A nutrient uptake role for bacterial cell envelope extensions
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Edited by A. Dale Kaiser, Stanford University School of Medicine, Stanford, CA, and approved June 8, 2006 (received for review March 13, 2006)
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 high-affinity 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.
Footnotes
- ¶To whom correspondence should be addressed at: Department of Biology, Indiana University, 1001 East Third Street, Bloomington, IN 47405-3700. E-mail: ybrun{at}indiana.edu
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↵ †Present address: Division of Infectious Diseases, Massachusetts General Hospital/Harvard Medical School, Cambridge, MA 02139.
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Author contributions: J.K.W., S.S., L.A.S., J.P.R., and Y.V.B. designed research; J.K.W., S.S., and L.A.S. performed research; J.K.W., S.S., L.A.S., and J.P.R. contributed new reagents/analytic tools; J.K.W., S.S., L.A.S., J.P.R., and Y.V.B. analyzed data; and J.K.W., S.S., L.A.S., J.P.R., and Y.V.B. wrote the paper.
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Conflict of interest statement: No conflicts declared.
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This paper was submitted directly (Track II) to the PNAS office.
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See Commentary on page 11435.
- Abbreviations:
- FDP,
- fluorescein diphosphate;
- IM,
- inner membrane;
- OM,
- outer membrane;
- ABC,
- ATP-binding cassette.
- © 2006 by The National Academy of Sciences of the USA
