Abstract

Magnetotactic bacteria (MTB) are morphologically and phylogenetically diverse prokaryotes. They can form intracellular chain-assembled magnetite (Fe3O4) or greigite (Fe3S4) nanocrystals each enveloped by a lipid bilayer membrane called a magnetosome. Magnetotactic cocci have been found to be the most abundant morphotypes of MTB in various aquatic environments. However, knowledge on magnetosome biomineralization within magnetotactic cocci remains elusive due to small number of strains that have been cultured. By using a coordinated fluorescence and scanning electron microscopy method, we discovered a unique magnetotactic coccus strain (tentatively named SHHC-1) in brackish sediments collected from the estuary of Shihe River in Qinhuangdao city, eastern China. It phylogenetically belongs to the Alphaproteobacteria class. Transmission electron microscopy analyses reveal that SHHC-1 cells formed many magnetite-type magnetosomes organized as two bundles in each cell. Each bundle contains two parallel chains with smaller magnetosomes generally located at the ends of each chain. Unlike most magnetotactic alphaproteobacteria that generally form magnetosomes with uniform crystal morphologies, SHHC-1 magnetosomes display a more diverse variety of crystal morphology even within a single cell. Most particles have rectangular and rhomboidal projections, whilst others are triangular, or irregular. High resolution transmission electron microscopy observations coupled with morphological modeling indicate an idealized model—elongated octahedral crystals, a form composed of eight {111} faces. Furthermore, twins, multiple twins and stack dislocations are frequently observed in the SHHC-1 magnetosomes. This suggests that biomineralization of strain SHHC-1 magnetosome might be less biologically controlled than other magnetotactic alphaproteobacteria. Alternatively, SHHC-1 is more sensitive to the unfavorable environments under which it lives, or a combination of both factors may have controlled the magnetosome biomineralization process within this unique MTB.

Highlights

  • Magnetotactic bacteria (MTB) are a group of geographically widespread prokaryotes sharing the common ability to form magnetite (Fe3O4) or greigite (Fe3S4) nanocrystals intracellularly, each surrounded by a lipid bilayer membrane (Bazylinski and Frankel, 2004)

  • Magnetotacic bacteria in the microcosms were routinely checked with the hanging-drop technique (Schüler, 2002) using an Olympus microscope BX51 equipped with phase-contrast, fluorescence and a DP70 digital camera system (Olympus Corp., Tokyo, Japan)

  • high angle annular dark field (HAADF)-scanning TEM (STEM) tomography observations clearly evidenced that each bundle was composed of two parallel closely assembled magnetosome chains (Figures 1D–F and Supplementary movie)

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Summary

Introduction

Magnetotactic bacteria (MTB) are a group of geographically widespread prokaryotes sharing the common ability to form magnetite (Fe3O4) or greigite (Fe3S4) nanocrystals intracellularly, each surrounded by a lipid bilayer membrane (Bazylinski and Frankel, 2004) These intracellular magnetic particles are called magnetosomes that generally arrange into chain structures (Balkwill et al, 1980). They serve as a cellular biocompass, enabling the MTB cells to passively align along the geomagnetic field lines Using this compass, MTB can actively swim, to their favorite niches at or just below the oxic-anoxic interface (OAI) in aquatic environments (Frankel et al, 1997; Bazylinski and Frankel, 2004). Fossilized remains of MTB (i.e., magnetofossils) have been tentatively used to retrieve paleomagnetic and paleoenvironmental information from ancient sediments (Hesse, 1994; Yamazaki and Kawahata, 1998; Snowball et al, 2002; Roberts et al, 2011; Larrasoana et al, 2014; Liu et al, 2015), and to trace the origin and evolution of life on Earth and even perhaps Mars (Chang and Kirschvink, 1989; McKay et al, 1996; Thomas-Keprta et al, 2002)

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