The ultrastructure of chemolithoautotrophic Gallionella ferruginea and Thiobacillus ferrooxidans as revealed by chemical fixation and freeze-etching

Lütters, Susanne; Hanert, Hans H.

doi:10.1007/bf00413137

Cited by 23 publications

(18 citation statements)

References 26 publications

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“…3). The close relationship to the chemolithotrophic Gallionella ferruginea is also reflected by an extensive intracellular membrane system, also found in some Nitrosomonas species, consisting (in part) of irregular tubes protruding into the cytoplasm continuous with the cytoplasmic membrane (30). The tubular membrane system of R purpureus also resembles those of Gallionella femuginea and some Nitrosomonas species.…”

Section: Resultsmentioning

confidence: 71%

Evolutionary relationships among ammonia- and nitrite-oxidizing bacteria

Alm²,

et al. 1994

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Comparative 16S rRNA sequencing was used to evaluate phylogenetic relationships among selected strains of ammonia-and nitrite-oxidizing bacteria. All characterized strains were shown to be affiliated with the proteobacteria. The study extended recent 16S rRNA-based studies of phylogenetic diversity among nitrifiers by the comparison of eight strains of the genus Nitrobacter and representatives of the genera Nitrospira and Nitrospina. The later genera were shown to be affiliated with the delta subdivision of the proteobacteria but did not share a specific relationship to each other or to other members of the delta subdivision. All characterized Nitrobacter strains constituted a closely related assemblage within the alpha subdivision of the proteobacteria. As previously observed, all ammonia-oxidizing genera except Nitrosococcus oceanus constitute a monophyletic assemblage within the beta subdivision of the proteobacteria. Errors in the 16S rRNA sequences for two strains previously deposited in the databases by other investigators (Nitrosolobus multiformis C-71 and Nitrospira briensis C-128) were corrected. Consideration of physiology and phylogenetic distribution suggested that nitrite-oxidizing bacteria of the alpha and gamma subdivisions are derived from immediate photosynthetic ancestry. Each nitrifier retains the general structural features of the specific ancestor's photosynthetic membrane complex. Thus, the nitrifiers, as a group, apparently are not derived from an ancestral nitrifying phenotype.Biologists have been asking questions concerning the evolutionary origins of, and phylogenetic relationships among, chemolithotrophic microorganisms for well over a century. However, it has been only in the last decade that comparative molecular studies have provided the basis to shape an understanding of their phylogeny. Most notably, the use of comparative rRNA sequencing has provided an all-encompassing phylogenetic framework within which all the chemolithotrophs can be placed. The emerging phylogeny has, in turn, provided insights into their antiquity and the origins of lithotrophic metabolism. For example, sulfur oxidation and iron oxidation appear to be evolutionarily early and widespread metabolic modes that are not confined to a single phylogenetic assemblage of bacteria (27). An University, Evanston, with secondary consideration of cell shape and the highly characteristic cytoplasmic membrane structures (46). All known ammonia-oxidizing bacteria are obligate chemolithoautotrophs. In contrast, some nitrite-oxidizing bacteria are mixotrophs and also can grow heterotrophically (4, 26). Although the existing taxonomy assigns these bacteria to a single family, accumulating biochemical and molecular data do not support their phylogenetic coherence.Physiological and enzymatic data argue against a close relatedness between ammonia and nitrite oxidizers. They employ two very different key enzyme systems for the energygaining oxidation of ammonia and nitrite (5). Comparative sequencing studies based on 16S rRNA oli...

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Section: Resultsmentioning

confidence: 71%

Evolutionary relationships among ammonia- and nitrite-oxidizing bacteria

Alm²,

et al. 1994

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“…2c), the elongated fibers show strong Fe signals, but the bacterial cell shows only traces. Lutters and Hanert (11) found that an intracytoplasmic membrane system invaginated from the concave side of the Gallionella cell and concluded that this system was involved in Fe 2ϩ oxidation and Fe 3ϩ excretion. Kucera and Wolfe (10) noted that Gallionella cells possessed the unusual ability to secrete twisted, Fe 3ϩ -encrusted stalks.…”

Section: Resultsmentioning

confidence: 99%

“…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.…”

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confidence: 99%

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

Suzuki

Hashimoto

Matsumoto

et al. 2011

Appl Environ Microbiol

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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 ...

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“…A plausible explanation for this difference is that the energy cost for stalk formation decreases the survivability for Sta + in conditions where the stalk is unneeded. The Sta-cells, on the other hand, can use reserve carbon such as PHB, (poly-[3-hydroxybutyrate) or glycogen [18] solely for a maintaining metabolism instead of both metabolism and stalk formation, rendering a prolonged survival. The observation that our pure cultures frequently lost the ability to produce a stalk when grown in the FC-medium confirms that the stalk is not of critical importance for growth and survival in this medium.…”

Section: Discussionmentioning

confidence: 99%

Benefits associated with the stalk of Gallionella ferruginea, evaluated by comparison of a stalk-forming and a non-stalk-forming strain and biofilm studies in situ

Hallbeck

Pedersen

1995

Microb Ecol

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Factors that regulate and induce stalk formation by the iron-oxidizing and stalk-forming bacterium Gallionella ferruginea were studied in laboratory cultures and in situ. A stalk-forming strain, Sta(+), and a non-stalk-forming strain, Sta(-), were used for comparative studies of the benefits associated with the stalk. Two different growth media were used: a ferrous sulfide medium (FS-medium), with slow oxidation of iron giving high concentrations of toxic oxygen radicals and a ferrous carbonate medium (FC-medium), with fast iron oxidation giving low concentration of the toxic oxygen radicals. It was found that Sta(+) cells grown in the FS-medium survived 3 weeks longer than Sta(-) cells grown in the FS-medium. When each strain was grown in the FC-medium, the Sta(-) cells had an advantage and survived 8 weeks longer than the Sta(+) cells. No difference in survival was found for Sta(+) cells grown in FS-medium compared to growth in FC-medium. In laboratory cultures, the average stalk length per cell values were 7-2.5 times higher (92 h and 150-300 h growth, respectively) in a medium with 620 μM iron than in a medium with 290 μM iron. Gallionella ferruginea Sta(+) outcompeted Sta(-) cells when inoculated as mixed populations in FC-medium. It has previously been suggested that stalk formation in vitro is induced by oxygen. To confirm this observation, biofilm development in natural waters was studied in two wells, one with trace amounts of oxygen (LH) and one without (TH). A dense biofilm developed on surfaces exposed to flowing well LH water, but no biofilm developed in well TH. Stalks were formed in water samples from both wells when allowed to make contact with air. This work demonstrates for the first time that the stalk has a protecting function against the toxic oxygen radicals formed during the chemical iron oxidation. It also shows that it is the oxidation rate of the ferrous iron and not its concentration that is harmful to the cells. The stalk gives G. ferruginea a unique possibility to colonize and survive in habitats with high contents of iron, inaccessible for bacteria without a defense system against the oxidation of iron.

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The ultrastructure of chemolithoautotrophic Gallionella ferruginea and Thiobacillus ferrooxidans as revealed by chemical fixation and freeze-etching

Cited by 23 publications

References 26 publications

Evolutionary relationships among ammonia- and nitrite-oxidizing bacteria

Evolutionary relationships among ammonia- and nitrite-oxidizing bacteria

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

Benefits associated with the stalk of Gallionella ferruginea, evaluated by comparison of a stalk-forming and a non-stalk-forming strain and biofilm studies in situ

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