Abstract:
The signaling transduction proteins of the PII superfamily, such as the PII-like protein SbtB,
represent an ancient and exceptionally well-preserved protein family ubiquitously across all
domains of life. Within cyanobacteria, SbtB serves as the main regulator of the carbon
concentrating mechanism (CCM) and inorganic carbon (Ci) acclimation and is co-expressed
from a bicistronic operon with the sodium-dependent bicarbonate transporter (SbtA). SbtB
regulates bicarbonate uptake by direct interaction with all three cyanobacterial bicarbonate
transporters: SbtA, BicA, and BCT1, in response to fluctuations in Ci levels and the adenylate
energy charge (AEC). This study proposes a novel model for SbtB-mediated regulation of SbtA,
emphasizing the significance of the flexible SbtB T-loop structure for this interaction, akin to
the canonical PII T-loop in target protein interactions. In the AMP-bound state, corresponding
to low Ci (LC) supply, SbtB inserts its T-loop into the inter-domain cleft of SbtA, inducing an
inward-open conformation that facilitates substrate secretion into the cytoplasm while
inhibiting backward bicarbonate transport. However, the cellular function of SbtB extends
beyond bicarbonate uptake, significantly impacting central carbon metabolism and Ci
acclimation. In the absence of SbtB in the slr1513 knockout mutant (ΔsbtB), CCM-associated
gene expression, including the master Ci acclimation regulator NdhR, is broadly affected,
resulting in a constitutively LC pre-acclimated state.
In Synechocystis sp. PCC 6803, SbtB has been identified as the primary receptor of the
second messenger, c-di-AMP. The SbtB:c-di-AMP complex regulates glycogen synthesis
through its interaction with the glycogen branching enzyme (GlgB), which is essential for
nighttime cyanobacterial survival.
While SbtB primarily influences cellular functions related to the central carbon metabolism,
c-di-AMP plays a multifaceted role in governing various cellular processes. These encompass
the maintenance of ion homeostasis, notably K+
, Na+
, and Mg2+, thus regulating
osmoprotection. C-di-AMP also exerts control over the central nitrogen metabolism, either
directly or indirectly, by modulating the expression of NtcA, which in turn impacts on the
process of chlorosis. Additionally, c-di-AMP plays a pivotal role in regulating the uptake of
glutamine by regulating the activity of the basic amino acid and glutamine transporter complex
BgtAB. Moreover, it is indispensable for facilitating chromatic acclimation by influencing the
expression of CpcL through Rbp2.
Carbon Concentrating Mechanism