Anomalous Magnetic Orientations of Magnetosome Chains in a Magnetotactic Bacterium: Magnetovibrio blakemorei Strain MV-1

Hitchcock AP (2013) Anomalous Magnetic Orientations of Magnetosome Chains in a Magnetotactic Bacterium: Magnetovibrio blakemorei Strain MV-1. PLoS ONE 8(1): e53368. doi:10.1371/journal.pone.0053368 Anomalous Magnetic Orientations of Magnetosome Chains in a Magnetotactic Bacterium: Magnetovibrio blakemorei Strain MV-1 Samanbir S. Kalirai 0 Dennis A. Bazylinski 0 Adam P. Hitchcock 0 Josh Neufeld, University of Waterloo, Canada 0 1 Department of Chemistry and Chemical Biology, McMaster University , Hamilton, Ontario , Canada , 2 School of Life Sciences, University of Nevada at Las Vegas , Las Vegas, Nevada , United States of America There is a good deal of published evidence that indicates that all magnetosomes within a single cell of a magnetotactic bacterium are magnetically oriented in the same direction so that they form a single magnetic dipole believed to assist navigation of the cell to optimal environments for their growth and survival. Some cells of the cultured magnetotactic bacterium Magnetovibrio blakemorei strain MV-1 are known to have relatively wide gaps between groups of magnetosomes that do not seem to interfere with the larger, overall linear arrangement of the magnetosomes along the long axis of the cell. We determined the magnetic orientation of the magnetosomes in individual cells of this bacterium using Fe 2p X-ray magnetic circular dichroism (XMCD) spectra measured with scanning transmission X-ray microscopy (STXM). We observed a significant number of cases in which there are sub-chains in a single cell, with spatial gaps between them, in which one or more sub-chains are magnetically polarized opposite to other sub-chains in the same cell. These occur with an estimated frequency of 4.060.2%, based on a sample size of 150 cells. We propose possible explanations for these anomalous cases which shed insight into the mechanisms of chain formation and magnetic alignment. - Funding: CLS is supported by the Canada Foundation for Innovation (CFI), NSERC, Canadian Institutes of Health Research (CIHR), National Research Council (NRC) and the University of Saskatchewan. DAB is supported by U. S. National Science Foundation (NSF) grant EAR-0920718. The ALS is supported by the Director, Office of Energy Research, Office of Basic Energy Sciences, Materials Sciences Division of the U.S. Department of Energy, under Contract No. DE-AC02-05CH11231. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Magnetotactic bacteria (MTB) are ubiquitous in marine and freshwater environments [1,2,3]. They are a diverse group phylogenetically and morphologically which are linked by the ability to biomineralize membrane-bounded magnetic nanoparticles termed magnetosomes. Magnetosomes are single-domain magnetic crystals of either magnetite, Fe3O4, or greigite, Fe3S4 [4], typically oriented in one or more chains. The magnetosomes are responsible for a behaviour called magnetotaxis in which cells passively align and swim along the Earths geomagnetic field lines, which are inclined, except at the equator [5]. By reducing a threedimensional search problem to one of a single dimension, magnetotaxis allows for motile bacteria to more efficiently locate and maintain position at an optimal chemical environment, generally the oxic-anoxic interface, in aquatic habitats characterized by vertical chemical (e.g., oxygen) concentration gradients [5]. Thus in chemically-stratified habitats, MTB appear to have a significant advantage over non-magnetotactic bacteria in locating their preferred environment [6]. Magnetite-producing MTB synthesize magnetised chains of generally closely spaced, coherently aligned magnetosomes in order to maximize the dipole interaction to the Earths magnetic field [7,8,9]. The ability to reproducibly manufacture magnetosome magnetite crystals with high chemical purity, tight sizedistribution and uniform shape represents an exquisite process of biomineralization [10,11]. The size distribution of magnetosome crystals is highly controlled to be within the single-domain size regime [11] thereby maximizing the individual dipole moment of each magnetosome and preventing adverse size-dependent effects such as superparamagnetism and multiple domain formation which eliminate or lessen the efficacy of the magnetic particle. There is great interest in understanding biomineralization and its associated processes, both from a fundamental perspective and also for biomimetic applications [12,13]. Thus, shortly after the initial discovery [14,15] of magnetotactic bacteria, an enormous effort to understand the phenomenon in depth began and it is still underway today. Much of the effort to understand magnetosome biomineralization has involved genetic techniques which has not only resulted in the discovery of genes involved in the structure, formation and organization of magnetosomes (the mam, mms and mtx genes) but also in finding that most of these genes are located as clusters within the genome that are further organized as a magnetosome gene island [16]. Techniques such as transmission electron microscopy (TEM) have been employed to fill the knowledge gap that is related to the understanding of the role of individual mam genes as well as a generic understanding of chain growth and interactions among individual magnetosomes within a chain [17]. The final magnetosome chain organization is dependent on a number of complex processes including the biological control of the growth and assembly of magnetosomes. Furthermore magnetic interactions of particles play an important role in the final observed organization of magnetosome chains. TEM [18] and electron holography measurements [18,19] have shown that the magnetic interactions that dictate the magnetic anisotropy present in magnetosome chains are largely due to dipolar interactions of magnetosomes whereas alignment along the magnetic easy axis plays a significantly smaller role. Electron holography was also used to map the magnetic microstructure of a MV-1 magnetosome chain [7]. That study, the first to map the magnetic moment of a single magnetosome chain, measured a moment of 7610216 Am2 for a chain containing 15 magnetosomes (,1600 nm long) [7]. Several studies have shown that some magnetosome proteins play an important role in magnetosome chain organization. MamJ has been shown to anchor magnetosomes to a filament while MamK [20,21] is required for magnetosome organization into a single chain. Scheffel et al. [20] showed through cryo-electron tomography measurements that DMamJ deletion mutants of Magnetospirillum gryphiswaldense show no organization of magnetosomes despite the presence of cytoskeletal filaments which magnetosomes anchor onto in wild type cells. Komeili et al. [21] used cryo-electron tomography to show that the cytoskeletal filament is composed of MamK (...truncated)