Affiliation:
1. Department of Microbiology, University of Hawaii, Honolulu, Hawaii, USA
2. Department of Pharmaceutical Sciences, College of Pharmacy, Oregon State University, Corvallis, Oregon, USA
3. Department of Biology, Illinois Wesleyan University, Bloomington, Illinois, USA
Abstract
ABSTRACT
To stabilize cellular integrity in the face of environmental perturbations, most bacteria, including cyanobacteria, synthesize and maintain a strong, flexible, three-dimensional peptidoglycan lattice.
Anabaena
sp. strain PCC 7120 is a filamentous cyanobacterium capable of differentiating morphologically distinct nitrogen-fixing heterocyst cells in a periodic pattern. While heterocyst development has been shown to require proper peptidoglycan remodeling, the role of peptidoglycan synthesis has remained unclear. Here we report the identification of two peptidoglycan synthesis genes,
murC
(
alr5065
) and
murB
(
alr5066
), as required for heterocyst development. The
murC
and
murB
genes are predicted to encode a UDP-
N
-acetylmuramate:
l
-alanine ligase and a UDP-
N
-acetylenolpyruvoylglucosamine reductase, respectively, and we confirm enzymatic function through complementation of
Escherichia coli
strains deficient for these enzymes. Cells depleted of either
murC
or
murB
expression failed to differentiate heterocysts under normally inducing conditions and displayed decreased filament integrity. To identify the stage(s) of development affected by
murC
or
murB
depletion, the spatial distribution of expression of the patterning marker gene,
patS
, was examined. Whereas
murB
depletion did not affect the pattern of
patS
expression,
murC
depletion led to aberrant expression of
patS
in all cells of the filament. Finally, expression of
gfp
controlled by the region of DNA immediately upstream of
murC
was enriched in differentiating cells and was repressed by the transcription factor NtcA. Collectively, the data in this work provide evidence for a direct link between peptidoglycan synthesis and the maintenance of a biological pattern in a multicellular organism.
IMPORTANCE
Multicellular organisms that differentiate specialized cells must regulate morphological changes such that both cellular integrity and the dissemination of developmental signals are preserved. Here we show that the multicellular bacterium
Anabaena
, which differentiates a periodic pattern of specialized heterocyst cells, requires peptidoglycan synthesis by the murine ligase genes
murC
(
alr5065
) and
murB
(
alr5066
) for maintenance of patterned gene expression, filament integrity, and overall development. This work highlights the significant influence that intracellular structure and intercellular connections can have on the execution of a developmental program.
Funder
Illinois Wesleyan University
Oregon State University
Publisher
American Society for Microbiology
Subject
Molecular Biology,Microbiology
Cited by
11 articles.
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