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Plant peptidoglycan precursor biosynthesis : conservation between moss chloroplasts and Gram-negative bacteria

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Dowson, Amanda J., Lloyd, Adrian J., Cuming, Andrew C., Roper, David I., Frigerio, Lorenzo and Dowson, Christopher G. (2022) Plant peptidoglycan precursor biosynthesis : conservation between moss chloroplasts and Gram-negative bacteria. Plant Physiology, 190 (1). pp. 165-179. doi:10.1093/plphys/kiac176 ISSN 1532-2548.

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Official URL: http://dx.doi.org/10.1093/plphys/kiac176

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Abstract

Accumulating evidence suggests that peptidoglycan, consistent with a bacterial cell wall, is synthesized around the chloroplasts of many photosynthetic eukaryotes, from glaucophyte algae to early-diverging land plants including pteridophyte ferns, but the biosynthetic pathway has not been demonstrated. Here, we employed mass spectrometry and enzymology in a two-fold approach to characterize the synthesis of peptidoglycan in chloroplasts of the moss Physcomitrium (Physcomitrella) patens. To drive the accumulation of peptidoglycan pathway intermediates, P. patens was cultured with the antibiotics fosfomycin, D-cycloserine, and carbenicillin, which inhibit key peptidoglycan pathway proteins in bacteria. Mass spectrometry of the trichloroacetic acid-extracted moss metabolome revealed elevated levels of five of the predicted intermediates from uridine diphosphate N-acetylglucosamine (UDP-GlcNAc) through the uridine diphosphate N-acetylmuramic acid (UDP-MurNAc)-D,L-diaminopimelate (DAP)-pentapeptide. Most Gram-negative bacteria, including cyanobacteria, incorporate meso-diaminopimelic acid (D,L-DAP) into the third residue of the stem peptide of peptidoglycan, as opposed to L-lysine, typical of most Gram-positive bacteria. To establish the specificity of D,L-DAP incorporation into the P. patens precursors, we analyzed the recombinant protein UDP-N-acetylmuramoyl-L-alanyl-D-glutamate–2,6-diaminopimelate ligase (MurE) from both P. patens and the cyanobacterium Anabaena sp. (Nostoc sp. strain PCC 7120). Both ligases incorporated D,L-DAP in almost complete preference to L-Lys, consistent with the mass spectrophotometric data, with catalytic efficiencies similar to previously documented Gram-negative bacterial MurE ligases. We discuss how these data accord with the conservation of active site residues common to DL-DAP-incorporating bacterial MurE ligases and of the probability of a horizontal gene transfer event within the plant peptidoglycan pathway.

Item Type: Journal Article
Subjects: Q Science > QK Botany
Q Science > QP Physiology
Q Science > QR Microbiology
Divisions: Faculty of Science, Engineering and Medicine > Science > Life Sciences (2010- )
Library of Congress Subject Headings (LCSH): Physcomitrella patens, Peptidoglycans, Chloroplasts, Gram-negative bacteria
Journal or Publication Title: Plant Physiology
Publisher: Oxford University Press
ISSN: 1532-2548
Official Date: September 2022
Dates:
DateEvent
September 2022Published
25 May 2022Available
6 March 2022Accepted
5 January 2022Submitted
Volume: 190
Number: 1
Page Range: pp. 165-179
DOI: 10.1093/plphys/kiac176
Status: Peer Reviewed
Publication Status: Published
Access rights to Published version: Open Access (Creative Commons)
Date of first compliant deposit: 13 July 2022
Date of first compliant Open Access: 13 July 2022
RIOXX Funder/Project Grant:
Project/Grant IDRIOXX Funder NameFunder ID
MR/N002679/1UK Research and Innovationhttp://dx.doi.org/10.13039/100014013
MR/S014934/1UK Research and Innovationhttp://dx.doi.org/10.13039/100014013
72691[EPSRC] Engineering and Physical Sciences Research Councilhttp://dx.doi.org/10.13039/501100000266
UNSPECIFIEDUniversity of Warwickhttp://dx.doi.org/10.13039/501100000741

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