Magnetism plays a pivotal role in many biological systems. However, the intensity of the magnetic forces exerted between magnetic bodies is usually low, which demands the development of ultra-sensitivity tools for proper sensing. In this framework, magnetic force microscopy (MFM) offers excellent lateral resolution and the possibility of conducting single-molecule studies like other single-probe microscopy (SPM) techniques. This comprehensive review attempts to describe the paramount importance of magnetic forces for biological applications by highlighting MFM’s main advantages but also intrinsic limitations. While the working principles are described in depth, the article also focuses on novel micro- and nanofabrication procedures for MFM tips, which enhance the magnetic response signal of tested biomaterials compared to commercial nanoprobes. This work also depicts some relevant examples where MFM can quantitatively assess the magnetic performance of nanomaterials involved in biological systems, including magnetotactic bacteria, cryptochrome flavoproteins, and magnetic nanoparticles that can interact with animal tissues. Additionally, the most promising perspectives in this field are highlighted to make the reader aware of upcoming challenges when aiming toward quantum technologies.

A Review of the Current State of Magnetic Force Microscopy to Unravel the Magnetic Properties of Nanomaterials Applied in Biological Systems and Future Directions for Quantum Technologies

Abstract Magnetotactic bacteria (MTB) are a group of phylogenetically and morphologically diverse prokaryotes that have the capability of sensing Earth's magnetic field via nanocrystals of magnetic iron minerals. These crystals are enclosed within intracellular membranes or organelles known as magnetosomes and enable a sensing function known as magnetotaxis. Although MTB were discovered over half a century ago, the study of the magnetosome biogenesis and organization remains limited to a few cultured MTB strains. Here, we present an integrative genomic and phenomic analysis to investigate the genetic basis of magnetosome biomineralization in both cultured and uncultured strains from phylogenetically diverse MTB groups. The magnetosome gene contents/networks of strains are correlated with magnetic particle morphology and chain configuration. We propose a general model for gene networks that control/regulate magnetosome biogenesis and chain assembly in MTB systems.

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Key gene networks that control magnetosome biomineralization in magnetotactic bacteria

Dissimilatory iron-reducing bacteria (DIRB) oxidize organic matter or hydrogen and reduce ferric iron to form Fe(II)-bearing minerals, such as magnetite and siderite. However, compared with magnetite, which was extensively studied, the mineralization process and mechanisms of siderite remain unclear. Here, with the combination of advanced electron microscopy and synchrotron-based scanning transmission X-ray microscopy (STXM) approaches, we studied in detail the morphological, structural, and chemical features of biogenic siderite via a growth experiment with Shewanella oneidensis MR-4. Results showed that along with the growth of cells, Fe(II) ions were increasingly released into solution and reacted with CO32- to form micrometer-sized siderite minerals with spindle, rod, peanut, dumbbell, and sphere shapes. They are composed of many single-crystal siderite plates that are fanned out from the center of the particles. Additionally, STXM revealed Fh and organic molecules inside siderite. This suggests that the siderite crystals might assemble around a Fh-organic molecule core and then continue to grow radially. This study illustrates the biomineralization and assembly of siderite by a successive multistep growth process induced by DIRB, also provides evidences that the distinctive shapes and the presence of organic molecules inside might be morphological and chemical features for biogenic siderite.

Morphological, Microstructural, and In Situ Chemical Characteristics of Siderite Produced by Iron-Reducing Bacteria.

Inspired by nature’s remarkable ability to form intricate minerals, researchers have unlocked transformative strategies for creating next-generation biosensors with exceptional sensitivity, selectivity, and biocompatibility. By mimicking how organisms orchestrate mineral growth, biomimetic and bioinspired materials are significantly impacting biosensor design. Engineered bioinspired materials offer distinct advantages over their natural counterparts, boasting superior tunability, precise controllability, and the ability to integrate specific functionalities for enhanced sensing capabilities. This remarkable versatility enables the construction of various biosensing platforms, including optical sensors, electrochemical sensors, magnetic biosensors, and nucleic acid detection platforms, for diverse applications. Additionally, bioinspired materials facilitate the development of smartphone-assisted biosensing platforms, offering user-friendly and portable diagnostic tools for point-of-care applications. This review comprehensively explores the utilization of naturally occurring and engineered biominerals and materials for diverse biosensing applications. We highlight the fabrication and design strategies that tailor their functionalities to address specific biosensing needs. This in-depth exploration underscores the transformative potential of biominerals and materials in revolutionizing biosensing, paving the way for advancements in healthcare, environmental monitoring, and other critical fields.

Biominerals and Bioinspired Materials in Biosensing: Recent Advancements and Applications

Nickel iron (hydroxyl) hydroxide with unique layered structure and controllable composition is widely regarded as typical oxygen evolution reaction (OER) catalysts. Recently, developing top-down approaches to realize the facile preparation of transition metal hydroxide catalyst is received widely attention. Based on the natural microorganism corrosion behavior, this work demonstrates the external magnetic field-assisted microbial corrosion strategy to construct advanced transition metal hydroxide OER catalyst, and the prepared biofilm electrode presents superior OER performance in the existence of magnetic field, which needs an overpotential of 287 mV at 100 mA cm-2. Experimental and theoretical calculations show the applied magnetic field can accelerate sulfate reducing bacteria (SRB) corrosion and chemical corrosion. The additional magnetic field can promote SRB corrosion to produce FeS, which can facilitate the optimization of O intermediate desorption from the NiOOH catalyst during the OER process, reducing the reaction energy barrier for O→OOH. The synergistic effect between the nickel-iron oxyhydroxides originated from the accelerated chemical corrosion and FeS produced from the accelerated SRB corrosion interpret the improved OER activity. This work explores the influence of magnetic field on the construction of advanced OER materials, which can provide an effective magnetic field-assisted corrosion engineering strategy, and promote the development of multidisciplinary fields of physics, biology, and emerging energy conversion technologies. 

Magnetic Field-assisted Microbial Corrosion Construction Iron Sulfides Incorporated Nickel-Iron Hydroxide towards Efficient Oxygen Evolution

Magnetotactic bacteria (MTB) biomineralize intracellular magnetic nanocrystals and swim along geomagnetic field lines. While few axenic MTB cultures exist, living cells can be separated magnetically from natural environments for analysis. The bacterial universal 27F/1492R primer pair has been used widely to amplify nearly full-length 16S rRNA genes and to provide phylogenetic portraits of MTB communities. However, incomplete coverage and amplification biases inevitably prevent detection of some phylogenetically specific or non-abundant MTB. Here, we propose a new formulation of the upstream 390F primer that we combined with the downstream 1492R primer to specifically amplify 1,100-bp 16S rRNA gene sequences of sulfate-reducing MTB in freshwater sediments from Lake Weiyanghu, Xi'an, northwestern China. With correlative fluorescence in situ hybridization and scanning/transmission electron microscopy, three novel MTB strains (WYHR-2, WYHR-3, and WYHR-4) from the Desulfobacterota phylum were identified phylogenetically and structurally at the single cell level. Strain WYHR-2 produces bullet-shaped magnetosome magnetite, while the other two strains produce both cubic/prismatic greigite and bullet-shaped magnetite. Our results expand knowledge of bacterial diversity and magnetosome biomineralization of sulfate-reducing MTB. We also propose a general strategy for identifying and characterizing uncultured MTB from natural environments. This article is protected by copyright. All rights reserved.

Identification of sulfate-reducing magnetotactic bacteria via a group-specific 16S rDNA primer and correlative fluorescence and electron microscopy: strategy for culture-independent study.

Magnetotactic bacteria (MTB) have the remarkable capability of producing intracellularly membrane-enveloped magnetic nanocrystals (i.e., magnetosomes) and swimming along geomagnetic field lines. Despite more than 50 years of research, bacterial diversity and magnetosome biomineralization within MTB are relatively less known in the Gammaproteobacteria class than other groups. This is incompatible with the status of Gammaproteobacteria as the most diverse class of gram-negative bacteria with a number of ecologically important bacteria. Here, we identify a novel MTB strain YYHR-1 affiliated with the Gammaproteobacteria class of the Pseudomonadota phylum from a freshwater lake. In YYHR-1, most magnetosome crystals are organized into a long chain aligned along the cell long axis, unusually, a few small superparamagnetic crystals are located at the side of the chain, off the main chain axis. Micromagnetic simulations indicate that magnetostatic interactions among adjacent crystals within a chain reduces the Gibbs energy to enhance chain stability. Genomic analysis suggests that duplication of magnetosome gene clusters may result in off-chain magnetosomes formation. By integrating available genomic data from Gammaproteobacteria, the phylogenetic position of MTB in this class is reassigned here. Our new findings expand knowledge about MTB diversity and magnetosome biomineralization, and deepen understanding of the phylogenetics of the Gammaproteobacteria.

Phylogenetics and biomineralization of a novel magnetotactic Gammaproteobacterium from a freshwater lake in Beijing, China.

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Key gene networks that control magnetosome biomineralization in magnetotactic bacteria

Identification of sulfate-reducing magnetotactic bacteria via a group-specific 16S rDNA primer and correlative fluorescence and electron microscopy: strategy for culture-independent study.

Phylogenetics and biomineralization of a novel magnetotactic Gammaproteobacterium from a freshwater lake in Beijing, China.