8 :8A8T4Y GKBA B9 @4:A8GK� 4AGKDB�K8U� (B��B�KA: GT84G@8AG �KG� :�WG4T4��8���8I D4�G8TK4� @4:A8GKG8 C4TGK��8U �8T8 �BWY C�8� GB 4AGKDB�K8U GB 9BT@ �BA�W:4G8U� +A BA8 8Z4@C�8I @4:A8GK� 4AGKDB�K8U �BW�� D8 WU8� 9BT G�8 SW4AGK��4GKBA

Page 8: Bacterial Magnetosomes: Microbiology, Biomineralization ...materials, mainly magnetite, has been reported for an extremely diverse range of organisms including algae (Torres de Araujo

B9 +:�� 6�8 CTB�8�WT8 KA�B��8� K@@BDK�KMKA: ;WBT8UY �8KAYKUBG�KB��4A4G8Y�BA�W:4G8� 4AGKYE@BWU8 +:�F 4AGKY DB�K8U BA D4�G8TK4� @4:A8GBUB@8 C4TGK��8U E�4/4@WT4 8G 4�� NVVNF� 6�8 CT8U8A�8 B9 G�8 @4:A8GBUB@8 @8@Y DT4A8 T8UW�G8� KA �KUC8TUKBA 4A� �4A��KA: CTBC8TGK8U UWC8TKBT GB G�BU8 B9 U�AG�8GK� @4:A8GK� C4TGK��8 �BA�WY :4G8U E�4GUWA:4 NVVNF� 1G�8T T8CBTG8� 8Z4@C�8U 9BT G�8 4CC�K�4GKBA B9 4AGKDB�K8U K@@BDK�KM8� BA D4�G8TK4� @4:A8GBUB@8U KA��W�8 G�8 �8G8�GKBA 4A� T8@B�4� B9 NA ��D� �8��U 9TB@ D4�G8TK4� UWUC8AUKBAU E�4/4@WT4 8G 4�� NVV24F 4U �8�� 4U G�8 �K:��� U8AUKGK�8 �8G8�GKBA B9 4��8TY :8AU E�4/4@WT4 4A� �4GUWA4:4 NVV2F�

�4GUWA:4 4A� �B�BT/8TU KA�BTCBT4G8� D4�G8TK4� @4:A8GKG8 C4TGK��8U KAGB 8W�4T�BGK� �8��UI ��K�� �BW�� D8 @4AKCW�4G8� D� 4 @4:A8GK� �8��� �4:A8GBUB@8U �8T8 KAGTB�W�8� KAGB T8� D�BB� �8��U D� 9WUKBA �KG� D4�G8TK4� UC�8TBC�4UGU @8�K4G8� D� CB��8G���8A8 :���B�� ��B�8 @4:A8GBG4�GK� D4�G8TK4 �4�8 4�UB D88A KAGTB�W�8� KAGB �8W/B��G8U D� C�4:B��GBUKU E�4GUWA4:4 8G 4�� NV)VF�

34�G8TK4� @4:A8GKG8 C4TGK��8U �8T8 4�UB WU8� 4U �4TTKY 8TU 9BT G�8 KAGTB�W�GKBA B9 a�O KAGB �8��U� +A 4 @8G�B� �8U�TKD8� D� 64/8�4@4 8G 4�� ENVVRFI D4�G8TK4� @4:A8GKG8 C4TGK��8U �B4G8� �KG� C�4U@K� a�O �8T8 WU8� 9BT G�8 D4��KUGK� GT4AU9BT@4GKBA B9 G�8 @4TKA8 ��4ABD4�G8TKW@ ���������-��- WUKA: 4 C4TGK��8 :WA� +A 4ABG�8T 8ZC8TKY @8AGI a�O B�K:BAW��8BGK�8U �8T8 K@@BDK�KM8� BA D4�Y G8TK4� @4:A8GKG8 C4TGK��8U 4A� WU8� 9BT G�8 �8G8�GKBA B9 @��O E5B�8 8G 4�� NVV2F� D8

OABG�8T 4CC�K�4GKBA B9 D4�G8TK4� @4:A8GBUB@8U @4� �K8 KA G�8KT CBG8AGK4� WU8 4U 4 �BAGT4UG 4:8AG 9BT @4:A8GK� T8UBA4A�8 K@4:KA: 4A� GW@BTYUC8�K�� �TW: �4TTK8TU D4U8� BA KAGT4GW@BT4� 8ATK��@8AG E3W�G8 4A� 3TBB/U NVVcF� 5�AG�8GK� �KCBUB@8U �BAG4KAKA: UWC8TC4T4@4:Y A8GK� KTBA BZK�8 C4TGK��8U �4�8 4�T84�� D88A WU8� KA DKB@8�K�4� 4CC�K�4GKBAU B9 G�KU G�C8 E�4J WU8T 8G 4�� NVVcF� O:4KAI D8�4WU8 B9 G�8KT WAKSW8 @4:A8GK� 4A� �T�UG4��KA8 CTBC8TGK8U 4A� G�8 A4GWT4� CT8U8A�8 B9 4 UWTTBWA�KA: @8@DT4A8I @4:A8GBUB@8U @K:�G D8 UWC8TKBT KA UB@8 4CC�K�4GKBAU� +G �4U 4�UB D88A �8@BAUGT4G8� G�4G 4CC��Y KA: G�8 CTKA�KC�8 B9 �BA�A8� DKB@KA8T4�KM4GKBA �KG�KA G�8 �4�KG� B9 4CB98TTKGKA T8UW�G8� KA G�8 KAAB�4GK�8 @4Y G8TK4� @4:A8GB98TTKGKAI ��K�� �4U @BT8 8�8�GK�8 4U 4 @4:A8GK�YT8UBA4A�8 �BAGT4UG 4:8AG G�4A ��8@BU�AG�8GK� C4TGK��8U E3W�G8 8G 4�� NVV`F�

E�������,:��

O�G�BW:� G�8 DKBG8��AB�B:K�4� CBG8AGK4� B9 D4�G8TK4� @4:A8GKG8 �4U D88A �8@BAUGT4G8�I GB �4G8 AB 4CC�K�4GKBA �4U D88A 8ZC�BKG8� BA 4 �B@@8T�K4� U�4�8� 6�KU KU C4TY GK4��� D8�4WU8 B9 G�8 CTBD�8@U T8�4G8� GB @4UU �W�GK�4GKBA B9 @4:A8GBG4�GK� D4�G8TK4I ��K�� KU UGK�� GBB 8ZC8AUK�8 9BT @BUG CT4�GK�4� CWTCBU8U� �B�8�8TI G�8 WU8 B9 D4�G8TK4� @4:A8GBUB@8U �BW�� D8 �B@C8GKGK�8 KA UB@8 UC8�K4�KM8� 4CC�K�4GKBAUI ��8T8 C8T98�G �T�UG4��KA8 CTBC8TGK8U 4A� T8�4GK�8�� U@4�� 4@BWAGU 4T8 T8SWKT8�I 4U KA UB@8 DKBY @8�K�4� 4CC�K�4GKBAUI 9BT 8Z4@C�8� OABG�8T T84UBA 9BT G�8 �K@KG8� CT4�GK�4DK�KG� B9 @4A� K�84U KU G�8 �4�/ B9 4

9WA�4@8AG4� WA�8TUG4A�KA: B9 G�8 DKB��8@K�4� 4A� :8Y A8GK� CTKA�KC�8U D8�KA� G�8 CTB�8UU B9 D4�G8TK4� @4:A8GKG8 DKB@KA8T4�KM4GKBA� �BT8 T8U84T�� KA G�KU �8�� KU ��84T�� T8SWKT8�� 6�8 @BUG �TKGK�4� KUUW8 KU G�8 @8��4AKU@ D� ��K�� G�8 BT:4AK� @4GTKZ �BAGTB�U G�8 AW��84GKBA 4A� :TB�G� B9 G�8 C4TGK��8U� (WTG�8T KA�8UGK:4GKBA B9 G�8 UGTW�GWT8 4A� �B@CBUKGKBA B9 G�8 @4:A8GBUB@8 @8@Y DT4A8 4A� KGU CTBG8KA BT:4AKM4GKBA KU G�8T89BT8 8UU8AGK4� 9BT WA�8TUG4A�KA: KBA GT4AUCBTG G�TBW:� G�8 @8@DT4A8 4A� G�8 84T�� UG4:8U B9 �T�UG4� 9BT@4GKBA�

+A�T84U8� 8�BTGU U�BW�� D8 �KT8�G8� GB G�8 :8A8GK� 4A� @B�8�W�4T DKB�B:K�4� 4A4��UKU B9 @4:A8GBUB@8 9BT@4Y GKBA� 6�8 4CC�K�4GKBA B9 :8A8GK� 8A:KA88TKA: G8��AKSW8U @K:�G CBUUKD�� T8UW�G KA @4:A8GBUB@8 C4TGK��8U �KG� K@CTB�8� CTBC8TGK8U 4A� 4 @BT8 �8C8A�4D�8 CTB�W�GKBA CTB�8UU� (BT 8Z4@C�8I KG �4U D88A UW::8UG8� G�4G @4:Y A8GBUB@8YUC8�K�� CTBG8KAU @K:�G D8 WU8� 9BT G�8 �BAY UGTW�GKBA B9 :8A8 9WUKBAU GB �BWC�8 DKB4�GK�8 UWDUG4A�8U �KT8�G�� KA BT�8T GB �KUC�4� G�8@ BA G�8 UWT94�8 B9 G�8 @4:A8GBUB@8 C4TGK��8U E�4/4@WT4 8G 4�� NVVRDF� �8Y A8GK� 8A:KA88TKA: @K:�G 4�UB D8 WU8� 9BT �BAGTB� B9 G�8 ��8@K�4� �B@CBUKGKBA� 6�8 @B�K��4GKBA B9 G�8 GT4AUCBTG U�UG8@ T8UCBAUKD�8 9BT G�8 4��W@W�4GKBA B9 KTBA KAGB G�8 @4:A8GBUB@8 �8UK��8 @K:�G T8UW�G KA 4A 4�G8T8� UC8�K��KG� 9BT @8G4� WCG4/8I CBG8AGK4��� �K8��KA: �T�UG4�U �KG� AB�8� @4:A8GK� 4A� �T�UG4��KA8 CTBC8TGK8U� 1A�8 G�8 :8A8U 9BT G�8 DKB@KA8T4�KM4GKBA C4G��4� 4T8 K�8AGK�8�I G�8� @K:�G

8ZCT8UU8� KA 4 T84�K�� �W�GK�4D�8 �BUG BT:4AKU@I G�8T8D� CBG8AGK4��� 8�K@KA4GKA: G�8 �K'�W�GK8U 4UUB�K4G8� �KG� G�8 �W�GK�4GKBA B9 @4:A8GBG4�GK� D4�G8TK4� (WA�Y GKBA4� 8ZCT8UUKBA B9 UKA:�8 :8A8U 9TB@ .B�����-����DDME KA NA ��D� �4U 4�T84�� D88A �8@BAUGT4G8� E38TUBA 8G 4�� NV)VI NVVNFI DWG G�8 �8G8TB�B:BWU 8ZCT8UUKBA B9 :8A8U T8�4G8� GB D4�G8TK4� DKB@KA8T4�KM4GKBA �BW�� D8 �K@KG8� D� G�8 �4�/ B9 4A KAGT4�8��W�4T �B@C4TG@8AG� O�G8TA4GK�8��I D4�G8TK4� �BUGU �KG� 4A 8ZKUGKA: KAGT4��GBC�4U@4GK� @8@DT4A8 U�UG8@I UW�� 4U C�BGBGTBC�K� D4�G8TK4I @K:�G D8 @BT8 4CCTBCTK4G8 9BT 8ZCT8UUKBA 4A� KAGT4�8��W�4T G4T:8GKA: B9 G�8 DKB@KA8T4�KM4GKBA @4��KA8T��

(KA4���I KA G�8 �K:�G B9 G�8 �T4@4GK� �K�8TUKG� B9 A4GY WT4��� B��WTTKA: @4:A8GBG4�GK� D4�G8TK4 �KG� �4TK4D�8 �T�UG4� @BTC�B�B:K8UI KA�T84U8� 8�BTG U�BW�� D8 :K�8A GB G�8 KUB�4GKBA 4A� UGW�� B9 BG�8T @4:A8GBG4�GK� UC8�K8U �KG� CBG8AGK4��� WAKSW8 984GWT8U B9 G�8 DKB@KA8T4�KM4GKBA CTB�8UU� 7A�8TUG4A�KA: �B� �K�8T8AG D4�G8TK4 4��K8�8 UC8�K8UYUC8�K�� �BAGTB� B�8T G�8 DKB@KA8T4�KM4GKBA CTBY �8UU �BW�� D8 WU8� KA G4K�BTKA: �K�8T8AG �T�UG4� @BTY C�B�B:K8U �KG� G�8 �8UKT8� CTBC8TGK8U�

�bBF�1��2����F�� a�5� �4U UWCCBTG8� D� :T4AGU 9TB@ G�8 a8Y WGU��8 (BTU��WA:U:8@8KAU��49G 4A� G�8 �4ZY��4A�/Y5B�K8G�� ��3�(� �4U UWCCBTG8� D� �5( :T4AG %�� VcN`N�N� �8 4T8 :T4G89W� GB �� 348W8T�8KAI a�O� 34M��KAU/KI 5� 5CTKA: 4A� 3� 68DB 9BT �KUY �WUUKBAU 4A� �B��4DBT4GKBA�

����������

34�4� O5I %TBW�4�8 +�I �4@8U �O3 ENVV`F 6T84G@8AG B9 �84�� @8G4� �BAG4@KA4AGU WUKA: @4:A8GBG4�GK� D4�G8TK4� +��� 6T4AU �4:A8G 2�� `c�c-`c�V

Page 9: Bacterial Magnetosomes: Microbiology, Biomineralization ...materials, mainly magnetite, has been reported for an extremely diverse range of organisms including algae (Torres de Araujo

34�4� O5I %TBW�4�8 +�I �4@8U �O3I �B8U���8T (aI �4T�K�/ �� ENVV)F %BAGKAWBWU T4�KBAW��K�8 T8�B�8T� 9TB@ �4UG8�4G8T WUKA: @4:A8GBG4�GK� D4�G8TK4� � �4:A8G �4:A8G �4G8T N)`� �`N-�``

34M��KAU/K aO ENVVRF 5GTW�GWT8 4A� 9WA�GKBA B9 G�8 D4�G8TK4� @4:A8GBUB@8� O5� �8�U bN� 22c-2`2

34M��KAU/K aOI (T4A/8� �3I �4AA4U�� �� ENV))F OA48TBDK� @4:A8GKG8 CTB�W�GKBA D� 4 @4TKA8 @4:A8GBG4�GK� D4�G8TKW@� �4GWT8 22`� RN)-RNV

34M��KAU/K aOI �4TT4GGY�88� OI (T4A/8� �3 ENVV`F ��8�GTBAY@KY �TBU�BCK� UGW�K8U B9 @4:A8GBUB@8U KA @4:A8GBG4�GK� D4�G8TK4� �K�TBU�BC� �8U 68�� �c� 2)V-`�N

38TUBA O�I �W�UBA a�I �4�8� �5 ENV)VF %�BAKA: 4A� ��4T4�Y G8TKM4GKBA B9 G�8 ���� :8A8 B9 ��MB-����DDME EB������B����ME� OT�� �K�TBDKB� NR�� Rbc-RcN

38TUBA aOI �W�UBA a�I �4�8� �5 ENVVNF %�BAKA: B9 4 U8SW8A�8 B9 ��MB-����DDME EB������B����ME G�4G �B@C�8@8AGU G�8 B��a :8A8 B9 N-��������B ��D�� �B� �K�TBDKB� R� ��b�-��b`

3�4/8@BT8 �� ENVcRF �4:A8GBG4�GK� D4�G8TK4� 5�K8A�8 NV�� 2cc-2cV 3�4/8@BT8 �� ENV)2F �4:A8GK� D4�G8TK4 4A� CTB�W�GU �8TK�8�

G�8T89TB@� 75 C4G8AG `2)RNNV 3�4/8@BT8 ��I �4T4G84 aI �B�98 �5 ENVcVF +UB�4GKBA 4A� CWT8

�W�GWT8 B9 4 9T8U��4G8T @4:A8GK� UCKTK��W@ KA ��8@K�4��� �8�A8� @8�KW@� � 34�G8TKB� N`�� c��-c�V

3�4/8@BT8 ��I 5�BTG �OI 34M��KAU/K aOI �BU8AD�4GG %I (T4A/8� �3 ENV)RF �K�TB48TBDK� �BA�KGKBAU 4T8 T8SWKT8� 9BT @4:A8GKG8 9BT@4GKBA �KG�KA ��MB-����DDME EB������B����ME� �8B@K�TBDKB� � `� R2-cN

3W�G8 ���I 3TBB/U �O ENVVcF �4:A8GK� A4ABC4TGK��8U 4U �BAGT4UG 4:8AGU 9BT K@4:KA:� +A� �4J 98�K 7I 5��WJ GG �I 68��8T �I �DBTB�U/K � E8�UF 5�K8AGK�� 4A� ��KAK�4� 4CC�K�4GKBAU B9 @4:A8GK� �4TTK8TU� ��8AW@I �8� �BT/I �BA�BAI CC R�c-R`2

3W�G8 ���I aBW:�4U 6I �4AA 5I (T4A/8� �3I �BU/B�KGM 3�I 3TBB/U �OI 34W@:4TGA8T %aI ��@4M4� �I (T4A/ �O ENVV`F �4:A8GB98TTKGKA� DKB@KA8T4�KM4GKBA 4U AB�8� @B�8�W�4T 4CY CTB4�� KA G�8 �8UK:A B9 G�8 KTBAYBZK�8YD4U8� @4:A8GK� T8UBY A4A�8 �BAGT4UG 4:8AGU� +A�8UG �4�KB� �V� 5�N`-�Nb

3WT:8UU ��I �4�4:W��K �I 54/4:W��K 6I 6�BTA�K�� ��I �4GUWY A4:4 6 ENVV2F ��B�WGKBA4T� T8�4GKBAU�KCU 4@BA: .B�����-, ����DDME UGT4KAU KA98TT8� 9TB@ C���B:8A8GK� 4A4��UKU B9 Nb5Y T��O U8SW8A�8U� � 34�G8TKB� NcR� bb)V-bbV`

a8�BA: �(I (T4A/8� �3I 34M��KAU/K aO ENVV2F �W�GKC�8 8�B�WY GKBA4T� BTK:KAU B9 @4:A8GBG4ZKU KA D4�G8TK4� 5�K8A�8 �RV� )�2-)�b

aWAKAY3BT/B�U/K ��I ��%4TGA8� ��I (T4A/8� �3I 34M��KAU/K aOI �BU94K �I 3WU8�/ �� ENVV)F �4:A8GK� @K�TBUGTW�GWT8 B9 @4:A8GBG4�GK� D4�G8TK4 D� 8�8�GTBA �B�B:T4C��� 5�K8A�8 �)�� N)b)-N)c�

(T4A/8� �3I 34M��KAU/K aO ENVV`F �4:A8GBG4ZKU 4A� @4:A8GK� C4TGK��8U KA D4�G8TK4� ��C8T�A8 +AG8T4�G V�� N2R-N`�

(T4A/8� �3I 3�4/8@BT8 �� ENV)�F �4�K:4GKBA4� �B@C4UU KA @4:Y A8GK� D4�G8TK4� � �4:A8G �4:A8G �4G8T NR-N)� NRb�-NRb`

(T4A/8� �3I �4C489G��@KBW �%I 3�4/8@BT8 ��I 1�3TK8A � ENV)2F (821` CT8�KCKG4GKBA KA @4:A8GBG4�GK� D4�G8TK4� 3KB��K@ 3KBC��U O�G4 cb2� N`c-NRV

(T4A/8� �3I 34M��KAU/K aOI �B�AUBA �5I 64��BT 3� ENVVcF �4:A8GBY48TBG4ZKU KA @4TKA8 �B��BK� D4�G8TK4� 3KBC��U � c2� VV`-N���

(T4A/8� �3I 34M��KAU/K aOI 5��WJ �8T a ENVV)F 3KB@KA8T4�KM4GKBA B9 @4:A8GK� KTBA @KA8T4�U KA @4:A8GBG4�GK� D4�G8TK4� 5WCT4@B� 5�K R� 2)2-2V�

(W/W@BTK �I 1�A4:K �I �BU�K@4GUW �I �B:W��K �I (W�K�4T4 6 ENVVcF �AM�@4GK� KTBA BZK�4GKBA 4A� T8�W�GKBA KA @4:A8GKG8 U�AG�8UKMKA: .B�����-����DDME EB������B����ME� � ���U +� c� bRV-bb�

(WA4/K �I 54/4K �I �4GUWA4:4 6I �KTBU8 5 ENVV�F 6�8 5 CB�8 �KUGTKDWGKBA BA @4:A8GK� :T4KAU KA C�TBZ8AKG8 �8G8T@KA8� D� @4:A8GBG4�GK� D4�G8TK4� ���U �4TG� ��4A8G +AG8TKBT c�� �R2-�b�

�BTD� �OI 38�8TK�:8 6�I 3�4/8@BT8 �� ENV))F %�4T4�G8TKM4GKBA B9 G�8 D4�G8TK4� @4:A8GBUB@8 @8@DT4A8� � 34�G8TKB� Nc�� )2`-)`N

�W8TKA �(I 3�4/8@BT8 �� ENVV�F �8�BZ ����KA: B9 KTBA UWCCBTGU :TB�G� 4A� @4:A8GKG8 U�AG�8UKU D� ��MB-����DDME EB�����, �B����ME� OCC� �A�KTBA �K�TBDKB� R)� NN��-NN�V

�W8TKABG �� ENVV`F �K�TBDK4� KTBA GT4AUCBTG� OAAW �8� �K�TBY DKB� `)� c`2-cc�

�4T4U/B �I �9WJ GMA8T �I �4CC �I (WGU��K/ �I 5��WJ �8T a ENVV2F a8G8T@KA4GKBA B9 G�8 �BA�8AGT4GKBA B9 @4:A8GBG4�GK� D4�G8TK4 D� @84AU B9 UWU�8CGKDK�KG� @84UWT8@8AGU� �CA � OCC� ���U 2�� �R�-�b�

�4T4U/B �I �9WJ GMA8T �I (WGU��K/ � ENVVRF aB@4KA 4A4��UKU D� @84AU B9 @4:A8GBG4�GK� D4�G8TK4� +��� 6T4AU �4:A8G 2N� V2)-V`V

�KTU���KA/ ��I �BD4�4U�KY�KTU���KA/ OI �BB�9BT� 3� ENVV�F �4:A8GKG8 DKB@KA8T4�KM4GKBA KA G�8 �W@4A DT4KA� �TB� �4G� O�4� 5�K 75O )V� cb)2-cb)c

�B��8� a�I 5GB�M �(I �BT� ��I ��K��KCU ��� ENV)cF OA48TBDK� CTB�W�GKBA B9 @4:A8GKG8 D� 4 �KUUK@K�4GBT�YKTBA T8�W�KA: @KY �TBBT:4AKU@� �4GWT8 22�� �R�-�R`

�B�8AUG4@ �O ENV)NF �KA8T4�U 9BT@8� D� BT:4AKU@U� 5�K8A�8 �NN� NN�b-NN2N

�4�8T 3O ENVV)F �4:A8GKG8 DKB@KA8T4�KM4GKBA KA G8T@KG8U� �TB� � 5B� �BA� 3KB� �bR� c22-c2c

�4AA 5 ENVV2F �B�8�W�4T G8�GBAK�U KA DKB@KA8T4�KM4GKBA 4A� DKB@K@8GK� @4G8TK4�U ��8@KUGT�� �4GWT8 2bR� `VV-R�R

�4AA 5I 5C4T/U ��%I �4�/8T ��I �KTU���KA/ �� ENV))F 7�GT4Y UGTW�GWT8I @BTC�B�:� 4A� BT:4AKM4GKBA B9 DKB:8AK� @4:A8GKG8 9TB@ UB�/8�8 U4�@BAI b���������M- ����B� K@C�K�4GKBAU 9BT @4:A8GTBT8�8CGKBA� � �ZC 3KB� N`�� 2R-`V

�4AA 5I 5C4T/U ��%I 3B4T� �� ENVV�F �4:A8GBG4�GK� D4�G8TK4� @K�TBDKB�B:�I DKB@KA8T4�KM4GKBAI C4�48B@4:A8GKU@ 4A� DKBY G8��AB�B:�� O�� �K�TBDKB� ���UKB� 2N� N�R-N)N

�4GUWA4:4 6 ENVVNF OCC�K�4GKBAU B9 D4�G8TK4� @4:A8GU� 6T8A�U 3KBG8��AB� V� VN-VR

�4GUWA4:4 6I �4@K�4 5 ENV)cF 7U8 B9 @4:A8GK� C4TGK��8U KUB�4G8� 9TB@ @4:A8GBG4�GK� D4�G8TK4 9BT 8AM�@8 K@@BDK�KM4GKBA� OCC� �K�TBDKB� 3KBG8��AB� �b� 2�)-22�

�4GUWA4:4 6I �4U�K@BGB �I �4/4@WT4 �I �4/4@WT4 �I �4U�K@BGB 5 ENV)VF ��4:B��GBUKU B9 D4�G8TK4� @4:A8GKG8 D� �8W/B��G8U� OCC� �K�TBDKB� 68��AB� 2N� `�N-`�R

�4GUWA4:4 6I 64�B/BTB (I �4/4@WT4 � ENVV�F �4UU �W�GWT8 B9 @4:A8GK� D4�G8TK4 4A� G�8KT 4CC�K�4GKBA GB ;B� G�C8 K@@WABY 4UU4�U� +��� 6T4AU �4:A8G �b� NRRc-NRRV

�4GUWA4:4 6I �4/4@WT4 %I 3WT:8UU ��I 5B�8 5 ENVV�F �8A8 GT4AU98T KA @4:A8GK� D4�G8TK4� GT4AUCBUBA @WG4:8A8UKU 4A� ��BAKA: B9 :8AB@K� a�O 9T4:@8AGU T8SWKT8� 9BT @4:A8GBUB@8 U�AG�8UKU� � 34�G8TKB� Nc`� �c`)-�cR2

�4GUWA4:4 6I �4@K�4 5I 6UW�K@WT4 � ENVVcF �TB�W�GKBA B9 CTBY G8KA E8AM�@8I 4AGKDB��I CTBG8KA OFY@4:A8GKG8 �B@C�8Z D� :8Y A8GK�4��� 8A:KA88T8� @4:A8GK� D4�G8TK4 .B�����-����DDME UC� O�3YN� +A� �4J 98�K 7I 5��WJ GG �I 68��8T �I �DBTB�U/K � E8�UF 5�K8AGK�� 4A� ��KAK�4� 4CC�K�4GKBAU B9 @4:A8GK� �4TTK8TU� ��8AW@I �8� �BT/ �BA�BAI CC �)c-�V`

�8��TW@ (%I �4AA 5I �8��BB� 3�I (T4A/8� �3I 34M��KAU/K aO ENVV24F ��8�GTBA @K�TBU�BC� UGW�� B9 @4:A8GBUB@8U KA G�B �W�GWT8� �KDTBK� @4:A8GBG4�K� D4�G8TK4� �TB� � 5B� �BA� .3KB�0 �RN� �2c-�`�

�8��TW@ (%I �4AA 5I �8��BB� 3�I (T4A/8� �3I 34M��KAU/K aO ENVV2DF ��8�GTBA @K�TBU�BC� UGW�� B9 @4:A8GBUB@8U KA 4 �W�Y GWT8� �B��BK� @4:A8GBG4�GK� D4�G8TKW@� �TB� � 5B� �BA� .3KB�0 �RN� �2N-�2b

�BU/B�KGM 3� ENVVRF 3KB@KA8T4�KM4GKBA B9 @4:A8GK� @KA8T4�U� �8� �8BC��U 22� N�2-N�)

�4/4@WT4 �I �4GUWA4:4 6 ENVV2F �K:��� U8AUKGK�8 �8G8�GKBA B9 4��8T:8A WUKA: D4�G8TK4� @4:A8GK� C4TGK��8U� OA4� %�K@ O�G4 �)N� R)R-R)V

�4/4@WT4 �I �4U�K@BGB �I �4GUWA4:4 6 ENVVNF +@@WAB4UU� @8G�B� 9BT G�8 �8G8T@KA4GKBA B9 K@@WAB:�BDW�KA � WUKA: D4�G8TK4� @4:A8GK� C4TGK��8U� OA4� %�8@ b2� �b)-�c�

�4/4@WT4 �I 3WT:8UU ��I �4:KW�4 �I �KW�B 5I 54/4:W��K 6I �4GUWA4:4 6 ENVV24F a8G8�GKBA 4A� T8@B�4� B9 N-��������B ��D� WUKA: ;WBT8U�KA KUBG�KB��4A4G8 �BA�W:4G8� @BAB��BA4� 4AGKY DB�� K@@BDK�KM8� BA D4�G8TK4� @4:A8GK� C4TGK��8U� OA4� %�8@ bR� ��2b-��2V

�4/4@WT4 %I 54/4:W��K 6I �W�B 5I 3WT:8UU ��I 5B�8 �I �4GUWA4:4 6 ENVV2DF %�4T4�G8TKM4GKBA B9 KTBA WCG4/8 KA G�8

Page 10: Bacterial Magnetosomes: Microbiology, Biomineralization ...materials, mainly magnetite, has been reported for an extremely diverse range of organisms including algae (Torres de Araujo

@4:A8GK� D4�G8TKW@ ��MB-����DDME UC� O�3YN� OCC� 3KB��8@ 3KBG8��AB� 2V�`�� NbV-Ncc

�4/4@WT4 %I 3WT:8UU ��I 5B�8 �I �4GUWA4:4 6 ENVVR4F OA KTBAY T8:W�4G8� :8A8I EB��I 8A�B�KA: 4A KTBA GT4AUCBTG CTBG8KA B9 .B�����-����DDME UC� UGT4KA O�3YN� � 3KB� %�8@ �c�� �) 2V�-�) 2Vb

�4/4@WT4 %I �K/W��K 6I 3WT:8UU ��I �4GUWA4:4 6 ENVVRDF +TBAY T8:W�4G8� 8ZCT8UUKBA 4A� @8@DT4A8 �B�4�KM4GKBA B9 G�8 @4:O CTBG8KA KA .B�����-����DDME -C UGT4KA O�3YN� � 3KB��8@ E6B/�BF NN)� �2-�c

1/W�4 �I a8A�4 �I (W/W@BTK � ENVVbF %�BAKA: 4A� U8SW8A�KA: B9 4 :8A8 8A�B�KA: 4 A8� @8@D8T B9 G�8 G8GT4GTK�BC8CGK�8 CTBG8KA 94@K�� 9TB@ @4:A8GBUB@8U B9 .B�����-����DDME EB�, �����B����ME� �8A8 NcN� VV-N��

�4B�8GGK �%I 3�4/8@BT8 �� ENV)bF ���TBZ4@4G8 CTB�W�GKBA D� ��MB-����DDME EB������B����ME� � 34�G8TKB� Nbc� NR2-Nb2

�4J WU8T 5I �8UM/4 �I �4:A8T 5I �B�9 ��I 3W�T ��I 38T:8T � ENVVcF �KCBUB@8Y8A�4CUW�4G8� UWC8TC4T4@4:A8GK� KTBA BZK�8 C4TGK��8U 4U @4T/8TU KA 4A ��+Y:WK�8� U84T�� 9BT GW@BTYUC8�K�� �TW: �4TTK8TU� OAGK�4A�8T aTW: a8U N�� N�R-N2R

�BU94K �I 3WU8�/ ��I 34M��KAU/K aOI (T4A/8� �3 ENVV)F �84�GKBA U8SW8A�8 B9 KTBA UW���8 @KA8T4�U KA D4�G8TK4 4A� G�8KT WU8 4U DKB@4T/8TU� 5�K8A�8 �)�� ))�-))2

��B4�U a ENVVRF �K�TBDK4� @4:A8GB@8G8T 8A4D�8U GK@8�� CT8�K�Y GKBA B9 BZ�:8A �8C�8GKBA KA DBGGB@ U8�K@8AGU 4A� B�8T��KA: DBGGB@ �4G8T� �A�KTBA 3W�� R� �GGC� ������U4K���B@�8A�KTBA� DW��8GKAU�UCTKA:VR�KA�8Z��G@�

54/4:W��K 6I 3WT:8UU ��I �4GUWA4:4 6 ENVV2F �4:A8GKG8 9BT@4Y GKBA D� 4 UW�C�4G8YT8�W�KA: D4�G8TKW@� �4GWT8 2bR� `c-`V

54TK/4�4 � ENVV`F OA KAGTB�W�GKBA GB DKB@K@8GK�U� 4 UGTW�GWT4� �K8�CBKAG� �K�TBU� �8U 68�� �c� 2b�-2cR

5���8K98T ��I 5��WJ �8T aI 5CTKA: 5I �8KM8A8::8T �I O@4AA �I �W��K: �I �BJ ��8T � ENVVNF 6�8 :8AWU .B�����-����DDME :8A� AB��I �8U�TKCGKBA B9 .B�����-����DDME ������-OBDc��-� UC� AB�� 4A� GT4AU98T B9 ��MB-����DDME EB������B����ME GB .B�����-, ����DDME EB������B����ME �B@D� AB�� 5�UG OCC� �K�TBDKB� N`� 2cV-2)R

5��WJ �8T aI 348W8T�8KA � ENVVbF +TBAY�K@KG8� :TB�G� 4A� /KA8GK�U B9 KTBA WCG4/8 KA .B�����-����DDME ������-OBDc��-�� OT�� �K�TBY DKB� Nbb� 2�N-2�c

5��WJ �8T aI 348W8T�8KA � ENVVc4F +TBA GT4AUCBTG 4A� @4:A8GKG8 �T�UG4� 9BT@4GKBA B9 G�8 @4:A8GK� D4�G8TKW@ .B�����-����DDME ������-OBDc��-�� � ���U +� c� b`c-bR�

5��WJ �8T aI 348W8T�8KA � ENVVcDF 6�8 DKB@KA8T4�KM4GKBA B9 @4:A8Y GKG8 KA @4:A8GK� D4�G8TK4� +A� 6T4WG�8KA O E8�F 3KBKABT:4AK� ��8@KUGT�� GT4AUKGKBA @8G4�U KA DKB�B:� 4A� �BBT�KA4GKBA ��8@KUGT�� a8WGU��8 (BTU��WA:U:8@8KAU��49G� �K�8�Y�%�I �8KA�8K@ �8� �BT/ %�K��8UG8TI CC �`-2b

5��WJ �8T aI 348W8T�8KA � ENVV)F a�A4@K�U B9 KTBA WCG4/8 4A� (821` DKB@KA8T4�KM4GKBA �WTKA: 48TBDK� 4A� @K�TB48TBDK� :TB�G� B9 .B�����-����DDME ������-OBDc��-�� � 34�G8TKB� N)�� NRV-Nb�

5��WJ �8T aI �BJ ��8T � ENVV�F 6�8 KUB�4GKBA B9 4 A8� @4:A8GK� UCKTK��W@� �8AGT4�D� �K/TBDKB� N`c� NR�-NRN

5��WJ �8T aI 7�� �I 348W8T�8KA � ENVVRF O UK@C�8 �K:�GYU�4GG8TKA: @8G�B� GB 4UU4� @4:A8GKU@ KA .B�����-����DDME ������-OBD, c��-�� (��5 �K�TBDKB� �8GG N2�� N2V-N`R

5��WJ �8T aI 348W8T�8KA �I 34M��KAU/K aO ENVVcF �B�4�KM4GKBA 4A� B��WTT8A�8 B9 @4:A8GBUB@8 CTBG8KAU 9TB@ .B�����-, ����DDME ������-OBDc��-� UGW�K8� D� 4A K@@WAB�B:K�4� @8G�B�� +A� ODUGT4�GU B9 G�8 VcG� �8A8T4� �88GKA: B9 G�8 O@8TK�4A 5B�K8G� 9BT �K�TBDKB�B:�I �K4@KI C 22�

5���4TGM 33I 3�4/8@BT8 � ENV)`F �4:A8GBG4�GK� D4�G8TK4 KA ��KAY K�4� 4UU4�I K@@WAB4UU� 4A� �8��U U8C4T4GKBA CTB�8�WT8U 4A� G�8 �K/8� 75 C4G8AG `bcc�bc

5B�8 �I �W�B 5I 54/4:W��K 6I �4/4@WT4 �I �4GUWA4:4 6 ENVV2F OCC�K�4GKBA B9 D4�G8TK4� @4:A8GK� C4TGK��8U 9BT �K:��� U8�8�GK�8 @8UU8A:8TY��O T8�B�8T� U�UG8@� 3KBG8��AB� 68�� c� b))-bV`

5C4T/U ��%I �4AA 5I 34M��KAU/K aI �B��8� aI �4AA4U�� ��I (T4A/8� �3 ENVV�F 5GTW�GWT8 4A� @BTC�B�B:� B9 @4:A8GKG8 4A48TBDK�4���YCTB�W�8� D� 4 @4TKA8 @4:A8GBG4�GK� D4�G8TKW@ 4A� 4 �KUUK@K�4GBT� KTBAYT8�W�KA: D4�G8TKW@� �4TG� ��4A8G 5�K �8GG V)� N`-��

5CTKA: 5I 5���8K98T �� ENVVRF aK�8TUKG� B9 @4:A8GBG4�GK� D4�G8TK4� 5�UG8@ OCC� �K�TBDKB� N)� N`c-NR2

5CTKA: 5I O@4AA �I �W��K: �I 5���8K98T ��I �8@8T�8A ��I �8G8TU8A � ENVV2F aB@KA4GKA: TB�8 B9 4A WAWUW4� @4:A8GBG4�GK� D4�G8TKW@ KA G�8 @K�TB48TBDK� MBA8 B9 4 9T8U��4G8T U8�K@8AG� OCC� �A�KTBA �K�TBDKB� RV� �2Vc-�`�2

5GB�M �( ENVV2F �4:A8GBUB@8U� � �8A �K�TBDKB� N2V� Nbb2-Nbc� 64/8�4@4 �I �4@4M4�4 OI �4/4@WT4 %I �4GUWA4:4 6 ENVVRF

OCC�K�4GKBA B9 D4�G8TK4� @4:A8GK� C4TGK��8U 4U AB�8� a�O �4TY TK8TU 9BT D4��KUGK� GT4AU9BT@4GKBA B9 4 @4TKA8 ��4ABD4�G8TKW@� 3KBG8��AB� 68�� V� 2RR-2b�

64@8:4K �I (W/W@BTK � ENVV`F �WTK��4GKBA 4A� UB@8 @B�8�W�4T 4A� 8AM�@4GK� 984GWT8U B9 4 AB�8� ��DYG�C8 ��GB��TB@8 � BZKY �4U8 9TB@ 4 @K�TB48TBDK� �8AKGTK�8TI .B�����-����DDME EB���, ���B����ME� (�35 �8GG 2`c� ��-�b

64@8:4K �I �4@4A4/4 6I (W/W@BTK � ENVV2F �WTK��4GKBA 4A� CTBC8TGK8U B9 4 ���GB��TB@ �� Y�K/8 �8@BCTBG8KA 9TB@ 4 @4:Y NA8GBG4�GK� D4�G8TKW@I ��MB-����DDME EB������B����ME� 3KB��K@ 3KBC��U O�G4 NNR)� N2c-�`2

6BTT8U �8 OT4W�B ((I �KT8U �OI (T4A/8� �3I 3K�W�B %�� ENV)bF �4:A8GKG8 4A� @4:A8GBG4ZKU KA 4�:48� 3KBC��U � R�� 2cR-2c)

�K�GU��/B �I �K�GU��/B � ENVVRF �4:A8GK� BTK8AG4GKBA KA 4AK@4�U� 5CTKA:8TI 38T�KA �8K�8�D8T: �8� �BT/

�4@4M4/K 6I 1�4A4:K �I (W�K�4T4 6I (W/W@BTK � ENVVRF �KY GTKG8 T8�W�G4U8 9TB@ G�8 @4:A8GBG4�GK� D4�G8TKW@ .B�����-, ����DDME EB������B����ME - 4 AB�8� ��GB��TB@8Y��ENF �KG� (8E++FYAKGTKG8 BZK�BT8�W�G4U8 4�GK�KG�� �WT � 3KB��8@ �22� bbR-bcN