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Halophilic Archaeon Haloquadratum Walsbyi Morphological and Structural Aspects of the Extremely Halophilic Archaeon Haloquadratum walsbyi Matilde Sublimi Saponetti1*, Fabrizio Bobba1, Grazia Salerno1, Alessandro Scarfato1, Angela Corcelli2, Annamaria Cucolo1 1 Department of Physics and Research Centre NanoMateS, University of Salerno and SPIN-CNR, Fisciano, Italy, 2 Department of Medical Biochemistry, Biology and Physics, University of Bari and IPCF-CNR, Bari, Italy Abstract Ultrathin square cell Haloquadratum walsbyi from the Archaea domain are the most abundant microorganisms in the hypersaline water of coastal salterns and continental salt lakes. In this work, we explore the cell surface of these microorganisms using amplitude-modulation atomic-force microscopy in nearly physiological conditions. We demonstrate the presence of a regular corrugation with a periodicity of 16–20 nm attributed to the surface layer (S-layer) protein lattice, striped domains asymmetrically distributed on the cell faces and peculiar bulges correlated with the presence of intracellular granules. Besides, subsequent images of cell evolution during the drying process indicate the presence of an external capsule that might correspond to the giant protein halomucin, predicted by the genome but never before observed by other microscopy studies. Citation: Sublimi Saponetti M, Bobba F, Salerno G, Scarfato A, Corcelli A, et al. (2011) Morphological and Structural Aspects of the Extremely Halophilic Archaeon Haloquadratum walsbyi. PLoS ONE 6(4): e18653. doi:10.1371/journal.pone.0018653 Editor: Purification Lopez-Garcia, Universite´ Paris Sud, France Received October 27, 2010; Accepted March 13, 2011; Published April 29, 2011 Copyright: ß 2011 Sublimi Saponetti et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: The authors have no support or funding to report. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] Introduction a wall with a thickness ranging from 15 to 25 nm and with a regular structure consisting of circular particles. In freeze-fracture The extremely halophilic archaeon Haloquadratum walsbyi was plane sections, it has also been observed that these particles appear first discovered in a coastal brine pool in the Sinai peninsula, to be arranged into orthogonal or hexagonal patterns with a Egypt, in the early 1980s; this novel organism aroused consider- spacing of approximately 23 nm; however, oblique sections able interest in the scientific community because of its square cell suggest more complex patterns, which vary among the different shape and its ability to inhabit environments extremely rich in salts microorganisms analysed [9,10]. More recently, electron cryomi- at the limit of water activity [1,2]. For a long time, investigations croscopy images of two different strains of H. walsbyi, C23 and into the physiology and biochemistry of H. walsbyi were very HBSQ001, have revealed similar internal structures such as gas limited, because of the difficulties inherent in obtaining axenic vesicles and poly-b-hydroxybutyrate (PHB) granules, whereas the cultures of the microorganism. Recently, two independent groups cell wall of the isolate HBSQ001 showed an apparently three- isolated and cultivated H. walsbyi and sequenced its genome layered complex structure [11]. [3,4,5]. Like other members of the Halobacteriaceae family, the H. In this work, we studied the haloarchaeon H. walsbyi strain walsbyi genome encodes photoactive retinal proteins of the HBSQ001 by Atomic Force Microscopy (AFM) to acquire new membrane and S-layer glycoproteins of the cell wall [6]. One of morphological details that had not yet been revealed by Electron the peculiarities arising from the genomic analysis is its ability to Microscopy analysis. In comparison with previous high-resolution express the giant protein halomucin, which should play an microscopy studies, by using amplitude modulation AFM, important role in protecting cells against desiccation by creating commonly referred to as either alternate contact (AC) mode or an aqueous shield covering the cells. Recently, the lipidome of the tapping mode, we analyzed native biological samples in nearly square cells has also been described [7,8]. To date, optical phase physiological conditions, thus minimizing any damage or artefacts contrast, confocal fluorescence and electron microscopy analyses due to fixation procedures [12,13]. In addition, we exploited the have been carried out to show the morphological features of these unique capability of AFM to monitor in real-time the dynamic microorganisms, which are characterized in three ways: by a evolution of surfaces so as to better understand their morpholog- square or rectangular shape, typically measuring 2–5 mm wide by ical features and their changes during the variations in 0.1–0.2 mm thick; by the presence of highly refractive gas vesicles environmental conditions. In this study, two different AFM (Fig. 1); and by poly-b-hydroxyalkanoate (PHA) granules in the experiments were carried out: in the first, we explored the cell cytoplasm [1,2]. Most microscopy studies have aimed to describe surface in an attempt to identify areas with different elasticity its intracellular organization, but only few details regarding the cell properties, while in the second, by continuously imaging cells wall have been reported. Some authors describe a structural during the drying process, we demonstrated the presence of a variability among different isolates. In one of the first studies on capsule appearing as a thin film external to the cell wall that, in cells collected from natural samples, the square organisms showed archaea, is constituted only by the surface layer (S-layer). PLoS ONE | www.plosone.org 1 April 2011 | Volume 6 | Issue 4 | e18653 Atomic Force Microscopy Study of an Archaeal Cell that modifies the average tip-surface separation. This provides a measurement of the surface corrugation, affording height profiles for each line, in other words imaging the surface topography. Simultaneously, the phase shift between the cantilever oscilla- tion and the oscillating driving force can be measured by means of phase imaging. In this case, as consequence of tip/sample interaction, different material properties of the surface are correlated with different phase shifts, and so phase imaging can be used to identify areas from a sample in terms of such differing properties as stiffness, adhesion, and viscoelasticity. The optimal oscillation frequency is different for height imaging and for phase imaging. In the former, it is convenient to operate at an oscillation driving frequency lower than the cantilever resonance frequency so that the gain can be calculated from the higher slope of the amplitude frequency response curve. By contrast, in order to optimise phase imaging, it is convenient to operate with a driving oscillation at the cantilever resonance frequency so as to get gain from the higher and more linear slope of the phase-frequency response curve at the expense of reduced topographic height resolution. Finally, when optimising for phase imaging and/or when the feedback amplitude is not correctly regulated, images Figure 1. Optical phase-contrast microscopy image of a H. obtained by acquiring the amplitude error signal, commonly walsbyi square cell. The numerous light dots represent gas vesicles. referred to as amplitude imaging, also revealed topographic Overall size is 10610 mm. Scale bar 1 mm. features with high lateral resolution but without any three- doi:10.1371/journal.pone.0018653.g001 dimensionality. Operating in AC mode on soft biological samples eliminates Materials and Methods lateral forces such as friction, adhesion, and electrostatic dragging, thus improving lateral resolution and allowing imaging for Microorganism culture specimens poorly adsorbed on a substrate. We studied the haloarchaeal cell H. walsbyi (strain HBSQ001) Effectively, in our experiments, after the tip was engaged on a provided by F. Rodrı´guez-Valera. The square cells were grown in selected point of the surface, the scan range was gradually liquid growth medium (HAS medium) containing per liter: 195 g increased, while optimizing appropriate scan parameters for the NaCl; 50 g MgSO4?7H2O; 35 g MgCl2?6H2O; 5 g KCl; 0.25 g sample’s roughness. The rule used to get low noise and low applied NaHCO3; 1 g NaNO3; 0.5 g CaCl2?2H2O; 0.05 g KH2PO4; tip forces was to identify a minimal driving amplitude and 0.03 g NH4Cl and 20 ml Tris-HCl (1 M, pH 7.4), supplemented maximal tapping amplitude setpoint. At low magnification (frame with 0.5 g glycerol, 0.1 g yeast extract and 1 g sodium pyruvate. size of about 3–5 mm), imaging was performed with scan rates in The strain was grown aerobically in light in a gyratory shaker at the range of 0.3–1 Hz while, at high magnification (sub-micron 80 rpm and 40uC [3]. frame size), scan rates were kept in the 1–3 Hz range. Images were recorded simultaneously in both height, amplitude error and phase AFM analysis modalities. In height imaging, the driving frequency was lower We operated both on dried and on liquid samples. Liquid than the resonance frequency so as to get higher sensitivity in the samples were prepared by applying a 10 ml droplet of cells in the tapping amplitude variations, whereas when optimizing for phase stationary growth phase onto
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