High‐resolution 2D and 3D cryo‐TEM reveals structural adaptations of two stalk‐forming bacteria to an Fe‐oxidizing lifestyle

Abstract

Aerobic neutrophilic Fe-oxidizing bacteria (FeOB) thrive where oxic and iron-rich anoxic waters meet. Here, iron microbial mats are commonly developed by stalk-forming Fe-oxidizers adapted to these iron-rich gradient environments, somehow avoiding iron encrustation. Few details are known about FeOB physiology; thus, the bases of these adaptations, notably the mechanisms of interactions with iron, are poorly understood. We examined two stalked FeOB: the marine Zetaproteobacterium Mariprofundus ferrooxydans and a terrestrial Betaproteobacterium Gallionella-like organism. We used cryo-transmission electron microscopy and cryo-electron tomography to provide unprecedented ultrastructural data on intact cell-mineral systems. Both FeOB localize iron mineral formation at stalk extrusion sites, while avoiding surface and periplasmic mineralization. The M. ferrooxydans cell surface is densely covered in fibrils while the terrestrial FeOB surface is smooth, suggesting a difference in surface chemistry. Only the terrestrial FeOB exhibited a putative chemotaxis apparatus, which may be due to differences in chemotaxis mechanisms. Both FeOB have a single flagellum, which alone is insufficient to account for cell motion during iron oxidation, suggesting that stalk extrusion is a mechanism for motility. Our results delineate the physical framework of iron transformations and characterize possible structural adaptations to the iron-oxidizing lifestyle. This study shows ultrastructural similarities and differences between two distinct FeOB, setting the stage for further (e.g. genomic) comparisons that will help us understand functional differences and evolutionary history.