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Evolution, purification, and characterization of RC0497: a peptidoglycan amidase from the prototypical spotted fever species Rickettsia conorii

  • Jignesh G. Patel , Hema P. Narra EMAIL logo , Krishna Mohan Sepuru , Abha Sahni , Sandhya R. Golla , Aishwarya Sahni , Amber Singh , Casey L.C. Schroeder , Imran H. Chowdhury , Vsevolod L. Popov and Sanjeev K. Sahni EMAIL logo
Published/Copyright: July 11, 2019
Biological Chemistry
From the journal Biological Chemistry Volume 401 Issue 2

Abstract

Rickettsial species have independently lost several genes owing to reductive evolution while retaining those predominantly implicated in virulence, survival, and biosynthetic pathways. In this study, we have identified a previously uncharacterized Rickettsia conorii gene RC0497 as an N-acetylmuramoyl-L-alanine amidase constitutively expressed during infection of cultured human microvascular endothelial cells at the levels of both mRNA transcript and encoded protein. A homology-based search of rickettsial genomes reveals that RC0497 homologs, containing amidase_2 family and peptidoglycan binding domains, are highly conserved among the spotted fever group (SFG) rickettsiae. The recombinant RC0497 protein exhibits α-helix secondary structure, undergoes a conformational change in the presence of zinc, and exists as a dimer at higher concentrations. We have further ascertained the enzymatic activity of RC0497 via demonstration of its ability to hydrolyze Escherichia coli peptidoglycan. Confocal microscopy on E. coli expressing RC0497 and transmission immunoelectron microscopy of R. conorii revealed its localization predominantly to the cell wall, septal regions of replicating bacteria, and the membrane of vesicles pinching off the cell wall. In summary, we have identified and functionally characterized RC0497 as a peptidoglycan hydrolase unique to spotted fever rickettsiae, which may potentially serve as a novel moonlighting protein capable of performing multiple functions during host-pathogen interactions.

Keywords: endothelial cells; N-acetylmuramoyl-L-alanine amidase; peptidoglycan; RC0497; Rickettsia; spotted fever group

Funding source: National Institute of Allergy and Infectious Diseases

Award Identifier / Grant number: 5R21 AI115231-02

Award Identifier / Grant number: 5R21 AI117483-02

Funding statement: The authors thank and acknowledge the support of Sealy Center for Structural Biology and Molecular Biophysics at the University of Texas Medical Branch (UTMB) at Galveston for providing the research equipment and resources used in this study. The authors also thank the laboratories of Dr. David Walker, MD, and Dr. Rong Fang, MD, PhD, at the UTMB for providing the RC0497 antibody. This work was supported in part by research project grants 5R21 AI115231-02 and 5R21 AI117483-02 from the National Institute of Allergy and Infectious Diseases, Funder Id: http://dx.doi.org/10.13039/100000060 at the National Institutes of Health, Bethesda, MD, and by institutional support funds from the UTMB to our laboratory. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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Supplementary Material

The online version of this article offers supplementary material (https://doi.org/10.1515/hsz-2018-0389).

Received: 2018-10-01
Accepted: 2019-06-29
Published Online: 2019-07-11
Published in Print: 2020-02-25

©2020 Walter de Gruyter GmbH, Berlin/Boston

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  2. Reviews
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  5. Research Articles/Short Communications
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https://doi.org/10.1515/hsz-2018-0389
Keywords for this article
endothelial cells; N-acetylmuramoyl-L-alanine amidase; peptidoglycan; RC0497; Rickettsia; spotted fever group

Articles in the same Issue

  1. Frontmatter
  2. Reviews
  3. Cysteine, glutathione and a new genetic code: biochemical adaptations of the primordial cells that spread into open water and survived biospheric oxygenation
  4. What you see is what you get: activity-based probes in single-cell analysis of enzymatic activities
  5. Research Articles/Short Communications
  6. Protein Structure and Function
  7. Evolution, purification, and characterization of RC0497: a peptidoglycan amidase from the prototypical spotted fever species Rickettsia conorii
  8. Cell Biology and Signaling
  9. Sohlh2 alleviates malignancy of EOC cells under hypoxia via inhibiting the HIF1α/CA9 signaling pathway
  10. Thioredoxin inhibitor PX-12 induces mitochondria-mediated apoptosis in acute lymphoblastic leukemia cells
  11. TMEM100 expression suppresses metastasis and enhances sensitivity to chemotherapy in gastric cancer
  12. Inhibitory effect of activin A on IL-9 production by mouse NK cells through Smad3 signaling
  13. Intracellular distribution of pseudorabies virus UL2 and detection of its nuclear import mechanism
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