FurC (PerR) contributes to the regulation of peptidoglycan remodeling and intercellular molecular transfer in the cyanobacterium
Anabaena
sp. strain PCC 7120
Authors: Sarasa-Buisan Cristina , Nieves-Morión Mercedes , Arévalo Sergio , Helm Richard F. , Sevilla Emma , Luque Ignacio , Fillat María F. 
Published: February 2024

ABSTRACT

Microbial extracellular proteins and metabolites provide valuable information concerning how microbes adapt to changing environments. In cyanobacteria, dynamic acclimation strategies involve a variety of regulatory mechanisms, being ferric uptake regulator proteins as key players in this process. In the nitrogen-fixing cyanobacterium
Anabaena
sp. strain PCC 7120, FurC (PerR) is a global regulator that modulates the peroxide response and several genes involved in photosynthesis and nitrogen metabolism. To investigate the possible role of FurC in shaping the extracellular environment of
Anabaena
, the analysis of the extracellular metabolites and proteins of a
furC
-overexpressing variant was compared to that of the wild-type strain. There were 96 differentially abundant proteins, 78 of which were found for the first time in the extracellular fraction of
Anabaena
. While these proteins belong to different functional categories, most of them are predicted to be secreted or have a peripheral location. Several stress-related proteins, including PrxA, flavodoxin, and the Dps homolog All1173, accumulated in the exoproteome of
furC
-overexpressing cells, while decreased levels of FurA and a subset of membrane proteins, including several export proteins and
amiC
gene products, responsible for nanopore formation, were detected. Direct repression by FurC of some of those genes, including
amiC1
and
amiC2,
could account for odd septal nanopore formation and impaired intercellular molecular transfer observed in the
furC
-overexpressing variant. Assessment of the exometabolome from both strains revealed the release of two peptidoglycan fragments in
furC
-overexpressing cells, namely 1,6-anhydro-N-acetyl-β-D-muramic acid (anhydroMurNAc) and its associated disaccharide (β-D-GlcNAc-(1-4)-anhydroMurNAc), suggesting alterations in peptidoglycan breakdown and recycling.

IMPORTANCE

Cyanobacteria are ubiquitous photosynthetic prokaryotes that can adapt to environmental stresses by modulating their extracellular contents. Measurements of the organization and composition of the extracellular milieu provide useful information about cyanobacterial adaptive processes, which can potentially lead to biomimetic approaches to stabilizing biological systems to adverse conditions.
Anabaena
sp. strain PCC 7120 is a multicellular, nitrogen-fixing cyanobacterium whose intercellular molecular exchange is mediated by septal junctions that traverse the septal peptidoglycan through nanopores. FurC (PerR) is an essential transcriptional regulator in
Anabaena
, which modulates the response to several stresses. Here, we show that
furC
-overexpressing cells result in a modified exoproteome and the release of peptidoglycan fragments. Phenotypically, important alterations in nanopore formation and cell-to-cell communication were observed. Our results expand the roles of FurC to the modulation of cell-wall biogenesis and recycling, as well as in intercellular molecular transfer.