Nanometer-Scale Visualization and Structural Analysis of the Inorganic/Organic Hybrid Structure of Gallionella ferruginea Twisted Stalks

Abstract

The so-called Fe/Mn-oxidizing bacteria have long been recognized for their potential to form extracellular iron hydroxide or manganese oxide structures in aquatic environments. Bacterial species belonging to the genus Gallionella, one type of such bacteria, oxidize iron and produce uniquely twisted extracellular stalks consisting of iron oxide-encrusted inorganic/organic fibers. This paper describes the ultrastructure of Gallionella cells and stalks and the visualized structural and spatial localization of constitutive elements within the stalks. Electron microscopy with energy-dispersive X-ray microanalysis showed the export site of the stalk fibers from the cell and the uniform distribution of iron, silicon, and phosphorous in the stalks. Electron energy-loss spectroscopy revealed that the stalk fibers had a central carbon core of bacterial exopolymers and that aquatic iron interacted with oxygen at the surface of the carbon core, resulting in deposition of iron oxides at the surface. This new knowledge of the structural and spatial associations of iron with oxygen and carbon provides deeper insights into the unique inorganic/organic hybrid structure of the stalks.Some microorganisms convert metal ions to their oxidized forms by enzymatic removal of electrons, causing physicochemical reactions associated with the resulting change of the local pH (19). The so-called Fe/Mn-oxidizing bacteria have long been recognized for their potential to form extracellular iron hydroxide or manganese oxide structures in aquatic environments (5,8,12,15,16,17). Bacteria belonging to the genus Gallionella are ubiquitous inhabitants of ocherous deposits that form in bodies of freshwater (5). They form a uniquely twisted extracellular iron oxide-encrusted bundle of fibers (commonly called a twisted stalk) (5). It is presently thought that the extracellular polysaccharides from the cell, which are the major organic components of the stalk, are closely linked with its mineralization by Fe, Si, and P (2, 4, 5, 7) and other minor elements (5). However, the structural origin and the presence of the stalk polysaccharides and the spatial association of elements within their structure remain unsolved in spite of a number of ultrastructural studies (2,7,11,14,18).Iron-oxidizing bacteria such as Gallionella, Leptothrix, Mariprofundus, and Rhodobacter (3,5,8,12,15,16,17), with the ability to form extracellular iron oxides, have evoked great interest in biological and geochemical fields of research. The potential for future industrial use of these biologically derived iron oxides clearly indicates the need for detailed systematic study of the interactions of the biological organics with the aquatic metals and minerals in the stalks. The aim of this study is to examine the ultrastructure of Gallionella cells and stalks and to define the structural and spatial localization of constitutive elements within the stalks. Our analyses included the use of scanning electron microscopy (SEM)/transmission electron microscopy (TEM) with energy-dispersive ...

Silicon and Phosphorus Linkage with Iron via Oxygen in the Amorphous Matrix of Gallionella ferruginea Stalks

“…1D, arrowhead). These features are consistent with earlier descriptions of Gallionella ferruginea (21,25,52). …”

Structural and Spatial Associations between Fe, O, and C in the Network Structure of the Leptothrix ochracea Sheath Surface

“…2J), in which the intense red Fe signals are localized at the fiber margin, but the green and/or yellowish signals are not. Suzuki et al (15) detected similar Fe/C localization patterns in Gallionella stalk fibers using EELS and proposed that (i) the C fibrils probably excreted from the bacterial cells were intermingled and folded at the fiber core region but not at the extreme margin and (ii) oxidized Fe could interact with C in the entire fiber. The biotic and abiotic Fe (11) measured rates of biological and autocatalytic oxidation in Fe-oxidizing bacteriainhabiting mats and showed the same order of magnitude for both oxidations.…”

“…Our previous EELS mapping (15) suggested that Fe could exist as iron oxide and/or oxyhydroxide in the fibers of G. ferruginea. It is likely that organic fibrils in the stalks and sheaths collect iron oxyhydroxides and control its recrystallization in the structures, which possibly explains the natural formation of the mineralized structures, as suggested by Chan et al (1, 2).…”

“…A diluted suspension of fragmented sheaths was air dried on a copper grid and subjected to HAADF-STEM imaging and STEM-EELS mapping, as described in our previous paper (15). The coarse network exposed at the broken plane of the sheath was analyzed using the aberration-corrected STEM (JEM-2100F with the CEOS C s -corrector).…”

Microaerophilic Fe(II)-Oxidizing Zetaproteobacteria Isolated from Low-Fe Marine Coastal Sediments: Physiology and Composition of Their Twisted Stalks

“…They demonstrated Ni 2ϩ immobilization for stalks produced by microaerophilic Fe(II)-oxidizing bacteria collected from an abandoned mine. Sorption of other transition metals to twisted stalks has also been reported (31,34,35,37,63). Therefore, the presence of twisted stalks affects the availability of transition metals not only for the stalk-forming bacteria but also for other microorganisms.…”