Magnetotaxis as an Adaptation to Enable Bacterial Shuttling of Microbial Sulfur and Sulfur Cycling Across Aquatic Oxic‐Anoxic Interfaces

Abstract

AbstractMagnetotactic bacteria (MTB) widely inhabit the oxic‐anoxic interface (OAI) of sediments and water columns, with their motility guided by geomagnetic fields (a behavior known as magnetotaxis). Beside biomineralizing membrane‐enveloped magnetite or greigite nanocrystals called magnetosomes, cells of many MTB groups contain numerous sulfur globules within their cells. Here, by combining transmission electron microscopy and synchrotron‐based scanning transmission X‐ray microscopy, we investigated the cellular structure and chemistry of Candidatus Magnetobacterium casensis (Mcas), a giant rod‐shaped MTB from the Nitrospirae phylum. We find that nitrate‐storing vacuoles and linearly polymeric sulfur globules occur exclusively within some Mcas cells along with magnetosomal magnetite. Genomic prediction indicates that Mcas cells have the potential to oxidize sulfide to sulfate (i.e., S2− → S0 → SO32− → SO42−), to reduce sulfate to sulfide (i.e., SO42− → SO32− → S2−), and to reduce nitrate to NH4+/N2. Together with previous environmental observations, comparative genomic analysis allows us to propose a model for Mcas involving the microbial sulfur cycle across aquatic OAIs based on magnetotaxis. Via directional movement guided by geomagnetic fields, Mcas cells shuttle either upward to upper microoxic zones for sulfur oxidation and nitrate accumulation in the OAI, or downward to deeper anoxic zones for sulfur deposition by coupling sulfide oxidation and nitrate reduction. Development of magnetotaxis makes MTB an efficient bacterial shuttle for C, N, S, and Fe across aquatic OAI environments and likely contributes significantly to their global biogeochemical cycling. It also benefits cell growth and magnetosomal magnetite formation in MTB.