Abstract
Leptothrix species produce microtubular organic–inorganic materials that encase the bacterial cells. The skeleton of an immature sheath, consisting of organic exopolymer fibrils of bacterial origin, is formed first, then the sheath becomes encrusted with inorganic material. Functional carboxyl groups of polysaccharides in these fibrils are considered to attract and bind metal cations, including Fe(III) and Fe(III)-mineral phases onto the fibrils, but the detailed mechanism remains elusive. Here we show that NH2 of the amino-sugar-enriched exopolymer fibrils is involved in interactions with abiotically generated Fe(III) minerals. NH2-specific staining of L. cholodnii OUMS1 detected a terminal NH2 on its sheath skeleton. Masking NH2 with specific reagents abrogated deposition of Fe(III) minerals onto fibrils. Fe(III) minerals were adsorbed on chitosan and NH2-coated polystyrene beads but not on cellulose and beads coated with an acetamide group. X-ray photoelectron spectroscopy at the N1s edge revealed that the terminal NH2 of OUMS1 sheaths, chitosan and NH2-coated beads binds to Fe(III)-mineral phases, indicating interaction between the Fe(III) minerals and terminal NH2. Thus, the terminal NH2 in the exopolymer fibrils seems critical for Fe encrustation of Leptothrix sheaths. These insights should inform artificial synthesis of highly reactive NH2-rich polymers for use as absorbents, catalysts and so on.
Highlights
Fe(III)-mineral phases onto the fibrils, but the detailed mechanism remains elusive
A strong correlation exists between the presence of acidic polysaccharides with carboxyl groups (COOH) and the distribution of iron oxyhydroxides in Leptothrix sheaths[6, 26], but little is known about the roles of NH2 within the sheath fibrils on the metal encrustation
We sought to ascertain the involvement of the terminal NH2 within the constitutive molecules of the immature sheath skeleton of OUMS1-WT in the adsorption of Fe(III) minerals to the skeleton by differential interference contrast (DIC) and fluorescent microscopy, scanning, transmission, and scanning-transmission electron microscopy (SEM, TEM, and STEM, respectively), energy-dispersive x-ray microanalysis (EDX), x-ray fluorescence and photoelectron spectroscopy (XRF and X-ray photoelectron spectroscopy (XPS), respectively) (Fig. 1)
Summary
Fe(III)-mineral phases onto the fibrils, but the detailed mechanism remains elusive. Leptothrix species, common inhabitants of freshwater environments, oxidize Fe(II) in the presence of low oxygen concentrations[11,12,13] and divide to form catenulate cells They excrete exopolymer fibrils, which are entangled with interfibrillar cross-linkers such as proteins and disulfide bridges to eventually form a microtubular, immature, organic sheath skeleton[7, 14, 15]. Sugar analysis of sheath fibrils prepared from L. cholodnii SP-6 (hereafter referred to as SP-6) has elucidated that the basic structure of sheath fibrils comprise heteropolysaccharides containing galactosamine (GalN) and glucosamine (GlcN), both of which have a terminal NH216 Another polysaccharide polymer with a terminal NH2, chitosan, is frequently used to adsorb transition metals from wastewater via the chelating ability of NH2 and an adjacent hydroxyl group[17,18,19,20], suggesting that the terminal NH2 within the sheath fibrils might play a key role in metal encrustation. We sought to ascertain the involvement of the terminal NH2 within the constitutive molecules of the immature sheath skeleton of OUMS1-WT in the adsorption of Fe(III) minerals to the skeleton by differential interference contrast (DIC) and fluorescent microscopy, scanning, transmission, and scanning-transmission electron microscopy (SEM, TEM, and STEM, respectively), energy-dispersive x-ray microanalysis (EDX), x-ray fluorescence and photoelectron spectroscopy (XRF and XPS, respectively) (Fig. 1)
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