A nutrient uptake role for bacterial cell envelope extensions

Abstract

Bacteria exist in a variety of morphologies, but the relationship between cellular forms and biological functions remains poorly understood. We show that stalks (prosthecae), cylindrical extensions of the Caulobacter crescentus cell envelope, can take up and hydrolyze organic phosphate molecules and contain the highaffinity phosphate-binding protein PstS, but not PstA, a protein that is required for transport of phosphate into the cytoplasm. Therefore, uptake, hydrolysis, and periplasmic binding of a phosphate source can take place in the stalk, but high-affinity import must take place in the cell body. Furthermore, by using analytical modeling, we illustrate the biophysical advantage of the stalk as a morphological adaptation to the diffusion-limited, oligotrophic environments where C. crescentus thrives. This advantage is due to the fact that a stalk is long and thin, a favorable shape for maximizing contact with diffusing nutrients while minimizing increases in both surface area and cell volume.acteria exhibit an amazing diversity of shapes and sizes. Bacterial cells can be round, cylindrical, curved, or coiled. Some are shaped like a flat square, others like a star; some are branched, and some have projections of the cell surface. Exactly how bacterial shapes are generated is not known, and the purposes of a specific cell shape are not always clear. Yet, in most cases, specific shapes are precisely reproduced at every generation. Cell shape changes can also occur during the life cycle of many bacterial species, such as the transformation of Sinorhizobium from rods to branched cells (Y forms) after colonization of legume root nodules. Although these morphological transformations are thought to play important roles in the life cycles of bacteria, the advantages of cell shape changes remain essentially speculative (1).Here, we investigate the function of prosthecae, cell envelope extensions that are present in a morphologically diverse group of Gram-negative bacteria (2). Unlike flagella or pili, prosthecae are true extensions of the cell proper, possessing both peptidoglycan and cell membranes. In the aquatic bacterium Caulobacter crescentus, prosthecae are referred to as stalks. The function of Caulobacter stalks is not known, but one common hypothesis is that they facilitate the acquisition of nutrients from the environment (3, 4). This hypothesis is consistent with the observation that stalks dramatically elongate under phosphate starvation conditions, with the capacity to reach lengths of Ͼ30 m (5, 6), a length that is approximately equivalent to that of 15 cell bodies. We show that the stalk of C. crescentus (Fig. 1A) can transport a nutrient molecule from the extracellular space into its periplasm and that the stalk constitutes a biophysically efficient morphological adaptation to environments where nutrient uptake is limited by diffusion. Results Stalks Can Take Up and Hydrolyze Fluorescein Diphosphate (FDP).To determine whether stalks are capable of nutrient uptake, we incubated cells with FDP, a fluor...

Protein localization and dynamics within a bacterial organelle

“…1B). The peripheral distribution of CC1679, a predicted periplasmic protein harboring an N-terminal SS, but no TM domains, is consistent with the notion that the periplasm is contiguous between the cell body and the stalk (18). In support of this, fragments with the putative SS of the BlaA (CC2139) β-lactamase (residues 1-50) or StpX (residues 1-49) are sufficient to yield mCherry-derived fluorescence along the cell body and the stalk (Fig.…”

The BAM complex subunit BamE (SmpA) is required for membrane integrity, stalk growth and normal levels of outer membrane β-barrel proteins in Caulobacter crescentus

“…Caulobacter cells grow elongated stalks (Gonin et al, 2000;Schmidt & Stanier, 1966) which enhance nutrient uptake (Wagner et al, 2006). Some strains, such as the mutants ctrA401 (Quon et al, 1996), rpoN (Brun & Shapiro, 1992) and tacA (Biondi et al, 2006;Skerker et al, 2005), are stalkless in rich medium but build polar stalks in low-phosphate medium.…”

“…Stalk biogenesis is initiated once in the life of the cell, during differentiation of the swarmer progeny into a stalked cell, and stalk growth continues throughout the life of the cell (Stove & Stanier, 1962). Stalks become elongated under conditions of phosphate limitation (Gonin et al, 2000;Schmidt & Stanier, 1966), and isolated stalks take up the fluorogenic organophosphate compound fluorescein diphosphate (Wagner et al, 2006). Stalk growth could be mediated by the same proteins that build the cell envelope as a whole, but there may also be a dedicated pathway for the assembly of stalk-specific proteins.…”

Irreversible adsorption of gold nanospheres on fiber optical tapers and microspheres

“…The effect can be advantageous both in device fabrication and in sensing applications, where a sensor placed on a highly curved surface will have a faster response than one placed on a flat surface. 3 This work was supported by the National Institute of Occupational Safety and Health (Grant No. 1U60OH009761-01) and the National Science Foundation (Grant No.…”

“…It is also of interest in biomedicine in describing processes such as ligand binding to macromolecules or digestion by microbes and cells. 3,4 It is then not surprising that the problem has been studied for a long time and that theoretical treatments have reached a high degree of sophistication. 5 However, the bulk of the experimental work in this field has been done on planar surfaces, and studies of adsorption onto curved collecting surfaces 4,6 have generally concerned regimes that are not directly applicable to optical and plasmonic device fabrication.…”